Sam Van Wassenbergh

Extremely fast prey capture in pipefish is powered by elastic recoil

The exceptionally high speed at which syngnathid fishes are able to rotate their snout towards prey and capture it by suction is potentially caused by a catapult mechanism in which the energy previously stored in deformed elastic elements is suddenly released. According to this hypothesis, tension is built up in tendons of the post-cranial muscles before prey capture is initiated. Next, an abrupt elastic recoil generates high-speed dorsal rotation of the head and snout, rapidly bringing the mouth close to the prey, thus enabling the pipefish to be close enough to engulf the prey by suction. However, no experimental evidence exists for such a mechanism of mechanical power amplification during feeding in these fishes. To test this hypothesis, inverse dynamical modelling based upon kinematic data from high-speed videos of prey capture in bay pipefish Syngnathus leptorhynchus, as well as electromyography of the muscle responsible for head rotation (the epaxial muscle) was performed. The remarkably high instantaneous muscle-mass-specific power requirement calculated for the initial phase of head rotation (up to 5795 W  kg−1), as well as the early onset times of epaxial muscle activity (often observed more than 300 ms before the first externally discernible prey capture motion), support the elastic power enhancement hypothesis.

Aquatic suction feeding dynamics: insights from computational modelling

Aquatic suction feeding in vertebrates involves extremely unsteady flow, externally as well as internally of the expanding mouth cavity. Consequently, studying the hydrodynamics involved in this process is a challenging research area, where experimental studies and mathematical models gradually aid our understanding of how suction feeding works mechanically. Especially for flow patterns inside the mouth cavity, our current knowledge is almost entirely based on modelling studies. In the present paper, we critically discuss some of the assumptions and limitations of previous analytical models of suction feeding using computational fluid dynamics.

A functional morphological approach to the scaling of the feeding system in the African catfish, Clarias gariepinus

SUMMARY Effects of size are pervasive and affect nearly all aspects of the biology of animals and plants. Theoretical scaling models have been developed to predict the effects of size on the functioning of musculo-skeletal systems. Although numerous experimental studies have investigated the effects of size on the movements of skeletal elements during locomotion and feeding in vertebrates, relatively little is known about the scaling of the muscles and bones responsible for the actual movements. Here, we examine the scaling of external morphology, skeletal elements of the feeding system, and a number of cranial muscles to understand how this may affect the movements observed during suction feeding in the African catfish, Clarias gariepinus. The results show that neither the head nor the cranial elements themselves scale according to geometric similarity models. Relative to head size, distinct changes in the mass and configuration of the feeding structures takes place. Unexpectedly, different cranial muscles show different scaling patterns that ultimately all lead to a positive allometry of muscle cross-sectional area relative to fish head size. This suggests that (1) the scaling of the cranial elements cannot be predicted a priori based on the scaling of external head dimensions and (2) the scaling of the feeding system is optimised towards high force output in the larger animals. An analysis of the consequences of the observed changes in morphology with size on performance traits, including bite force and jaw closing velocity, suggests a tight link between the scaling of the feeding system and the natural diet of these fish. Whereas for smaller size classes the system is tuned towards high bite forces, for animals with cranial lengths greater than 65 mm the scaling of the feeding system appears to be dictated by the hydrodynamic constraints on suction feeding.

Scaling of suction-feeding kinematics and dynamics in the African catfish, Clarias gariepinus.

SUMMARY Scaling effects on the kinematics of suction feeding in fish remain poorly understood, at least partly because of the inconsistency of the results of the existing experimental studies. Suction feeding is mechanically distinct from most other type of movements in that negative pressure inside the buccal cavity is thought to be the most important speed-limiting factor during suction. However, how buccal pressure changes with size and how this influences the speed of buccal expansion is unknown. In this paper, the effects of changes in body size on kinematics of suction feeding are studied in the catfish Clarias gariepinus. Video recordings of prey-capturing C. gariepinus ranging in total length from 111 to 923 mm were made, from which maximal displacements, velocities and accelerations of several elements of the cranial system were determined. By modelling the observed expanding head of C. gariepinus as a series of expanding hollow elliptical cylinders, buccal pressure and power requirement for the expansive phase of prey capture were calculated for an ontogenetic sequence of catfish. We found that angular velocities decrease approximately proportional with increasing cranial size, while linear velocities remain more or less constant. Although a decreasing (angular) speed of buccal expansion with increasing size could be predicted (based on calculations of power requirement and the expected mass-proportional scaling of available muscular power in C. gariepinus), the observed drop in (angular) speed during growth exceeds these predictions. The calculated muscle-mass-specific power output decreases significantly with size, suggesting a relatively lower suction effort in the larger catfish compared with the smaller catfish.

A test of mouth-opening and hyoid-depression mechanisms during prey capture in a catfish using high-speed cineradiography

SUMMARY Detailed morphological analyses have identified a number of different mechanical pathways by which the morphologically complex cranial system of fishes can achieve mouth opening and hyoid depression. However, many of these proposed mechanisms remain untested. Furthermore, very little is known about the precise timing of activity of each of these mechanisms, and about the magnitude of each mechanisms total contribution to its proposed function. In the present study, all mouth opening and hyoid depression mechanisms described for Clarias gariepinus, an air-breathing catfish, are analysed. High-speed X-ray videos were recorded during prey capture of three catfish implanted with small, radio-opaque markers in the cranial elements potentially involved. A kinematic analysis was performed from which data were used as input in planar four-bar models. This analysis shows that the opercular mouth-opening mechanism initiates mouth opening, but is not able to cause the complete mouth openings as observed on the X-ray videos. The latter is accomplished through the protractor hyoidei muscles, which couple hyoid depression to lower jaw depression in a four-bar system and also reinforce lower jaw depression by shortening during the final stage of mouth opening. Although the angulo-ceratohyal ligament was previously hypothesised to play a part in mouth opening, our results show that it probably does not, but rather functions as a hyoid-elevator during mouth closure. Finally, hyoid depression is exclusively achieved by the four-bar mechanism involving neurocranial elevation and pectoral girdle retraction, generally without any reinforcement by shortening of the sternohyoideus muscle. In contrast to the results from a recent analysis on sunfish, the catfishs sternohyoideus gradually elongates during hyoid depression.

Hydrodynamic modelling of aquatic suction performance and intra-oral pressures: limitations for comparative studies

The magnitude of sub-ambient pressure inside the bucco-pharyngeal cavity of aquatic animals is generally considered a valuable metric of suction feeding performance. However, these pressures do not provide a direct indication of the effect of the suction act on the movement of the prey item. Especially when comparing suction performance of animals with differences in the shape of the expanding bucco-pharyngeal cavity, the link between speed of expansion, water velocity, force exerted on the prey and intra-oral pressure remains obscure. By using mathematical models of the heads of catfishes, a morphologically diverse group of aquatic suction feeders, these relationships were tested. The kinematics of these models were fine-tuned to transport a given prey towards the mouth in the same way. Next, the calculated pressures inside these models were compared. The results show that no simple relationship exists between the amount of generated sub-ambient pressure and the force exerted on the prey during suction feeding, unless animals of the same species are compared. Therefore, for evaluating suction performance in aquatic animals in future studies, the focus should be on the flow velocities in front of the mouth, for which a direct relationship exists with the hydrodynamic force exerted on prey.

Scaling of Suction Feeding Performance in the Catfish Clarias gariepinus

Ontogenetic changes in the absolute dimensions of the cranial system together with changes in kinematics during prey capture can cause differences in the spatiotemporal patterns of water flow generated during suction feeding. Because the velocity of this water flow determines the force that pulls prey toward and into the mouth cavity, this can affect suction feeding performance. In this study, size‐related changes in the suction‐induced flow patterns are determined. To do so, a mathematical suction model is applied to video recordings of prey capturing Clarias gariepinus ranging in total length from 111 to 923 mm. Although large C. gariepinus could be expected to have increasing peak velocities of water flow compared with small individuals, the results from the hydrodynamic model show that this is not the case. Yet, when C. gariepinus becomes larger, the expansive phase is prolonged, resulting in a longer sustained flow. This flow also reaches farther in front of the mouth almost proportionally with head size. Forward dynamical simulations with spherical prey that are subjected to the calculated water flows indicate that the absolute distance from which a given prey can be sucked into the mouth as well as the maximal prey diameter increase substantially with increasing head size. Consequently, the range of potential prey that can be captured through suction feeding will become broader during growth of C. gariepinus. This appears to be reflected in the natural diet of this species, where both the size and the number of evasive prey increase with increasing predator size.

Scaling of contractile properties of catfish feeding muscles.

Biomechanical models are intrinsically limited in explaining the ontogenetic scaling relationships for prey capture kinematics in aquatic vertebrates because no data are available on the scaling of intrinsic contractile properties of the muscles that power feeding. However, functional insight into scaling relationships is fundamental to our understanding of the ecology, performance and evolution of animals. In this study, in vitro contractile properties of three feeding muscles were determined for a series of different sizes of African air-breathing catfishes (Clarias gariepinus). These muscles were the mouth closer musculus adductor mandibulae A2A3′, the mouth opener m. protractor hyoidei and the hypaxial muscles responsible for pectoral girdle retraction. Tetanus and twitch activation rise times increased significantly with size, while latency time was size independent. In accordance with the decrease in feeding velocity with increasing size, the cycle frequency for maximal power output of the protractor hyoidei and the adductor mandibulae showed a negative scaling relationship. Theoretical modelling predicts a scaling relationship for in vivo muscle function during which these muscles always produced at least 80% of their maximal in vitro power. These findings suggest that the contractile properties of these feeding muscles are fine-tuned to the changes in biomechanical constraints of movement of the feeding apparatus during ontogeny. However, each muscle appears to have a unique set of contractile properties. The hypaxials, the most important muscle for powering suction feeding in clariid catfish, differed from the other muscles by generating higher maximal stress and mass-specific power output with increased size, whilst the optimum cycle frequency for maximal power output only decreased significantly with size in the larger adults (cranial lengths greater than 60 mm).

Suction is kid's play: extremely fast suction in newborn seahorses

Ongoing anatomical development typically results in a gradual maturation of the feeding movements from larval to adult fishes. Adult seahorses are known to capture prey by rotating their long-snouted head extremely quickly towards prey, followed by powerful suction. This type of suction is powered by elastic recoil and requires very precise coordination of the movements of the associated feeding structures, making it an all-or-none phenomenon. Here, we show that newborn Hippocampus reidi are able to successfully feed using an extremely rapid and powerful snout rotation combined with a high-volume suction, surpassing that observed in adult seahorses. An inverse dynamic analysis shows that an elastic recoil mechanism is also used to power head rotation in newborn H. reidi. This illustrates how extreme levels of performance in highly complex musculoskeletal systems can be present at birth given a delayed birth and rapid development of functionally important structures. The fact that the head skeleton of newborn seahorses is still largely cartilaginous may not be problematic because the hydrodynamic stress on the rotating snout appeared considerably lower than in adult syngnathids.

Biomechanics and hydrodynamics of prey capture in the Chinese giant salamander reveal a high-performance jaw-powered suction feeding mechanism

During the evolutionary transition from fish to tetrapods, a shift from uni- to bidirectional suction feeding systems followed a reduction in the gill apparatus. Such a shift can still be observed during metamorphosis of salamanders, although many adult salamanders retain their aquatic lifestyle and feed by high-performance suction. Unfortunately, little is known about the interplay between jaws and hyobranchial motions to generate bidirectional suction flows. Here, we study the cranial morphology, as well as kinematic and hydrodynamic aspects related to prey capture in the Chinese giant salamander (Andrias davidianus). Compared with fish and previously studied amphibians, A. davidianus uses an alternative suction mechanism that mainly relies on accelerating water by separating the ‘plates’ formed by the long and broad upper and lower jaw surfaces. Computational fluid dynamics simulations, based on three-dimensional morphology and kinematical data from high-speed videos, indicate that the viscerocranial elements mainly serve to accommodate the water that was given a sufficient anterior-to-posterior impulse beforehand by powerful jaw separation. We hypothesize that this modified way of generating suction is primitive for salamanders, and that this behaviour could have played an important role in the evolution of terrestrial life in vertebrates by releasing mechanical constraints on the hyobranchial system.