Matthew J. McHenry

The ontogenetic scaling of hydrodynamics and swimming performance in jellyfish (Aurelia aurita)

SUMMARY It is not well understood how ontogenetic changes in the motion and morphology of aquatic animals influence the performance of swimming. The goals of the present study were to understand how changes in size, shape and behavior affect the hydrodynamics of jet propulsion in the jellyfish Aurelia aurita and to explore how such changes affect the ontogenetic scaling of swimming speed and cost of transport. We measured the kinematics of jellyfish swimming from video recordings and simulated the hydrodynamics of swimming with two computational models that calculated thrust generation by paddle and jet mechanisms. Our results suggest that thrust is generated primarily by jetting and that there is negligible thrust generation by paddling. We examined how fluid forces scaled with body mass using the jet model. Despite an ontogenetic increase in the range of motion by the bell diameter and a decrease in the height-to-diameter ratio, we found that thrust and acceleration reaction scaled with body mass as predicted by kinematic similarity. However, jellyfish decreased their pulse frequency with growth, and speed consequently scaled at a lower exponential rate than predicted by kinematic similarity. Model simulations suggest that the allometric growth in Aurelia results in swimming that is slower, but more energetically economical, than isometric growth with a prolate bell shape. The decrease in pulse frequency over ontogeny allows large Aurelia medusae to avoid a high cost of transport but generates slower swimming than if they maintained a high pulse frequency. Our findings suggest that ontogenetic change in the height-to-diameter ratio and pulse frequency of Aurelia results in swimming that is relatively moderate in speed but is energetically economical.

Larval zebrafish rapidly sense the water flow of a predator's strike

Larval fishes have a remarkable ability to sense and evade the feeding strike of a predator fish with a rapid escape manoeuvre. Although the neuromuscular control of this behaviour is well studied, it is not clear what stimulus allows a larva to sense a predator. Here we show that this escape response is triggered by the water flow created during a predators strike. Using a novel device, the impulse chamber, zebrafish (Danio rerio) larvae were exposed to this accelerating flow with high repeatability. Larvae responded to this stimulus with an escape response having a latency (mode=13–15 ms) that was fast enough to respond to predators. This flow was detected by the lateral line system, which includes mechanosensory hair cells within the skin. Pharmacologically ablating these cells caused the escape response to diminish, but then recover as the hair cells regenerated. These findings demonstrate that the lateral line system plays a role in predator evasion at this vulnerable stage of growth in fishes.

EVOLUTION OF BEHAVIOR AND NEURAL CONTROL OF THE FAST-START ESCAPE RESPONSE

Abstract The fast‐start startle behavior is the primary mechanism of rapid escape in fishes and is a model system for examining neural circuit design and musculoskeletal function. To develop a dataset for evolutionary analysis of the startle response, the kinematics and muscle activity patterns of the fast‐start were analyzed for four fish species at key branches in the phylogeny of vertebrates. Three of these species (Polypterus palmas, Lepisosteus osseus, and Amia calva) represent the base of the actinopterygian radiation. A fourth species (Oncorhynchus mykiss) provided data for a species in the central region of the teleost phylogeny. Using these data, we explored the evolution of this behavior within the phylogeny of vertebrates. To test the hypothesis that startle features are evolutionarily conservative, the variability of motor patterns and kinematics in fast‐starts was described. Results show that the evolution of the startle behavior in fishes, and more broadly among vertebrates, is not conservative. The fast‐start has undergone substantial change in suites of kinematics and electromyogram features, including the presence of either a one‐ or a two‐stage kinematic response and change in the extent of bilateral muscle activity. Comparative methods were used to test the evolutionary hypothesis that changes in motor control are correlated with key differences in the kinematics and behavior of the fast‐start. Significant evolutionary correlations were found between several motor pattern and behavioral characters. These results suggest that the startle neural circuit itself is not conservative. By tracing the evolution of motor pattern and kinematics on a phylogeny, it is shown that major changes in the neural circuit of the startle behavior occur at several levels in the phylogeny of vertebrates.

Zebrafish larvae evade predators by sensing water flow

SUMMARY The ability of fish to evade predators is central to the ecology and evolution of a diversity of species. However, it is largely unclear how prey fish detect predators in order to initiate their escape. We tested whether larval zebrafish (Danio rerio) sense the flow created by adult predators of the same species. When placed together in a cylindrical arena, we found that larvae were able to escape 70% of predator strikes (mean escape probability Pescape=0.7, N=13). However, when we pharmacologically ablated the flow-sensitive lateral line system, larvae were rarely capable of escape (mean Pescape=0.05, N=11). In order to explore the rapid events that facilitate a successful escape, we recorded freely swimming predators and prey using a custom-built camera dolly. This device permitted two-dimensional camera motion to manually track prey and record their escape response with high temporal and spatial resolution. These recordings demonstrated that prey were more than 3 times more likely to evade a suction-feeding predator if they responded before (Pescape=0.53, N=43), rather than after (Pescape=0.15, N=13), a predators mouth opened, which is a highly significant difference. Therefore, flow sensing plays an essential role in predator evasion by facilitating a response prior to a predators strike.

The flexural stiffness of superficial neuromasts in the zebrafish(Danio rerio) lateral line

SUMMARY Superficial neuromasts are structures that detect water flow on the surface of the body of fish and amphibians. As a component of the lateral line system, these receptors are distributed along the body, where they sense flow patterns that mediate a wide variety of behaviors. Their ability to detect flow is governed by their structural properties, yet the micromechanics of superficial neuromasts are not well understood. The aim of this study was to examine these mechanics in zebrafish (Danio rerio) larvae by measuring the flexural stiffness of individual neuromasts. Each neuromast possesses a gelatinous cupula that is anchored to hair cells by kinocilia. Using quasi-static bending tests of the proximal region of the cupula, we found that flexural stiffness is proportional to the number of hair cells, and consequently the number of kinocilia, within a neuromast. From this relationship, the flexural stiffness of an individual kinocilium was found to be 2.4×10–20 N m2. Using this value, we estimate that the 11 kinocilia in an average cupula generate more than four-fifths of the total flexural stiffness in the proximal region. The relatively minor contribution of the cupular matrix may be attributed to its highly compliant material composition (Youngs modulus of ∼21 Pa). The distal tip of the cupula is entirely composed of this material and is consequently predicted to be at least an order of magnitude more flexible than the proximal region. These findings suggest that the transduction of flow by a superficial neuromast depends on structural dynamics that are dominated by the number and height of kinocilia.

The mechanical scaling of coasting in zebrafish (Danio rerio)

SUMMARY Many fish species span two or three orders of magnitude in length during the growth from larvae to adults, and this change may have dramatic consequences for locomotor performance. We measured how the performance of coasting changes over the life history of zebrafish (Danio rerio) and examined the scaling of mechanics underlying this change. Adult zebrafish coast disproportionately further and faster and maintain their speed for a longer duration than do larvae and juveniles. Measurements of drag on tethered dead fish suggest that adult fish operate in an inertial regime by coasting at relatively high Reynolds numbers (Re>1000), and in vivo drag measurements showed adults to operate with a drag coefficient (Cinert≈0.024) that was consistent with previously published estimates. However, drag scaled differently at lower Re values than those assumed in previous studies. We found a viscous regime at Re<300, which corresponds to the routine coasting of larvae and juveniles. Despite these changes in hydrodynamics over growth, a mathematical model of coasting mechanics suggests that the disproportionately longer coasting of adults is caused primarily by their large body mass and high speed at the beginning of coasting. We therefore propose that changes in coasting performance with growth are dictated primarily by the scaling of momentum rather than resulting from hydrodynamic changes. These results provide an opportunity for new interpretations of function in the growth and evolution of fish.

Mechanical filtering by the boundary layer and fluid–structure interaction in the superficial neuromast of the fish lateral line system

A great diversity of aquatic animals detects water flow with ciliated mechanoreceptors on the body’s surface. In order to understand how these receptors mechanically filter signals, we developed a theoretical model of the superficial neuromast in the fish lateral line system. The cupula of the neuromast was modeled as a cylindrical beam that deflects in response to an oscillating flow field. Its accuracy was verified by comparison with prior measurements of cupular deflection in larval zebrafish (Danio rerio). The model predicts that the boundary layer of flow over the body attenuates low-frequency stimuli. The fluid–structure interaction between this flow and the cupula attenuates high-frequency stimuli. The number and height of hair cell kinocilia and the dimensions of the cupular matrix determine the range of intermediate frequencies to which a neuromast is sensitive. By articulating the individual mechanical contributions of the boundary layer and the components of cupular morphology, this model provides the theoretical framework for understanding how a hydrodynamic receptor filters flow signals.

Gentamicin is ototoxic to all hair cells in the fish lateral line system

Hair cells of the lateral line system in fish may differ in their susceptibility to damage by aminoglycoside antibiotics. Gentamicin has been reported to damage hair cells within canal neuromasts, but not those within superficial neuromasts. This finding, based on SEM imaging, indicates a distinction in the physiology of hair cells between the two classes of neuromast. Studies concerned with the individual roles of canal and superficial neuromasts in behavior have taken advantage of this effect in an attempt to selectively disable canal neuromasts without affecting superficial neuromast function. Here we present an experimental test of the hypothesis that canal neuromasts are more vulnerable to gentamicin than superficial neuromasts. We measured the effect of gentamicin exposure on hair cells using vital stains (DASPEI and FM1-43) in the neuromasts of Mexican blind cave fish (Astyanaxfasciatus) and zebrafish (Daniorerio). Contrary to the findings of prior studies that used SEM, gentamicin significantly reduced dye uptake by hair cells of both canal and superficial neuromasts in both species. Therefore, lateral line hair cells of both neuromast types are vulnerable to gentamicin ototoxicity. These findings argue for a re-evaluation of the results of studies that have used gentamicin to differentiate the roles of the two classes of neuromast in fish behavior.

The hydrodynamics of locomotion at intermediate Reynolds numbers: undulatory swimming in ascidian larvae (Botrylloides sp.).

SUMMARY Understanding how the shape and motion of an aquatic animal affects the performance of swimming requires knowledge of the fluid forces that generate thrust and drag. These forces are poorly understood for the large diversity of animals that swim at Reynolds numbers (Re) between 100 and 102. We experimentally tested quasi-steady and unsteady blade-element models of the hydrodynamics of undulatory swimming in the larvae of the ascidian Botrylloides sp. by comparing the forces predicted by these models with measured forces generated by tethered larvae and by comparing the swimming speeds predicted with measurements of the speed of freely swimming larvae. Although both models predicted mean forces that were statistically indistinguishable from measurements, the quasi-steady model predicted the timing of force production and mean swimming speed more accurately than the unsteady model. This suggests that unsteady force (i.e. the acceleration reaction) does not play a role in the dynamics of steady undulatory swimming at Re≈102. We explored the relative contribution of viscous and inertial force to the generation of thrust and drag at 100<Re<102 by running a series of mathematical simulations with the quasi-steady model. These simulations predicted that thrust and drag are dominated by viscous force (i.e. skin friction) at Re≈100 and that inertial force (i.e. form force) generates a greater proportion of thrust and drag at higher Re than at lower Re. However, thrust was predicted to be generated primarily by inertial force, while drag was predicted to be generated more by viscous than inertial force at Re≈102. Unlike swimming at high (>102) and low (<100) Re, the fluid forces that generate thrust cannot be assumed to be the same as those that generate drag at intermediate Re.

The morphology and mechanical sensitivity of lateral line receptors in zebrafish larvae (Danio rerio).

SUMMARY The lateral line system of fish and amphibians detects water flow with receptors on the surface of the body. Although differences in the shape of these receptors, called neuromasts, are known to influence their mechanics, it is unclear how neuromast morphology affects the sensitivity of the lateral line system. We examined the functional consequences of morphological variation by measuring the dimensions of superficial neuromasts in zebrafish larvae (Danio rerio) and mathematically modeling their mechanics. These measurements used a novel morphometric technique that recorded landmarks in three dimensions at a microscopic scale. The mathematical model predicted mechanical sensitivity as the ratio of neuromast deflection to flow velocity for a range of stimulus frequencies. These predictions suggest that variation in morphology within this species generates a greater than 30-fold range in the amplitude of sensitivity and more than a 200-fold range of variation in cut-off frequency. Most of this variation was generated by differences in neuromast height that do not correlate with body position. Our results suggest that natural variation in cupular height within a species is capable of generating large differences in their mechanical filtering and dynamic range.