Heidi L. Fuchs

Active downward propulsion by oyster larvae in turbulence.

SUMMARY Oyster larvae (Crassostrea virginica) could enhance their settlement success by moving toward the seafloor in the strong turbulence associated with coastal habitats. We characterized the behavior of individual oyster larvae in grid-generated turbulence by measuring larval velocities and flow velocities simultaneously using infrared particle image velocimetry. We estimated larval behavioral velocities and propulsive forces as functions of the kinetic energy dissipation rate ε, strain rate γ, vorticity ξ and acceleration α. In calm water most larvae had near-zero vertical velocities despite propelling themselves upward (swimming). In stronger turbulence all larvae used more propulsive force, but relative to the larval axis, larvae propelled themselves downward (diving) instead of upward more frequently and more forcefully. Vertical velocity magnitudes of both swimmers and divers increased with turbulence, but the swimming velocity leveled off as larvae were rotated away from their stable, velum-up orientation in strong turbulence. Diving speeds rose steadily with turbulence intensity to several times the terminal fall velocity in still water. Rapid dives may require a switch from ciliary swimming to another propulsive mode such as flapping the velum, which would become energetically efficient at the intermediate Reynolds numbers attained by larvae in strong turbulence. We expected larvae to respond to spatial or temporal velocity gradients, but although the diving frequency changed abruptly at a threshold acceleration, the variation in propulsive force and behavioral velocity was best explained by the dissipation rate. Downward propulsion could enhance oyster larval settlement by raising the probability of larval contact with oyster reef patches.

Larval responses to turbulence and temperature in a tidal inlet: Habitat selection by dispersing gastropods?

Author Posting.

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 two-phase, 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. Summary: Turbulence and waves induce oyster larvae to swim faster upward or to dive. These behaviors are energetically costly but could reduce predation mortality and enhance larval delivery to adult habitats.

Biophysical Constraints on Optimal Patch Lengths for Settlement of a Reef-Building Bivalve

Reef-building species form discrete patches atop soft sediments, and reef restoration often involves depositing solid material as a substrate for larval settlement and growth. There have been few theoretical efforts to optimize the physical characteristics of a restored reef patch to achieve high recruitment rates. The delivery of competent larvae to a reef patch is influenced by larval behavior and by physical habitat characteristics such as substrate roughness, patch length, current speed, and water depth. We used a spatial model, the “hitting-distance” model, to identify habitat characteristics that will jointly maximize both the settlement probability and the density of recruits on an oyster reef (Crassostrea virginica). Modeled larval behaviors were based on laboratory observations and included turbulence-induced diving, turbulence-induced passive sinking, and neutral buoyancy. Profiles of currents and turbulence were based on velocity profiles measured in coastal Virginia over four different substrates: natural oyster reefs, mud, and deposited oyster and whelk shell. Settlement probabilities were higher on larger patches, whereas average settler densities were higher on smaller patches. Larvae settled most successfully and had the smallest optimal patch length when diving over rough substrates in shallow water. Water depth was the greatest source of variability, followed by larval behavior, substrate roughness, and tidal current speed. This result suggests that the best way to maximize settlement on restored reefs is to construct patches of optimal length for the water depth, whereas substrate type is less important than expected. Although physical patch characteristics are easy to measure, uncertainty about larval behavior remains an obstacle for predicting settlement patterns. The mechanistic approach presented here could be combined with a spatially explicit metapopulation model to optimize the arrangement of reef patches in an estuary or region for greater sustainability of restored habitats.

Swimming behavior and velocities of barnacle cyprids in a downwelling flume

It has been proposed that barnacle cyprids can maintain position in shoreward- propagating fronts by swimming upward against a downwelling flow, potentially mediating onshore transport of larvae toward intertidal habitat. This study developed a novel flume to characterize swimming behavior of barnacle cyprids in a laboratory downwelling flow. Seawater was pumped through a cylindrical observation chamber fitted with diffusers to produce a homogeneous down- welling velocity field. The flume generated plug flow with mean downwelling velocities (indicated by negative sign) of 0 to -47.3 mm s -1 . Behavior experiments were done with wild Semibalanus bal- anoides cyprids. Vertical swimming rates and behaviors were estimated from video observations, and a mixture model was used to estimate velocity distributions for distinct behavioral modes. Larvae exhibited multiple behaviors but typically swam upward in response to downwelling, with a maxi- mum estimated vertical velocity of 72.3 mm s -1 . When faced with downwelling flows, cyprids alter- nated between upward swimming and downward swimming to maintain their vertical position in the chamber. As downwelling velocities increased, cyprids that remained in the field of view of the cam- eras exhibited faster mean upward swimming velocities. It is unclear how long individual S. bal- anoides cyprids can maintain depth, but cyprids were able to maintain depth throughout the 2 min observation period. This study supports earlier hypotheses based on field observations by demon- strating that S. balanoides cyprids swim well enough to counter downwelling velocities characteris- tic of convergence zones. Swimming against downwelling flow could be an adaptive behavior that enables shoreward transport in the absence of any larval ability to swim toward shore or even to sense its direction.

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. Summary: Oyster larvae exhibit behavioral responses to flow-induced rotation of the body relative to gravity; in turbulence, these responses will enhance control of vertical motion.

Waves cue distinct behaviors and differentiate transport of congeneric snail larvae from sheltered versus wavy habitats

Significance Many marine populations grow and spread via larvae that disperse in ocean currents. Larvae can alter their physical transport by swimming vertically or sinking in response to environmental signals. However, it remains unknown whether any signals could enable larvae to navigate over large scales. We studied larval responses to water motions in closely related snails, one from turbulent coastal inlets and one from the wavy continental shelf. These two species reacted similarly to turbulence but differently to waves, causing their transport patterns to diverge in wavy, offshore regions. Contrasting responses to waves could enable these similar species to maintain separate spatial distributions. Wave-induced behaviors provide evidence that larvae may detect waves as both motions and sounds useful in navigation. Marine population dynamics often depend on dispersal of larvae with infinitesimal odds of survival, creating selective pressure for larval behaviors that enhance transport to suitable habitats. One intriguing possibility is that larvae navigate using physical signals dominating their natal environments. We tested whether flow-induced larval behaviors vary with adults’ physical environments, using congeneric snail larvae from the wavy continental shelf (Tritia trivittata) and from turbulent inlets (Tritia obsoleta). Turbulence and flow rotation (vorticity) induced both species to swim more energetically and descend more frequently. Accelerations, the strongest signal from waves, induced a dramatic response in T. trivittata but almost no response in competent T. obsoleta. Early stage T. obsoleta did react to accelerations, ruling out differences in sensory capacities. Larvae likely distinguished turbulent vortices from wave oscillations using statocysts. Statocysts’ ability to sense acceleration would also enable detection of low-frequency sound from wind and waves. T. trivittata potentially hear and react to waves that provide a clear signal over the continental shelf, whereas T. obsoleta effectively “go deaf” to wave motions that are weak in inlets. Their contrasting responses to waves would cause these larvae to move in opposite directions in the water columns of their respective adult habitats. Simulations showed that the congeners’ transport patterns would diverge over the shelf, potentially reinforcing the separate biogeographic ranges of these otherwise similar species. Responses to turbulence could enhance settlement but are unlikely to aid large-scale navigation, whereas shelf species’ responses to waves may aid retention over the shelf via Stokes drift.

Biophysical coupling between turbulence, veliger behavior, and larval supply

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 2005