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.

Prey preferences of invasive (Hemigrapsus sanguineus, H. takanoi) and native (Carcinus maenas) intertidal crabs in the European Wadden Sea

Invasive predators can have wide-ranging effects on invaded ecosystems and identifying the prey spectra and preferences of invaders are important steps in assessing their potential impacts on native biota. In this study, we investigated prey preferences of two invasive crab species (Hemigrapsus sanguineus and Hemigrapsus takanoi) that recently invaded Europe's shores and compared them with preferences of native shore crabs (Carcinus maenas) of similar size. In laboratory experiments, all three crab species preferred animal over algal prey. In general, sessile mussels (Mytilus edulis) were preferred over motile amphipods (Gammarus locusta) by all three crab species but amphipod predation was lower in the invasive compared with the native crabs. For the two invasive crab species, this pattern was the same in treatments where prey was offered separately (no-choice treatments) or simultaneously (choice treatments), while for the native crabs, mussel preference disappeared in choice treatments. The general preference of mussels by all three crab species suggests that local invasions of crabs most likely lead to increased competition among crabs. In addition, given that local densities of invasive crabs are often much higher than those of native crabs, predation pressure on native mussels can be expected to strongly increase at invaded sites. In contrast, local predation pressure on amphipods may be less affected by the crab invasions. Further field studies are needed to establish the magnitude of competition and predation pressure exerted by the invaders under natural conditions.

Heterotrophic Dinoflagellate Growth and Grazing Rates Reduced by Microplastic Ingestion

Microplastics are ubiquitous contaminants in marine ecosystems worldwide, threatening fisheries production, food safety, and human health. Ingestion of microplastics by fish and large zooplankton has been documented, but there are few studies focusing on single-celled marine predators, including heterotrophic dinoflagellates. In laboratory experiments, the heterotrophic dinoflagellate species Oxyrrhis marina and Gyrodinium sp. readily ingested both algal prey and polystyrene microplastic spheres (2.5–4.5 μm), while Protoperidinium sp. did not ingest microplastics. Compared to algae-only fed dinoflagellates, those that ingested microplastics had growth rates reduced by 25–35% over the course of 5 days. Reduced growth resulted in a 30–50% reduction of secondary production as measured as predator biomass. Ingestion rates of algal prey were also reduced in the microplastic treatments. When given a mixture of microplastics and algal prey, O. marina displayed a higher selectivity for algal prey than Gyrodinium sp. Observations in the coastal ocean showed that phylogenetically diverse taxa ingested microplastic beads, and thus heterotrophic dinoflagellates could contribute to trophic transfer of microplastics to higher trophic levels. The results of this study may suggest that continued increase in microplastic pollution in the ocean could lead to reduced secondary production of heterotrophic protists due to microplastic ingestion, altering the flow of energy and matter in marine microbial food webs.

Dimethyl sulfide acts as eat-me signal during microbial predator-prey interactions in the ocean

Phytoplankton are key components of the oceanic carbon and sulfur cycles 1. During bloom events, some species can emit massive amounts of the organosulfur volatile dimethyl sulfide (DMS) to the atmosphere, where it can modulate aerosol formation and affect climate. In aquatic environments, DMS plays an important role as a chemical signal mediating diverse trophic-level interactions. Yet its role in microbial predator-prey interactions remains elusive with contradicting evidence for its role in algal chemical defense and in grazer’s chemoattraction to prey cells. Here, we investigated the signaling role of DMS during zooplankton-algae interactions by genetic and biochemical manipulation of the algal DMS-generating enzyme (Dimethylsulfoniopropionate lyase, DL) from the bloom-forming alga Emiliania huxleyi. We inhibited DL activity in live E. huxleyi cells by the novel DL-inhibitor 2-bromo-3-(dimethylsulfonio)-propionate (Br-DMSP) , and overexpressed DL in the model diatom Thalassiosira pseudonana. We showed that algal DL activity did not serve as anti-grazing chemical defense, and paradoxically enhanced grazing by the model microzooplankton Oxyrrhis marina and other micro- and mesozooplankton, including ciliates and copepods. Consumption of algal prey with induced DL activity also promoted O. marina’s growth. Overall, our results demonstrate that DMS-mediated herbivory may be ecologically important and prevalent during prey-predator dynamics in oceanic ecosystems. The role of DMS as an appetizing signal to grazers revealed here raises fundamental questions regarding the retention of its biosynthetic enzyme through the evolution of dominant bloom-forming phytoplankton in the ocean.

Large-scale ciliary reversal mediates capture of individual algal prey by Müller’s larva

We documented capture of microalgal prey by several species of wild-caught Müller’s larvae of polyclad flatworm. To our knowledge, this is the first direct observation of feeding mechanism in this classical larval type. High-speed video recordings show that virtually all captures are mediated by large-scale transient ciliary reversal over one or more portions of the main ciliary band corresponding to individual lobes or tentacles. Local ciliary beat reversals alter near-field flow to suck parcels of food-containing water mouthward. Many capture episodes entail sufficient coordinated flow disruption that these compact-bodied larvae tumble dramatically. Similar behaviors were recorded in at least four distinct species, one of which corresponds to the ascidian-eating polyclad Pseudoceros.

Space station image captures a red tide ciliate bloom at high spectral and spatial resolution

Mesodinium rubrum is a globally distributed nontoxic ciliate that is known to produce intense red-colored blooms using enslaved chloroplasts from its algal prey. Although frequent enough to have been observed by Darwin, blooms of M. rubrum are notoriously difficult to quantify because M. rubrum can aggregate into massive clouds of rusty-red water in a very short time due to its high growth rates and rapid swimming behavior and can disaggregate just as quickly by vertical or horizontal dispersion. A September 2012 hyperspectral image from the Hyperspectral Imager for the Coastal Ocean sensor aboard the International Space Station captured a dense red tide of M. rubrum (106 cells per liter) in surface waters of western Long Island Sound. Genetic data confirmed the identity of the chloroplast as a cryptophyte that was actively photosynthesizing. Microscopy indicated extremely high abundance of its yellow fluorescing signature pigment phycoerythrin. Spectral absorption and fluorescence features were related to ancillary photosynthetic pigments unique to this organism that cannot be observed with traditional satellites. Cell abundance was estimated at a resolution of 100 m using an algorithm based on the distinctive yellow fluorescence of phycoerythrin. Future development of hyperspectral satellites will allow for better enumeration of bloom-forming coastal plankton, the associated physical mechanisms, and contributions to marine productivity.