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

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.

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

Planktotrophic invertebrate larvae require energy to develop, disperse and settle successfully, and it is unknown how their energetics are impacted by turbulence. Ciliated larvae gain metabolic energy from their phytoplankton food to offset the energetic costs of growth, development and ciliary activity for swimming and feeding. Turbulence may affect the energetic balance by inducing behaviors that alter the metabolic costs and efficiency of swimming, by raising the encounter rate with food particles and by inhibiting food capture. We used experiments and an empirical model to quantify the net rate of energy gain, swimming efficiency and food capture efficiency for eyed oyster larvae (Crassostrea virginica) in turbulence. At dissipation rates representative of coastal waters, larvae lost energy even when food concentrations were very high. Both feeding activity and turbulence-induced behaviors incurred high metabolic costs. Swimming efficiency was concave up versus dissipation rate, suggesting that ciliary activity for food handling became more costly while swimming became more efficient with turbulence intensity. Though counter-intuitive, swimming may have become more efficient in turbulence because vorticity-induced rotation caused larvae to swim more horizontally, which requires less effort than swimming vertically against the pull of gravity. Overall, however, larvae failed to offset high activity costs with food energy gains because turbulence reduced food capture efficiency more than it enhanced food encounter rates. Younger, smaller larvae may have some energetic advantages, but competent larvae would lose energy at turbulence intensities they experience frequently, suggesting that turbulence-induced starvation may account for much of oysters' high larval mortality.

Directional flow sensing by passively stable larvae.

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.

Directional flow sensing by passively stable larvae.

Mollusc 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 behaviors were 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.

Hydrodynamic sensing and behavior by oyster larvae in turbulence and waves.

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.

Active downward propulsion by oyster larvae in turbulence.

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.

Adsorptive exchange of coccolith biominerals facilitates viral infection.

Marine coccolithophores are globally distributed, unicellular phytoplankton that produce nanopatterned, calcite biominerals (coccoliths). These biominerals are synthesized internally, deposited into an extracellular coccosphere, and routinely released into the external medium, where they profoundly affect the global carbon cycle. The cellular costs and benefits of calcification remain unresolved. Here, we show observational and experimental evidence, supported by biophysical modeling, that free coccoliths are highly adsorptive biominerals that readily interact with cells to form chimeric coccospheres and with viruses to form "viroliths," which facilitate infection. Adsorption to cells is mediated by organic matter associated with the coccolith base plate and varies with biomineral morphology. Biomineral hitchhiking increases host-virus encounters by nearly an order of magnitude and can be the dominant mode of infection under stormy conditions, fundamentally altering how we view biomineral-cell-virus interactions in the environment.

Temperate infection in a virus-host system previously known for virulent dynamics.

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus-host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host-virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host-virus densities.

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.