Hydrodynamic sensing and behavior by oyster larvae in turbulence and waves

Abstract

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.

Behavioral responses of invertebrate larvae to water column cues

“…Various studies highlight that larvae actively respond to turbulence or components of turbulence, e.g., larval boat snails Crepidula fornicata increase upward swimming with increasing turbulence level [67], larval sea slugs Phestilla sibogae retract their vela when encountering turbulent filaments containing chemical cues [48], and larval eastern oysters Crassostrea virginica dive when experiencing high fluid acceleration over short time intervals [29]. Together with other modeling studies, these earlier works suggest turbulence enhances larval settlement [68,56] (but see [69], who suggested that an increase in turbulence reduces settlement in scallop larvae). Recently, deformation associated with horizontal shear has been suggested to induce competency in larval urchins [70] and to induce cloning in coral larvae [71].…”

“…In the water column, strong swimming larvae such as crab zoea actively change their swimming speeds in response to turbulence intensity [54] and barnacle cyprids swim upwards to counteract downwelling currents [55]. For moderate swimming larvae such as oyster larvae, a plasticity in response to turbulence has been observed, where competentto-settle larvae have been observed both to sink [27] and swim upward [56,28] in high turbulence; these active behavioral responses may be regulated by body size. For weaker swimming plankton, such as larval sand dollars, it has been observed that their morphologies primarily interact passively with ambient flow [57,46].…”

Directional flow sensing by passively stable larvae

“…Couette flow produces high strain rates and vorticity, whereas solid-body rotation produces negligible strain and constant vorticity. Rotating flows unavoidably produce centripetal acceleration, but here the accelerations were lower than those that previously induced larvae to dive in rectilinear wave motions (Fuchs et al, 2015). Each device was operated in two different orientations, one with its axis horizontal and one with its axis vertical (Figs 2,3).…”

“…1). Oyster larvae respond to both turbulence and waves by either swimming faster upward or diving actively downward (Fuchs et al, , 2015. In waves, these responses are elicited by high accelerations, indicating that statocysts can function as accelerometers (Fuchs et al, 2015).…”

“…Oyster larvae respond to both turbulence and waves by either swimming faster upward or diving actively downward (Fuchs et al, , 2015. In waves, these responses are elicited by high accelerations, indicating that statocysts can function as accelerometers (Fuchs et al, 2015). In turbulence, accelerations are generally smaller than those eliciting responses in waves, and larvae probably respond to strains or vorticity, both of which are highly correlated with the dissipation rate ε of turbulent kinetic energy (Tennekes and Lumley, 1972).…”