Timothy E. Higham

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 integration of locomotion and prey capture in vertebrates: Morphology, behavior, and performance

For most vertebrates, locomotion is a fundamental component of prey capture. Despite this ubiquitous link, few studies have quantified the integration of these complex systems. Several variables related to locomotor performance, including maximum speed, acceleration, deceleration, maneuverability, accuracy, and approach stability, likely influence feeding performance in vertebrates. The relative importance of these measures of performance, however, depends on the ecology of the predator. While factors such as morphology and physiology likely define the limits of these variables, other factors such as motivation of the predator, prey type, and habitat structure can also influence performance. Understanding how these variables relate to feeding under a given suite of ecological conditions is central to understanding predator-prey interactions, and ultimately how locomotion and feeding have co-evolved. The goals of this article are to discuss several variables of locomotor performance related to prey capture, present new data on the relationship between locomotor and feeding morphology in fishes, discuss the evolution of prey capture in cichlid fishes, and outline some future directions for research. While suction feeding is a primary mechanism of prey capture in fishes, swimming is vital for accurately positioning the mouth relative to the prey item. Many fishes decelerate during prey capture using their body and fins, but the pectoral fins have a dominant role in maintaining approach stability. This suggests that fishes employing high-performance suction feeding (relatively small mouth) will have larger pectoral fins to facilitate accurate and stable feeding. I provide new data on the relationship between pectoral fin morphology and maximum gape in centrarchid fishes. For seven species, pectoral fin area was significantly, and negatively, correlated with maximum gape. This example illustrates that the demands from one complex system (feeding) can influence another complex system (locomotion). Future studies that examine the morphological, physiological, and functional evolution of locomotion involved in prey capture by aquatic and terrestrial vertebrates will provide insight into the origin and consequences of diversity.

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.

Locomotion of lizards on inclines and perches: hindlimb kinematics of an arboreal specialist and a terrestrial generalist

SUMMARY Arboreal animals, especially lizards, often traverse three-dimensional networks of narrow perches with variable and steep inclines, but the effects of both incline and narrow surfaces on the locomotor movement and function of limbs are poorly understood. Thus, we quantified the three-dimensional hindlimb kinematics of a specialized arboreal lizard, Chamaeleo calyptratus, moving horizontally, and up and down a 30° incline on a narrow (2.4 cm) perch and a flat surface. We compared the flat-surface data of C. calyptratus with those of an anatomically generalized terrestrial lizard, Dipsosaurus dorsalis. Inclines had significant main effects for relatively few kinematic variables of C. calyptratus (11%) compared to D. dorsalis (73%). For C. calyptratus, the main effects of locomotor surface were nearly three times more widespread than those of incline. The foot of C. calyptratus was markedly anterior to the hip at footfall, primarily as a result of an unusually extended knee for a lizard. A large amount of knee flexion during early stance may be used by C. calyptratus to actively pull the body forward in a manner not found in D. dorsalis. Unexpectedly, the pelvic rotation of C. calyptratus greatly exceeded that of D. dorsalis and, unlike D. dorsalis, was not affected by incline. The more medial location of the foot of C. calyptratus on the narrow perch during stance was primarily a result of knee flexion rather than femur depression. Unlike previous qualitative descriptions of chameleons, our data for the hindlimb posture of C. calyptratus during stance indicate that the limb was not particularly erect.

Functional diversification within and between muscle synergists during locomotion

Locomotion arises from the complex and coordinated function of limb muscles. Yet muscle function is dynamic over the course of a single stride and between strides for animals moving at different speeds or on variable terrain. While it is clear that motor unit recruitment can vary between and within muscles, we know little about how work is distributed within and between muscles under in vivo conditions. Here we show that the lateral gastrocnemius (LG) of helmeted guinea fowl (Numida meleagris) performs considerably more work than its synergist, the medial gastrocnemius (MG) and that the proximal region of the MG (pMG) performs more work than the distal region (dMG). Positive work done by the LG was approximately twice that of the proximal MG when the birds walked at 0.5 m s−1, and four times when running at 2.0 m s−1. This is probably due to different moments at the knee, as well as differences in motor unit recruitment. The dMG performed less work than the pMG because its apparent dynamic stiffness was greater, and because it exhibited a greater recruitment of slow-twitch fibres. The greater compliance of the pMG leads to increased stretch of its fascicles at the onset of force, further enhancing force production. Our results demonstrate the capacity for functional diversity between and within muscle synergists, which increases with changes in gait and speed.

Feeding, fins and braking maneuvers: locomotion during prey capture in centrarchid fishes.

SUMMARY Locomotion is an integral aspect of the prey capture strategy of almost every predatory animal. For fishes that employ suction to draw prey into their mouths, locomotor movements are vital for the correct positioning of the mouth relative to the prey item. Despite this, little is known regarding the relationships between locomotor movements and prey capture. To gain insights into how fishes move during prey capture and the mechanisms underlying deceleration during prey capture, I measured the fin and body movements of largemouth bass, Micropterus salmoides, and bluegill sunfish, Lepomis macrochirus. Using a high-speed video camera (500 frames s-1), I captured locomotor and feeding movements in lateral and ventral (via a mirror) view. Largemouth bass swam considerably faster than bluegill during the approach to the prey item, and both species decelerated substantially following prey capture. The mean magnitude of deceleration was significantly higher in largemouth bass (-1089 cm s-2) than bluegill (-235 cm s-2), and the timing of maximum deceleration was much later for largemouth bass (30.3 ms after maximum gape) than bluegill (6.7 ms after maximum gape). Both species employed their pectoral, anal and caudal fins in order to decelerate during prey capture. However, largemouth bass protracted their pectoral fins more and faster, likely contributing to the greater magnitude of deceleration in the species. The primary mechanism for increased deceleration was an increase in approach speed. The drag forces experienced by the fins and body are proportional to the velocity of the flow squared. Thus, the braking forces exerted by fins, without any change in kinematics, will increase exponentially with small increases in swimming speed, perhaps allowing these fishes to achieve higher braking forces at higher swimming speeds without altering body or fin kinematics. This result can likely be extended to other maneuvers such as turning.

A new angle on clinging in geckos: incline, not substrate, triggers the deployment of the adhesive system

Lizards commonly climb in complex three-dimensional habitats, and gekkotans are particularly adept at doing this by using an intricate adhesive system involving setae on the ventral surface of their digits. However, it is not clear whether geckos always deploy their adhesive system, given that doing so may result in decreased (i.e. reduction in speed) locomotor performance. Here, we investigate circumstances under which the adhesive apparatus of clinging geckos becomes operative, and examine the potential trade-offs between speed and clinging. We quantify locomotor kinematics of a gecko with adhesive capabilities (Tarentola mauritanica) and one without (Eublepharis macularius). Whereas, somewhat unusually, E. macularius did not suffer a decrease in locomotor performance with an increase in incline, T. mauritanica exhibited a significant decrease in speed between the level and a 10° incline. We demonstrate that this results from the combined influence of slope and the deployment of the adhesive system. All individuals kept their digits hyperextended on the level, but three of the six individuals deployed their adhesive system on the 10° incline, and they exhibited the greatest decrease in velocity. The deployment of the adhesive system was dependent on incline, not surface texture (600 grit sandpaper and Plexiglas), despite slippage occurring on the level Plexiglas substrate. Our results highlight the type of sensory feedback (gravity) necessary for deployment of the adhesive system, and the trade-offs associated with adhesion.

How forelimb and hindlimb function changes with incline and perch diameter in the green anole, Anolis carolinensis

SUMMARY The range of inclines and perch diameters in arboreal habitats poses a number of functional challenges for locomotion. To effectively overcome these challenges, arboreal lizards execute complex locomotor behaviors involving both the forelimbs and the hindlimbs. However, few studies have examined the role of forelimbs in lizard locomotion. To characterize how the forelimbs and hindlimbs differentially respond to changes in substrate diameter and incline, we obtained three-dimensional high-speed video of green anoles (Anolis carolinensis) running on flat (9 cm wide) and narrow (1.3 cm) perches inclined at 0, 45 and 90 deg. Changes in perch diameter had a greater effect on kinematics than changes in incline, and proximal limb variables were primarily responsible for these kinematic changes. In addition, a number of joint angles exhibited greater excursions on the 45 deg incline compared with the other inclines. Anolis carolinensis adopted strategies to maintain stability similar to those of other arboreal vertebrates, increasing limb flexion, stride frequency and duty factor. However, the humerus and femur exhibited several opposite kinematic trends with changes in perch diameter. Further, the humerus exhibited a greater range of motion than the femur. A combination of anatomy and behavior resulted in differential kinematics between the forelimb and the hindlimb, and also a potential shift in the propulsive mechanism with changes in external demand. This suggests that a better understanding of single limb function comes from an assessment of both forelimbs and hindlimbs. Characterizing forelimb and hindlimb movements may reveal interesting functional differences between Anolis ecomorphs. Investigations into the physiological mechanisms underlying the functional differences between the forelimb and the hindlimb are needed to fully understand how arboreal animals move in complex habitats.