Directional flow sensing by passively stable larvae

Abstract

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.

Turbulence induces metabolically costly behaviors and inhibits food capture in oyster larvae, causing net energy loss

“…was ∼20% lower than would be expected in isotropic turbulence at the observed dissipation rates (Taylor, 1935;Fuchs and Gerbi, 2016). Vorticity is the likely cue for behavioral responses to turbulence (Fuchs et al, 2015a), so reduced vorticity may have induced weaker or less frequent reactions to turbulence than previously observed.…”

“…Competent larvae responded to turbulence by swimming with more effort, incurring high activity costs, while their food capture was impeded by increased speed relative to particles and/or erosion of feeding currents by eddy motions. Pre-competent larvae may have lower activity costs in turbulence because they lack statocyststhe probable mechanism for sensing fluid motion (Fuchs et al, 2015a)until the pediveliger stage (Ellis and Kempf, 2011) and should be unreactive to turbulence, incurring no extra swimming costs. Precompetent larvae are also smaller relative to the Kolmogorov scale and may have a size refuge from erosion of feeding currents.…”

“…We investigated how turbulence affects energetics of larval oysters, Crassostrea virginica Gmelin 1791. In turbulence, oyster larvae react primarily to fluid rotation (vorticity), sensed using simple gravity-detecting organs (statocysts; Fuchs et al, 2015a). Turbulence induces oyster larvae to swim more strongly upward and to dive downward with greater frequency and effort (Wheeler et al, 2013;Fuchs et al, , 2015a.…”

“…In turbulence, oyster larvae react primarily to fluid rotation (vorticity), sensed using simple gravity-detecting organs (statocysts; Fuchs et al, 2015a). Turbulence induces oyster larvae to swim more strongly upward and to dive downward with greater frequency and effort (Wheeler et al, 2013;Fuchs et al, , 2015a. These flow-induced behaviors will raise the metabolic cost of swimming, but by how much depends on the unknown swimming efficiency.…”

Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour

“…Such responses usually involve vertical movements in the water column to enter or exit particular flows [273]. For example, different mollusc larvae can either sink, or actively swim downwards or upwards in response to different flow environments [270,[274][275][276][277][278][279]. Arthropod larvae also swim upwards in response to increased turbulence [280].…”