Connecting alveolate cell biology with trophic ecology in the marine plankton using the ciliate Favella as a model

Hydrodynamic signals from turbulence and waves may provide marine invertebrate larvae with behavioral cues that affect the pathways and energetic costs of larval delivery to adult habitats. Oysters (Crassostrea virginica) live in sheltered estuaries with strong turbulence and small waves, but their larvae can be transported into coastal waters with large waves. These contrasting environments have different ranges of hydrodynamic signals, because turbulence generally produces higher spatial velocity gradients, whereas waves can produce higher temporal velocity gradients. To understand how physical processes affect oyster larval behavior, transport and energetics, we exposed larvae to different combinations of turbulence and waves in flow tanks with (1) wavy turbulence, (2) a seiche and (3) rectilinear accelerations. We quantified behavioral responses of individual larvae to local instantaneous flows using twophase, infrared particle-image velocimetry. Both high dissipation rates and high wave-generated accelerations induced most larvae to swim faster upward. High dissipation rates also induced some rapid, active dives, whereas high accelerations induced only weak active dives. In both turbulence and waves, faster swimming and active diving were achieved through an increase in propulsive force and power output that would carry a high energetic cost. Swimming costs could be offset if larvae reaching surface waters had a higher probability of being transported shoreward by Stokes drift, whereas diving costs could be offset by enhanced settlement or predator avoidance. These complex behaviors suggest that larvae integrate multiple hydrodynamic signals to manage dispersal tradeoffs, spending more energy to raise the probability of successful transport to suitable locations.

Section: Aggregated Behavior Observationsmentioning

confidence: 99%

Hydrodynamic sensing and behavior by oyster larvae in turbulence and waves

Fuchs

Gerbi

Hunter

et al. 2015

“…The statocysts' dual sensing mechanism sets oyster larvae apart from plankton that sense spatial velocity gradients using external mechanoreceptors. Many copepods and ciliates sense mechanical deformations using antennae or membrane receptors, respectively (Naitoh and Eckert, 1969;Strickler and Bal, 1973;Yen et al, 1992;Echevarria et al, 2014), and they respond to strains with rapid jumps, which enable escape from predator-generated feeding currents (Kiørboe et al, 1999;Jakobsen, 2001). Some feeding currents generate both high strains and high accelerations (Higham et al, 2006;Holzman et al, 2008), yet few plankton react to accelerations (e.g.…”

Section: Discussionmentioning

confidence: 99%

Directional flow sensing by passively stable larvae

Fuchs

Christman

Gerbi

et al. 2015

Mollusk larvae have a stable, velum-up orientation that may influence how they sense and react to hydrodynamic signals applied in different directions. Directional sensing abilities and responses could affect how a larva interacts with anisotropic fluid motions, including those in feeding currents and in boundary layers encountered during settlement. Oyster larvae (Crassostrea virginica) were exposed to simple shear in a Couette device and to solid-body rotation in a single rotating cylinder. Both devices were operated in two different orientations, one with the axis of rotation parallel to the gravity vector, and one with the axis perpendicular. Larvae and flow were observed simultaneously with near-infrared particle-image velocimetry, and behavior was quantified as a response to strain rate, vorticity and centripetal acceleration. Only flows rotating about a horizontal axis elicited the diving response observed previously for oyster larvae in turbulence. The results provide strong evidence that the turbulence-sensing mechanism relies on gravity-detecting organs (statocysts) rather than mechanosensors (cilia). Flow sensing with statocysts sets oyster larvae apart from zooplankters such as copepods and protists that use external mechanosensors in sensing spatial velocity gradients generated by prey or predators. Sensing flow-induced changes in orientation, rather than flow deformation, would enable more efficient control of vertical movements. Statocysts provide larvae with a mechanism of maintaining their upward swimming when rotated by vortices and initiating dives toward the seabed in response to the strong turbulence associated with adult habitats.

“…As with RDs, the involvement of voltagegated channels in mediating MSDs in Favella sp. is suggested by the fact that transient depolarizations and reversals may be elicited by the injection of positive current (Echevarria et al, 2014).…”

Section: +mentioning

confidence: 99%

“…G-protein coupled receptor (GPCR) pathways may be important in linking these signal transduction mechanisms (Echevarria et al, 2014). GPCR signaling pathways are crucial for chemosensation of prey in ciliates, as demonstrated in experiments with the marine ciliate Uronema sp., where chemosensory responses to prey were decreased by application of pharmacological compounds that inhibited the GPCR signal transduction pathway (Hartz et al, 2008).…”

Section: +mentioning

confidence: 99%

“…(Fig. 1A) is a cosmopolitan member of the plankton community that has well-described trophic behaviors (Stoecker and Sanders, 1985;Stoecker, 1988, 1989;Taniguchi and Takeda, 1988;Stoecker et al, 1995Stoecker et al, , 2013Strom et al, 2007) and has morphological and behavioral characteristics that are representative of marine planktonic ciliates; they are therefore an excellent model for studying the sensory mechanisms underlying the trophic ecology of marine alveolate grazers (Montagnes, 2013;Echevarria et al, 2014). [Note: the genus Favella has been recently redescribed and some former Favella spp.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Feast or flee: bioelectrical regulation of feeding and predator evasion behaviors in the planktonic alveolateFavellasp. (Spirotrichia)

Echevarria

Wolfe

Taylor

2015

Self Cite

Alveolate (ciliates and dinoflagellates) grazers are integral components of the marine food web and must therefore be able to sense a range of mechanical and chemical signals produced by prey and predators, integrating them via signal transduction mechanisms to respond with effective prey capture and predator evasion behaviors. However, the sensory biology of alveolate grazers is poorly understood. Using novel techniques that combine electrophysiological measurements and high-speed videomicroscopy, we investigated the sensory biology of Favella sp., a model alveolate grazer, in the context of its trophic ecology. Favella sp. produced frequent rhythmic depolarizations (∼500 ms long) that caused backward swimming and are responsible for endogenous swimming patterns relevant to foraging. Contact of both prey cells and non-prey polystyrene microspheres at the cilia produced immediate mechanostimulated depolarizations (∼500 ms long) that caused backward swimming, and likely underlie aggregative swimming patterns of Favella sp. in response to patches of prey. Contact of particles at the peristomal cavity that were not suitable for ingestion resulted in depolarizations after a lag of ∼600 ms, allowing time for particles to be processed before rejection. Ingestion of preferred prey particles was accompanied by transient hyperpolarizations (∼1 s) that likely regulate this step of the feeding process. Predation attempts by the copepod Acartia tonsa elicited fast (∼20 ms) animal-like action potentials accompanied by rapid contraction of the cell to avoid predation. We have shown that the sensory mechanisms of Favella sp. are finely tuned to the type, location, and intensity of stimuli from prey and predators.