Responding to the signal and the noise: behavior of planktonic gastropod larvae in turbulence.

Swimming organisms may actively adjust their behavior in response to the flow around them. Ocean flows are typically turbulent and are therefore characterized by chaotic velocity fluctuations. While some studies have observed planktonic larvae altering their behavior in response to turbulence, it is not always clear whether a plankter is responding to an individual turbulence fluctuation or to the time-averaged flow. To distinguish between these two paradigms, we conducted laboratory experiments with larvae in turbulence. We observed veliger larvae of the gastropod Crepidula fornicata in a jet-stirred turbulence tank while simultaneously measuring two components of the fluid and larval velocity. Larvae were studied at two different stages of development, early and late, and their behavior was analyzed in response to different characteristics of turbulence: acceleration, dissipation and vorticity. Our analysis considered the effects of both the time-averaged flow and the instantaneous flow, around the larvae. Overall, we found that both stages of larvae increased their upward swimming speeds in response to increasing turbulence. However, we found that the early-stage larvae tended to respond to the time-averaged flow, whereas the late-stage larvae tended to respond to the instantaneous flow around them. These observations indicate that larvae can integrate flow information over time and that their behavioral responses to turbulence can depend on both their present and past flow environments.

Remoras pick where they stick on blue whales.

Animal-borne video recordings from blue whales in the open ocean show that remoras preferentially adhere to specific regions on the surface of the whale. Using empirical and computational fluid dynamics analyses, we show that remora attachment was specific to regions of separating flow and wakes caused by surface features on the whale. Adhesion at these locations offers remoras drag reduction of up to 71-84% compared with the freestream. Remoras were observed to move freely along the surface of the whale using skimming and sliding behaviors. Skimming provided drag reduction as high as 50-72% at some locations for some remora sizes, but little to none was available in regions where few to no remoras were observed. Experimental work suggests that the Venturi effect may help remoras stay near the whale while skimming. Understanding the flow environment around a swimming blue whale will inform the placement of biosensor tags to increase attachment time for extended ecological monitoring.

Theoretical and computational fluid dynamics of an attached remora (Echeneis naucrates).

Remora fishes have a unique dorsal suction pad that allows them to form robust, reliable, and reversible attachment to a wide variety of host organisms and marine vessels. Although investigations of the suction pad have been performed, the primary force that remoras must resist, namely fluid drag, has received little attention. This work provides a theoretical estimate of the drag experienced by an attached remora using computational fluid dynamics informed by geometry obtained from micro-computed tomography. Here, simulated flows are compared to measured flow fields of a euthanized specimen in a flow tank. Additionally, the influence of the host's boundary layer is investigated, and scaling relationships between remora features are inferred from the digitized geometry. The results suggest the drag on an attached remora is similar to that of a streamlined body, and is minimally influenced by the host's viscous boundary layer. Consequently, this evidence does not support the hypothesis that remoras discriminate between attachment locations based on hydrodynamic considerations. Comparison of the simulated drag with experimental friction tests show that even at elevated swimming speeds it is unlikely that remoras are dislodged by drag alone, and furthermore that larger remoras may be more difficult to dislodge than smaller remoras indicating that they become more suited to attachment as they mature.

Ontogenetic changes in larval swimming and orientation of pre-competent sea urchin Arbacia punctulata in turbulence.

Many marine organisms have complex life histories, having sessile adults and relying on the planktonic larvae for dispersal. Larvae swim and disperse in a complex fluid environment and the effect of ambient flow on larval behavior could in turn impact their survival and transport. However, to date, most studies on larvae-flow interactions have focused on competent larvae near settlement. We examined the importance of flow on early larval stages by studying how local flow and ontogeny influence swimming behavior in pre-competent larval sea urchins, Arbacia punctulata We exposed larval urchins to grid-stirred turbulence and recorded their behavior at two stages (4- and 6-armed plutei) in three turbulence regimes. Using particle image velocimetry to quantify and subtract local flow, we tested the hypothesis that larvae respond to turbulence by increasing swimming speed, and that the increase varies with ontogeny. Swimming speed increased with turbulence for both 4- and 6-armed larvae, but their responses differed in terms of vertical swimming velocity. 4-Armed larvae swam most strongly upward in the unforced flow regime, while 6-armed larvae swam most strongly upward in weakly forced flow. Increased turbulence intensity also decreased the relative time that larvae spent in their typical upright orientation. 6-Armed larvae were tilted more frequently in turbulence compared with 4-armed larvae. This observation suggests that as larvae increase in size and add pairs of arms, they are more likely to be passively re-oriented by moving water, rather than being stabilized (by mechanisms associated with increased mass), potentially leading to differential transport. The positive relationship between swimming speed and larval orientation angle suggests that there was also an active response to tilting in turbulence. Our results highlight the importance of turbulence to planktonic larvae, not just during settlement but also in earlier stages through morphology-flow interactions.

Disentangling the functional roles of morphology and motion in the swimming of fish.

In fishes the shape of the body and the swimming mode generally are correlated. Slender-bodied fishes such as eels, lampreys, and many sharks tend to swim in the anguilliform mode, in which much of the body undulates at high amplitude. Fishes with broad tails and a narrow caudal peduncle, in contrast, tend to swim in the carangiform mode, in which the tail undulates at high amplitude. Such fishes also tend to have different wake structures. Carangiform swimmers generally produce two staggered vortices per tail beat and a strong downstream jet, while anguilliform swimmers produce a more complex wake, containing at least two pairs of vortices per tail beat and relatively little downstream flow. Are these differences a result of the different swimming modes or of the different body shapes, or both? Disentangling the functional roles requires a multipronged approach, using experiments on live fishes as well as computational simulations and physical models. We present experimental results from swimming eels (anguilliform), bluegill sunfish (carangiform), and rainbow trout (subcarangiform) that demonstrate differences in the wakes and in swimming performance. The swimming of mackerel and lamprey was also simulated computationally with realistic body shapes and both swimming modes: the normal carangiform mackerel and anguilliform lamprey, then an anguilliform mackerel and carangiform lamprey. The gross structure of simulated wakes (single versus double vortex row) depended strongly on Strouhal number, while body shape influenced the complexity of the vortex row, and the swimming mode had the weakest effect. Performance was affected even by small differences in the wakes: both experimental and computational results indicate that anguilliform swimmers are more efficient at lower swimming speeds, while carangiform swimmers are more efficient at high speed. At high Reynolds number, the lamprey-shaped swimmer produced a more complex wake than the mackerel-shaped swimmer, similar to the experimental results. Finally, we show results from a simple physical model of a flapping fin, using fins of different flexural stiffness. When actuated in the same way, fins of different stiffnesses propel themselves at different speeds with different kinematics. Future experimental and computational work will need to consider the mechanisms underlying production of the anguilliform and carangiform swimming modes, because anguilliform swimmers tend to be less stiff, in general, than are carangiform swimmers.

Fish biorobotics: kinematics and hydrodynamics of self-propulsion.

As a result of years of research on the comparative biomechanics and physiology of moving through water, biologists and engineers have made considerable progress in understanding how animals moving underwater use their muscles to power movement, in describing body and appendage motion during propulsion, and in conducting experimental and computational analyses of fluid movement and attendant forces. But it is clear that substantial future progress in understanding aquatic propulsion will require new lines of attack. Recent years have seen the advent of one such new avenue that promises to greatly broaden the scope of intellectual opportunity available to researchers: the use of biorobotic models. In this paper we discuss, using aquatic propulsion in fishes as our focal example, how using robotic models can lead to new insights in the study of aquatic propulsion. We use two examples: (1) pectoral fin function, and (2) hydrodynamic interactions between dorsal and caudal fins. Pectoral fin function is characterized by considerable deformation of individual fin rays, as well as spanwise (along the length) and chordwise (across the fin) deformation and area change. The pectoral fin can generate thrust on both the outstroke and instroke. A robotic model of the pectoral fin replicates this result, and demonstrates the effect of altering stroke kinematics on the pattern of force production. The soft dorsal fin of fishes sheds a distinct vortex wake that dramatically alters incoming flow to the tail: the dorsal fin and caudal fin act as dual flapping foils in series. This design can be replicated with a dual-foil flapping robotic device that demonstrates this phenomenon and allows examination of regions of the flapping performance space not available to fishes. We show how the robotic flapping foil device can also be used to better understand the significance of flexible propulsive surfaces for locomotor performance. Finally we emphasize the utility of self-propelled robotic devices as a means of understanding how locomotor forces are generated, and review different conceptual designs for robotic models of aquatic propulsion.

Jet flow in steadily swimming adult squid.

Although various hydrodynamic models have been used in past analyses of squid jet propulsion, no previous investigations have definitively determined the fluid structure of the jets of steadily swimming squid. In addition, few accurate measurements of jet velocity and other jet parameters in squid have been reported. We used digital particle imaging velocimetry (DPIV) to visualize the jet flow of adult long-finned squid Loligo pealei (mantle length, L(m)=27.1+/-3.0 cm, mean +/-S.D.) swimming in a flume over a wide range of speeds (10.1-59.3 cm s(-1), i.e. 0.33-2.06 L(m) s(-1)). Qualitatively, squid jets were periodic, steady, and prolonged emissions of fluid that exhibited an elongated core of high speed flow. The development of a leading vortex ring common to jets emitted from pipes into still water often appeared to be diminished and delayed. We were able to mimic this effect in jets produced by a piston and pipe arrangement aligned with a uniform background flow. As in continuous jets, squid jets showed evidence of the growth of instability waves in the jet shear layer followed by the breakup of the jet into packets of vorticity of varying degrees of coherence. These ranged from apparent chains of short-lived vortex rings to turbulent plumes. There was some evidence of the complete roll-up of a handful of shorter jets into single vortex rings, but steady propulsion by individual vortex ring puffs was never observed. Quantitatively, the length of the jet structure in the visualized field of view, L(j), was observed to be 7.2-25.6 cm, and jet plug lengths, L, were estimated to be 4.4-49.4 cm using average jet velocity and jet period. These lengths and an average jet orifice diameter, D, of 0.8 cm were used to calculate the ratios L(j)/D and L/D, which ranged from 9.0 to 32.0 and 5.5 to 61.8, respectively. Jets emitted from pipes in the presence of a background flow suggested that the ratio between the background flow velocity and the jet velocity was more important than L/D to predict jet structure. Average jet velocities in steadily swimming squid ranged from 19.9 to 85.8 cm s(-1) (0.90-2.98 L(m) s(-1)) and were always greater in magnitude than swimming speed. Maximum instantaneous fluid speeds within squid jets ranged from 25.6 to 136.4 cm s(-1). Average jet thrust determined both from jet velocity and from three-dimensional approximations of momentum change in successive jet visualizations showed some differences and ranged from 0.009 to 0.045 N over the range of swimming speeds observed. The fraction by which the average jet velocity exceeded the swimming speed, or 'slip', decreased with increasing swimming speed, which reveals higher jet propulsive efficiency at higher swimming speeds. Jet angle, subtended from the horizontal, decreased from approximately 29 degrees to 7 degrees with increasing swimming speed. Jet frequency ranged from 0.6 to 1.3 Hz in the majority of swimming sequences, and the data suggest higher frequencies at the lowest and highest speeds. Jet velocity, angle, period and frequency exhibited increased variability at speeds between 0.6 and 1.4 L(m) s(-1). This suggests that at medium speeds squid enjoy an increased flexibility in the locomotive strategies they use to control their dynamic balance.