Steven W. Day

Multidimensional analysis of suction feeding performance in fishes: fluid speed, acceleration, strike accuracy and the ingested volume of water

SUMMARY Suction feeding fish draw prey into the mouth using a flow field that they generate external to the head. In this paper we present a multidimensional perspective on suction feeding performance that we illustrate in a comparative analysis of suction feeding ability in two members of Centrarchidae, the largemouth bass (Micropterus salmoides) and bluegill sunfish (Lepomis macrochirus). We present the first direct measurements of maximum fluid speed capacity, and we use this to calculate local fluid acceleration and volumetric flow rate. We also calculated the ingested volume and a novel metric of strike accuracy. In addition, we quantified for each species the effects of gape magnitude, time to peak gape, and swimming speed on features of the ingested volume of water. Digital particle image velocimetry (DPIV) and high-speed video were used to measure the flow in front of the mouths of three fish from each species in conjunction with a vertical laser sheet positioned on the mid-sagittal plane of the fish. From this we quantified the maximum fluid speed (in the earthbound and fishs frame of reference), acceleration and ingested volume. Our method for determining strike accuracy involved quantifying the location of the prey relative to the center of the parcel of ingested water. Bluegill sunfish generated higher fluid speeds in the earthbound frame of reference, accelerated the fluid faster, and were more accurate than largemouth bass. However, largemouth bass ingested a larger volume of water and generated a higher volumetric flow rate than bluegill sunfish. In addition, because largemouth bass swam faster during prey capture, they generated higher fluid speeds in the fishs frame of reference. Thus, while bluegill can exert higher drag forces on stationary prey items, largemouth bass more quickly close the distance between themselves and prey. The ingested volume and volumetric flow rate significantly increased as gape increased for both species, while time to peak gape had little effect on the volume. However, peak gape distance did not affect the maximum fluid speed entering the mouth for either species. We suggest that species that generate high fluid speeds in the earthbound frame of reference will commonly exhibit small mouths and a high capacity to deliver force to buccal expansion, while species that ingest a large volume of water and generate high volumetric flow rates will have larger buccal cavities and cranial expansion linkage systems that favor displacement over force delivery.

Suction feeding mechanics, performance, and diversity in fishes

Despite almost 50 years of research on the functional morphology and biomechanics of suction feeding, no consensus has emerged on how to characterize suction-feeding performance, or its morphological basis. We argue that this lack of unity in the literature is due to an unusually indirect and complex linkage between the muscle contractions that power suction feeding, the skeletal movements that underlie buccal expansion, the sharp drop in buccal suction pressure that occurs during expansion, the flow of water that enters the mouth to eliminate the pressure gradient, and the forces that are ultimately exerted on the prey by this flow. This complexity has led various researchers to focus individually on suction pressure, flow velocity, or the distance the prey moves as metrics of suction-feeding performance. We attempt to integrate a mechanistic view of the ability of fish to perform these components of suction feeding. We first discuss a model that successfully relates aspects of cranial morphology to the capacity to generate suction pressure in the buccal cavity. This model is a particularly valuable tool for studying the evolution of the feeding mechanism. Second, we illustrate the multidimensional nature of suction-feeding performance in a comparison of bluegill, Lepomis macrochirus, and largemouth bass, Micropterus salmoides, two species that represent opposite ends of the spectrum of performance in suction feeding. As anticipated, bluegills had greater accuracy, lower peak flux into the mouth, and higher flow velocity and acceleration of flow than did bass. While the differences between species in accuracy of strike and peak water flux were substantial, peak suction velocity and acceleration were only about 50% higher in bluegill, a relatively modest difference. However, a hydrodynamic model of the forces that suction feeders exert on their prey shows that this difference in velocity is amplified by a positive effect of the smaller mouth aperture of bluegill on force exerted on the prey. Our model indicates that the pressure gradient in front of a fish that is feeding by suction, associated with the gradient in water velocity, results in a force on the prey that is larger than drag or acceleration reaction. A smaller mouth aperture results in a steeper pressure gradient that exerts a greater force on the prey, even when other features of the suction flow are held constant. Our work shows that some aspects of suction-feeding performance can be determined from morphology, but that the complexity of the behavior requires a diversity of perspectives to be used in order to adequately characterize performance.

Spatial and temporal patterns of water flow generated by suction-feeding bluegill sunfish Lepomis macrochirus resolved by Particle Image Velocimetry

SUMMARY The suction-feeding fish generates a flow field external to its head in order to draw prey into the mouth. To date there are very few empirical measurements that characterize the fluid mechanics of suction feeding, particularly the temporal and spatial patterns of water velocity in front of the fish. To characterize the flow in front of suction-feeding bluegill sunfish Lepomis macrochirus, measurements with high spatial (<1 mm) and temporal (500 Hz) resolution were taken using Particle Image Velocimetry (PIV). In an analysis separate from the PIV, high-speed video sequences were used for a novel method of visually tracking every seed particle for the duration of each feeding in order to determine directly the total parcel of water that the fish ingests. PIV measurements and particle tracking show that water is drawn from all around the mouth. Fluid velocity decreases rapidly with distance from the mouth and is only significant (>5% of speed at the mouth) within roughly 1 mouth diameter of the fish. Suction feeders gain little in terms of extending this flow field by even substantial increases in the fluid speed at the mouth opening. Instead, the chief advantage of increased flow speed at the mouth may be the increased magnitude of generated forces within the space very close to the mouth. After scaling of the velocity field based on size of the mouth opening and the measured fluid speed at a fixed position, the measured velocity profiles for all feedings are very similar to one another, so that a functional relationship for the magnitude of fluid speed as a function of distance from the predator mouth is presented and shown to be accurate over the range of kinematic variables tested. This relationship describes the velocity field both along the centerline of the fish and along transects lying at an angle to the centerline within both the mid-sagittal and frontal planes. Comparison of the time-resolved fluid velocity measurements to gape kinematics demonstrate that peak fluid speed occurs simultaneously with 95% of peak gape, showing that the bluegill maximizes nearly simultaneously both the generated forces and size of the region over which these forces act. The magnitude of peak fluid speed during each strike decreases as a function of increasing time to peak gape (r2=0.87), demonstrating a strong relationship between the rate of buccal cavity expansion and maximum generated flow speed.

The pressures of suction feeding: the relation between buccal pressure and induced fluid speed in centrarchid fishes

SUMMARY Suction feeding fish rapidly expand their oral cavity, resulting in a flow of water directed towards the mouth that is accompanied by a drop in pressure inside the buccal cavity. Pressure inside the mouth and fluid speed external to the mouth are understood to be mechanically linked but the relationship between them has never been empirically determined in any suction feeder. We present the first simultaneous measurements of fluid speed and buccal pressure during suction feeding in fishes. Digital particle image velocimetry (DPIV) and high-speed video were used to measure the maximum fluid speed in front of the mouth of four largemouth bass and three bluegill sunfish by positioning a vertical laser sheet on the mid-sagittal plane of the fish. Peak magnitude of pressure inside the buccal cavity was quantified using a transducer positioned within a catheter that opened into the dorsal wall of the buccal cavity. In both species the time of peak pressure preceded the time of peak fluid speed by as much as 42 ms, indicating a role for unsteady flow effects in shaping this relation. We parameterized an existing model of suction feeding to determine whether the relationship between peak pressures and fluid speeds that we observed could be predicted using just a few kinematic variables. The model predicted much higher fluid speeds than we measured at all values of peak pressure and gave a scaling exponent between them (0.51) that was higher than observed (0.36 for largemouth bass, 0.38 for bluegill). The scaling between peak buccal pressure and peak fluid speed at the mouth aperture differed in the two species, supporting the recent conclusion that species morphology affects this relation such that a general pattern may not hold.

The forces exerted by aquatic suction feeders on their prey

Successful prey capture by aquatic suction feeders depends on the ability of the predator to generate a flow of water external to the mouth that overcomes any movements and forces that the prey uses to resist the suction flow. Elucidating the nature and magnitude of these forces is a key to understanding what limits suction feeding performance. We identify three potential forces produced by the suction flow field: drag, acceleration reaction and the fluid pressure gradient. Using a mathematical model parametrized with empirical data from feeding bluegill, Lepomis macrochirus, we explore the relative magnitude of these forces under three encounter scenarios with a 5 mm diameter, spherical prey: an immobile mid-water prey; a similar prey that executes an escape response; and a prey item that grips a substratum. Contrary to the almost exclusive emphasis on drag in the suction feeding literature, it made a minor contribution to the total forces in all three cases. In all three scenarios, the pressure gradient is the largest of the three forces. These results are important because previous researchers have emphasized drag and have not explicitly recognized a role for the pressure gradient force in suction feeding. The simulations suggest previously unrecognized mechanisms that suction feeders can use to enhance the forces that they exert, by increasing the steepness of the pressure gradient that the prey item is exposed to. This can be accomplished either by increasing the rate of increase in fluid velocity or by restricting the size of the mouth aperture, which creates a steeper spatial gradient in pressure.

Jaw protrusion enhances forces exerted on prey by suction feeding fishes.

The ability to protrude the jaws during prey capture is a hallmark of teleost fishes, widely recognized as one of the most significant innovations in their diverse and mechanically complex skull. An elaborated jaw protrusion mechanism has independently evolved multiple times in bony fishes, and is a conspicuous feature in several of their most spectacular radiations, ultimately being found in about half of the approximately 30 000 living species. Variation in jaw protrusion distance and speed is thought to have facilitated the remarkable trophic diversity found across fish groups, although the mechanical consequences of jaw protrusion for aquatic feeding performance remain unclear. Using a hydrodynamic approach, we show that rapid protrusion of the jaws towards the prey, coupled with the spatial pattern of the flow in front of the mouth, accelerates the water around the prey. Jaw protrusion provides an independent source of acceleration from that induced by the unsteady flow at the mouth aperture, increasing by up to 35% the total force exerted on attached, escaping and free-floating passive prey. Despite initiating the strike further away, fishes can increase peak force on their prey by protruding their jaws towards it, compared with a ‘non-protruding’ state, where the distance to prey remains constant throughout the strike. The force requirements for capturing aquatic prey might have served as a selective factor for the evolution of jaw protrusion in modern fishes.

Multilaboratory Particle Image Velocimetry Analysis of the FDA Benchmark Nozzle Model to Support Validation of Computational Fluid Dynamics Simulations

This study is part of a FDA-sponsored project to evaluate the use and limitations of computational fluid dynamics (CFD) in assessing blood flow parameters related to medical device safety. In an interlaboratory study, fluid velocities and pressures were measured in a nozzle model to provide experimental validation for a companion round-robin CFD study. The simple benchmark nozzle model, which mimicked the flow fields in several medical devices, consisted of a gradual flow constriction, a narrow throat region, and a sudden expansion region where a fluid jet exited the center of the nozzle with recirculation zones near the model walls. Measurements of mean velocity and turbulent flow quantities were made in the benchmark device at three independent laboratories using particle image velocimetry (PIV). Flow measurements were performed over a range of nozzle throat Reynolds numbers (Re(throat)) from 500 to 6500, covering the laminar, transitional, and turbulent flow regimes. A standard operating procedure was developed for performing experiments under controlled temperature and flow conditions and for minimizing systematic errors during PIV image acquisition and processing. For laminar (Re(throat)=500) and turbulent flow conditions (Re(throat)≥3500), the velocities measured by the three laboratories were similar with an interlaboratory uncertainty of ∼10% at most of the locations. However, for the transitional flow case (Re(throat)=2000), the uncertainty in the size and the velocity of the jet at the nozzle exit increased to ∼60% and was very sensitive to the flow conditions. An error analysis showed that by minimizing the variability in the experimental parameters such as flow rate and fluid viscosity to less than 5% and by matching the inlet turbulence level between the laboratories, the uncertainties in the velocities of the transitional flow case could be reduced to ∼15%. The experimental procedure and flow results from this interlaboratory study (available at http://fdacfd.nci.nih.gov) will be useful in validating CFD simulations of the benchmark nozzle model and in performing PIV studies on other medical device models.

Scaling of suction-induced flows in bluegill: morphological and kinematic predictors for the ontogeny of feeding performance

SUMMARY During ontogeny, animals undergo changes in size and shape that result in shifts in performance, behavior and resource use. These ontogenetic changes provide an opportunity to test hypotheses about how the growth of structures affects biological functions. In the present study, we ask how ontogenetic changes in skull biomechanics affect the ability of bluegill sunfish, a high-performance suction feeder, to produce flow speeds and accelerations during suction feeding. The flow of water in front of the mouth was measured directly for fish ranging from young-of-year to large adults, using digital particle imaging velocimetry (DPIV). As bluegill size increased, the magnitude of peak flow speed they produced increased, and the effective suction distance increased because of increasing mouth size. However, throughout the size range, the timing of peak fluid speed remained unchanged, and flow was constrained to approximately one gape distance from the mouth. The observed scaling relationships between standard length and peak flow speed conformed to expectations derived from two biomechanical models, one based on morphological potential to produce suction pressure (the Suction Index model) and the other derived from a combination of morphological and kinematic variables (the Expanding Cone model). The success of these models in qualitatively predicting the observed allometry of induced flow speed reveals that the scaling of cranial morphology underlies the scaling of suction performance in bluegill.

Integrating the determinants of suction feeding performance in centrarchid fishes.

SUMMARY When suction-feeding vertebrates expand their buccal cavity to draw water into their mouth, they also exert a hydrodynamic force on their prey. This force is key to strike success, directly countering forces exerted by escaping or clinging prey. While the ability to produce high flow accelerations in front of the mouth is central to the predators ability to exert high forces on the prey, several mechanisms can contribute to the disparity between the potential and realized performance through their effect on flow and acceleration as experienced by the prey. In the present study, we test how interspecific variation in gape size, mouth displacement speed and the fishs ability to locate prey at the optimal position affect variation in the force exerted on attached prey. We directly measured these forces by allowing bluegill sunfish and largemouth bass to strike at ghost shrimp tethered to a load cell that recorded force at 5000 Hz, while synchronously recording strikes with a 500 Hz video. Strike kinematics of largemouth bass were slower than that of bluegill, as were estimated flow speeds and the force exerted on the prey. This difference in force persisted after taking into account the faster suction flows and accelerations of bluegill, and was only accounted for by considering interspecific differences in gape size, mouth displacement speed and fishs ability to locate the prey at the optimal position. The contribution to interspecific differences in the force exerted on the prey was estimated to be 42% for flow speed, 25% for strike efficiency, 3% for gape size and 30% for mouth displacement speed. Hence, kinematic diversity results in substantial differences in suction performance, beyond those expected based on the capacity to generate a high flow velocity. This functional complexity, in the form of biomechanically independent mechanisms that are recruited for one function, can potentially mitigate performance trade-offs in suction-feeding fishes.

Particle image velocimetry measurements of blood velocity in a continuous flow ventricular assist device.

The third prototype of a continuous flow ventricular assist device (CFVAD3) is being developed and tested for implantation in humans. The blood in the pump flows through a fully shrouded four-bladed impeller (supported by magnetic bearings) and through small clearance regions on either side of the impeller. Measurements of velocities using particle image velocimetry of a fluid with the same viscosity as blood have been made in one of these clearance regions. Particle image velocimetry is a technique that measures the instantaneous velocity field within an illuminated plane of the fluid field by scattering light from particles added to the fluid. These measurements have been used to improve understanding of the fluid dynamics within these critical regions, which are possible locations of both high shear and stagnation, both of which are to be avoided in a blood pump. Computational models of the pump exist and these models are currently being used to aid in the design of future prototypes. Among other things, these models are used to predict the potential for hemolysis and thrombosis. Measurements of steady flow at two operating speeds and flow rates are presented. The measurements are compared with the computed solutions to validate and refine, where necessary, the existing computational models.