Feeding in the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms

Roberts, Edward; Wootton, Emma C.; Davidson, Keith; Jeong, Hae Jin; Lowe, Christopher D.; Montagnes, David J. S.

doi:10.1093/plankt/fbq118

Cited by 76 publications

(70 citation statements)

References 92 publications

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“…Chemical recognition of prey has been well described for heterotrophic protists (reviewed in Roberts et al 2011). Chemical cues from potential algal prey can provide cues on prey presence and spatially directed information on food distribution and quality for potential consumers (Larsson and Dodson 1993).…”

Section: Discussionmentioning

confidence: 99%

Avoidance and attraction: Chemical cues influence predator‐prey interactions of planktonic protists

Harvey

Jeong

Menden‐Deuer

2013

Limnology & Oceanography

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We measured how predator-and prey-derived chemical cues affect swimming behaviors and encounter rates of two common phytoplankton species (Amphidinum carterae, Heterosigma akashiwo) and two heterotrophic dinoflagellate predators (Stoeckeria algicida, Gyrodiniellum shiwhaense). Using video and image analysis, the microscopic three-dimensional movement behaviors and macroscopic population distributions of the species were quantified in response to chemical cues derived from their respective predator or prey species. S. algicida preferentially feeds on H. akashiwo but displayed significant increases in swimming speed and turning rate when exposed to filtrate from either prey species. Prey cue-induced changes in predator swimming behavior resulted in an average 11% increase in encounter rate. S. algicida that respond to prey filtrate would reach their daily prey quota at a 25% lower ambient prey concentration. In contrast, G. shiwhaense, which rarely feeds and does not grow on H. akashiwo, exhibited no shifts in behavior in response to algal filtrate. Predator-derived cues from S. algicida elicited significant increases in upward motility in H. akashiwo, resulting in a shift in the prey population abundance away from the predator-derived chemical cue. These algal fleeing behaviors reduced estimated encounter rates by 4%, compared to non-fleeing behaviors. Our results provide quantitative evidence for the importance of chemical cues in modulating feeding interactions and emphasize the ramifications of individual behaviors, and modulation thereof, to population-level outcomes, including population distributions, and predation pressure.

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Section: Discussionmentioning

confidence: 99%

Avoidance and attraction: Chemical cues influence predator‐prey interactions of planktonic protists

Harvey

Jeong

Menden‐Deuer

2013

Limnology & Oceanography

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“…Cell size and grazing pressure. Protist prey selection may occur at various feeding steps, namely, capture, prey processing, ingestion, and digestion (11,43). Prey size is a trait that is easy to measure.…”

Section: Discussionmentioning

confidence: 99%

Some Mixotrophic Flagellate Species Selectively Graze on Archaea

Ballen-Segura

Felip

Catalan

2017

Appl Environ Microbiol

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Many phototrophic flagellates ingest prokaryotes. This mixotrophic trait becomes a critical aspect of the microbial loop in planktonic food webs because of the typical high abundance of these flagellates. Our knowledge of their selective feeding upon different groups of prokaryotes, particularly under field conditions, is still quite limited. In this study, we investigated the feeding behavior of three species (Rhodomonas sp., Cryptomonas ovata, and Dinobryon cylindricum) via their food vacuole content in field populations of a high mountain lake. We used the catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) protocol with probes specific for the domain Archaea and three groups of Eubacteria: Betaproteobacteria, Actinobacteria, and Cytophaga-Flavobacteria of Bacteroidetes. Our results provide field evidence that contrasting selective feeding exists between coexisting mixotrophic flagellates under the same environmental conditions and that some prokaryotic groups may be preferentially impacted by phagotrophic pressure in aquatic microbial food webs. In our study, Archaea were the preferred prey, chiefly in the case of Rhodomonas sp., which rarely fed on any other prokaryotic group. In general, prey selection did not relate to prey size among the grazed groups. However, Actinobacteria, which were clearly avoided, mostly showed a size of Ͻ0.5 m, markedly smaller than cells from the other groups.IMPORTANCE That mixotrophic flagellates are not randomly feeding in the main prokaryotic groups under field conditions is a pioneer finding in species-specific behavior that paves the way for future studies according to this new paradigm. The particular case that Archaea were preferentially affected in the situation studied shows that phagotrophic pressure cannot be disregarded when considering the distribution of this group in freshwater oligotrophic systems.KEYWORDS Archaea, mixotrophic protist, selective feeding M ixotrophic behavior, the combination of phototrophic and phagotrophic nutritional modes within a single cell, has been increasingly documented in aquatic systems (1, 2). Phagotrophy occurs in a variety of phytoplankton flagellate groups, including Chrysophyceae, dinoflagellates, prymnesiophytes, and cryptophytes, which comprise some picoeukaryotes (3-5). Currently, there is no doubt of the ubiquity of mixotrophy and its significance in the functioning of planktonic systems. Under oligotrophic conditions, phototrophic flagellates can account for up to 80% of total bacterial grazing (4,6,7).Predation by protists is among the primary mortality factors of prokaryotes in planktonic communities and thus is an important selective pressure. It becomes a structuring factor of the abundance, morphology, composition, and activity of bacterial assemblages (8, 9). The impact of protist predation appears to be modulated by the characteristics of the system (e.g., productivity) and predator and prey traits (10). Over

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“…O. marina and the dinoflagellates with an equatorial transverse flagellum do, as hypothesized, push water in front as they swim. This would mean reduced prey encounter rates, but these dinoflagellates create a feeding current that transports prey particles to the sulcus area, co-occurring with the site of prey capture and engulfment (Hansen and Calado, 1999;Roberts et al, 2011). Dinoflagellates with an anterior transverse flagellum do not push water in front of the swimming cell; instead, a feeding current directs prey toward the entire anterior part of the dinoflagellate.…”

Section: Discussionmentioning

confidence: 99%

“…For O. marina, data comprised sources collected by Roberts et al (2011), and for G. dominans those collected by Lee et al (2014) supplemented by the study of Yoo et al (2010). Where clearance rates were not explicitly given, these were calculated as the initial slope of ingestion vs prey concentration curves.…”

Section: Flow Fields Around Swimming Microorganismsmentioning

confidence: 99%

Feeding currents facilitate a mixotrophic way of life

Nielsen

Kiørboe

2015

The ISME Journal

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Mixotrophy is common, if not dominant, among eukaryotic flagellates, and these organisms have to both acquire inorganic nutrients and capture particulate food. Diffusion limitation favors small cell size for nutrient acquisition, whereas large cell size facilitates prey interception because of viscosity, and hence intermediately sized mixotrophic dinoflagellates are simultaneously constrained by diffusion and viscosity. Advection may help relax both constraints. We use high-speed video microscopy to describe prey interception and capture, and micro particle image velocimetry (micro-PIV) to quantify the flow fields produced by free-swimming dinoflagellates. We provide the first complete flow fields of free-swimming interception feeders, and demonstrate the use of feeding currents. These are directed toward the prey capture area, the position varying between the seven dinoflagellate species studied, and we argue that this efficiently allows the grazer to approach small-sized prey despite viscosity. Measured flow fields predict the magnitude of observed clearance rates. The fluid deformation created by swimming dinoflagellates may be detected by evasive prey, but the magnitude of flow deformation in the feeding current varies widely between species and depends on the position of the transverse flagellum. We also use the near-cell flow fields to calculate nutrient transport to swimming cells and find that feeding currents may enhance nutrient uptake by E75% compared with that by diffusion alone. We argue that all phagotrophic microorganisms must have developed adaptations to counter viscosity in order to allow prey interception, and conclude that the flow fields created by the beating flagella in dinoflagellates are key to the success of these mixotrophic organisms.

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Feeding in the dinoflagellate Oxyrrhis marina: linking behaviour with mechanisms

Cited by 76 publications

References 92 publications

Avoidance and attraction: Chemical cues influence predator‐prey interactions of planktonic protists

Avoidance and attraction: Chemical cues influence predator‐prey interactions of planktonic protists

Some Mixotrophic Flagellate Species Selectively Graze on Archaea

Feeding currents facilitate a mixotrophic way of life

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