Suction feeding biomechanics of Polypterus bichir: investigating linkage mechanisms and the contributions of cranial kinesis to oral cavity volume change

Many fishes use substantial cranial kinesis to rapidly increase buccal cavity volume, pulling prey into the mouth via suction feeding. Living polypterids are a key lineage for understanding the evolution and biomechanics of suction feeding due to their phylogenetic position and unique morphology. Polypterus bichir have fewer mobile cranial elements compared to teleosts (e.g., immobile [pre]maxillae) but successfully generate suction through dorsal, ventral, and lateral oral cavity expansion. However, the relative contributions of these motions to suction feeding success have not been quantified. Additionally, extensive body musculature and lack of opercular jaw opening linkages make P. bichir of interest for examining the role of cranial vs. axial muscles in driving mandibular depression. Here we analyze the kinematics of buccal expansion during suction feeding in P. bichir using X-Ray Reconstruction of Moving Morphology (XROMM) and quantify the contributions of skeletal elements to oral cavity volume expansion and prey capture. Mouth gape peaks early in the strike, followed by maximum cleithral and ceratohyal rotations, and finally by opercular and suspensorial abductions, maintaining the anterior-to-posterior movement of water. Using a new method of quantifying bones’ relative contributions to volume change (RCVC) we demonstrate that ceratohyal kinematics are the most significant drivers of oral cavity volume change. All measured cranial bone motions, except abduction of the suspensorium, are correlated with prey motion. Lastly, cleithral retraction is largely concurrent with ceratohyal retraction and jaw depression while the sternohyoideus maintains constant length, suggesting a central role of the axial muscles, cleithrum, and ceratohyal in ventral expansion.

Trophic guilds of suction-feeding fishes are distinguished by their characteristic hydrodynamics of swimming and feeding

Suction-feeding in fishes is a ubiquitous form of prey capture whose outcome depends both on the movements of the predator and the prey, and on the dynamics of the surrounding fluid, which exerts forces on the two organisms. The inherent complexity of suction-feeding has challenged previous efforts to understand how the feeding strikes are modified when species evolve to feed on different prey types. Here, we use the concept of dynamic similarity, commonly applied to understanding the mechanisms of swimming, flying, walking and aquatic feeding. We characterize the hydrodynamic regimes pertaining to (i) the forward movement of the fish (ram), and (ii) the suction flows for feeding strikes of 71 species of acanthomorph fishes. A discriminant function analysis revealed that feeding strikes of zooplanktivores, generalists and piscivores could be distinguished based on their hydrodynamic regimes. Furthermore, a phylogenetic comparative analysis revealed that there are distinctive hydrodynamic adaptive peaks associated with zooplanktivores, generalists and piscivores. The scaling of dynamic similarity across species, body sizes and feeding guilds in fishes indicates that elementary hydrodynamic principles govern the trophic evolution of suction-feeding in fishes.

Motor control in the epaxial musculature of bluegill sunfish in feeding and locomotion

ABSTRACT Fishes possess an impressive repertoire of feeding and locomotor behaviors that in many cases rely on the same power source: the axial musculature. As both functions employ different skeletal systems, head versus body, integrating these functions would likely require modular motor control. Although there have been many studies of motor control in feeding or locomotion in fishes, only one study to date has examined both functions in the same individuals. To characterize bilateral motor control of the epaxial musculature in feeding and locomotion, we measured muscle activity and shortening in bluegill sunfish (Lepomis macrochirus) using electromyography and sonomicrometry. We found that sunfish recruit epaxial regions in a dorsal-to-ventral manner to increase feeding performance, such that high-performance feeding activates all the epaxial musculature. In comparison, sunfish seemed to activate all three epaxial regions irrespective of locomotor performance. Muscle activity was present on both sides of the body in nearly all feeding and locomotor behaviors. Feeding behaviors used similar activation intensities on the two sides of the body, whereas locomotor behaviors consistently used higher intensities on the side undergoing muscle shortening. In all epaxial regions, fast-starts used the highest activation intensities, although high-performance suction feeding occasionally showed near-maximal intensity. Finally, active muscle volume was positively correlated with the peak rate of body flexion in feeding and locomotion, indicating a continuous relationship between recruitment and performance. A comparison of these results with recent work on largemouth bass (Micropterus salmoides) suggests that centrarchid fishes use similar motor control strategies for feeding, but interspecific differences in peak suction-feeding performance are determined by active muscle volume.

In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish

Virtually all fish rely on flows of water to transport food to the back of their pharynx. While external flows that draw food into the mouth are well described, how intra-oral water flows manage to deposit food at the esophagus entrance remains unknown. In theory, the posteriorly moving water must, at some point, curve laterally and/or ventrally to exit through the gill slits. Such flows would eventually carry food away from the esophagus instead of towards it. This apparent paradox calls for a filtration mechanism to deviate food from the suction-feeding streamlines. To study this gap in our fundamental understanding of how fish feed, we developed and applied a new technique to quantify three-dimensional patterns of intra-oral water flows in vivo. We combined stereoscopic high-speed x-ray videos to quantify skeletal motion (XROMM) with 3D x-ray particle tracking (XPT) of approximately neutrally buoyant spheres of 1.4 mm in diameter. We showed, for carp (Cyprinus carpio) and tilapia (Oreochromis niloticus), that water tracers displayed higher curvatures than food tracers, indicating an inertia-driven filtration. In addition, tilapia also exhibited a 'central jet' flow pattern, which aids in quickly carrying food to the pharyngeal jaw region. When the food was trapped at the branchial basket, it was resuspended and carried more centrally by periodical bidirectional waterflows, synchronized with head-bone motions. By providing a complete picture of the suction-feeding process and revealing fundamental differences in food transport mechanisms among species, this new technique opens a new area of investigation to fully understand how most aquatic vertebrates feed.

5. How amphibians feed

‘How amphibians feed’ studies how amphibians feed. Adult amphibians are all carnivores, mostly eating invertebrates. The most effective way for an amphibian to feed when it is under water is to get as close to its prey as possible, then open its mouth suddenly and widely to suck the food in with a stream of water. However, this kind of suction feeding is no use on land. Amphibians feeding on land must use an alternative method. The most common is to have a sticky tongue that can be protruded from the mouth to capture the prey. Another alternative method is to have strong jaws that can grasp the prey directly.

Elastic energy storage in seahorses leads to a unique suction flow dynamics compared to other actinopterygian

Suction feeding is a dominant prey-capture strategy across actinopterygians, consisting of a rapid expansion of the mouth cavity that drives a flow of water containing the prey into the mouth. Suction feeding is a power-hungry behavior, involving the actuation of cranial muscles as well as the anterior third of the fish's swimming muscles. Seahorses, which have reduced swimming muscles, evolved a unique mechanism for elastic energy storage that powers their suction flows. This mechanism allows seahorses to achieve head rotation speeds that are 50 times faster than fish lacking such a mechanism. However, it is unclear how the dynamics of suction flows in seahorses differ from the conserved pattern observed across other actinopterygians, nor how differenced in snout length across seahorses affect these flows. Using flow visualization experiments, we show that seahorses generate suction flows that are 8 times faster than similar-sized fish, and that the temporal patterns of cranial kinematics and suction flows in seahorses differs from the conserved pattern observed across other actinopterygians. However, the spatial patterns retain the conserved actinopterygian characteristics, where suction flows impact a radially symmetric region of ∼1 gape diameter outside the mouth. Within seahorses, increases in snout length were associated with slower suction flows and faster head rotation speeds, resulting in a trade-off between pivot feeding and suction feeding. Overall, this study shows how the unique cranial kinematics in seahorses are manifested in their suction feeding performance, and highlights the trade-offs associated with their unique morphology and mechanics.

Computational fluid dynamics provide evidence for a compensatory suction feeding like effect in the predatory strike of dragonfly larvae

Most fast-moving aquatic predators face the challenge of bow wave formation. Water in front of predator alarms or even displaces the prey. To mitigate the formation of such a bow wave, a strategy aiming at pressure reduction via suction has evolved convergently in several animal groups: compensatory suction feeding. The aquatic larvae of dragonflies and damselflies (Insecta: Odonata) are likely to face this challenge as well. They capture prey underwater using a fast-moving raptorial appendage, the so-called prehensile labial mask. Within dragonflies (Odonata: Anisoptera) two basic shapes of the prehensile labial mask have evolved, with an either flat and slender or concave distal segment. While the former is a pure grasping device, the latter is also capable of scooping up smaller prey and retaining it inside the cavity by arrays of bristle-like structures. The hydrodynamics of the prehensile labial mask was previously unknown. We used computational fluid dynamic (CFD) simulations of the distal segment of the mask, to investigate for the first time how different shapes of the mask impact their function. Our results suggest that both shapes are highly streamlined and generate a low-pressure area, likely leading to an effect analogous to the compensatory suction feeding. This might be an interesting concept for technical application in small scale grasping devices, e.g. for simple sampling mechanisms in small-sized autonomous underwater vehicles (μAUVs).

Suction feeding by elephants

Despite having a trunk that weighs over 100 kg, elephants mainly feed on lightweight vegetation. How do elephants manipulate such small items? In this experimental and theoretical investigation, we filmed elephants at Zoo Atlanta showing that they can use suction to grab food, performing a behaviour that was previously thought to be restricted to fishes. We use a mathematical model to show that an elephant’s nostril size and lung capacity enables them to grab items using comparable pressures as the human lung. Ultrasonographic imaging of the elephant sucking viscous fluids show that the elephant’s nostrils dilate up to 30 % in radius, which increases the nasal volume by 64 % . Based on the pressures applied, we estimate that the elephants can inhale at speeds of over 150 m s −1 , nearly 30 times the speed of a human sneeze. These high air speeds enable the elephant to vacuum up piles of rutabaga cubes as well as fragile tortilla chips. We hope these findings inspire further work in suction-based manipulation in both animals and robots.

A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature

The axial musculature of fishes has historically been characterized as the powerhouse for explosive swimming behaviors. However, recent studies show that some fish also use their ‘swimming’ muscles to generate over 90% of the power for suction feeding. Can the axial musculature achieve high power output for these two mechanically distinct behaviors? Muscle power output is enhanced when all of the fibers within a muscle shorten at optimal velocity. Yet, axial locomotion produces a mediolateral gradient of muscle strain that should force some fibers to shorten too slowly and others too fast. This mechanical problem prompted research into the gearing of fish axial muscle and led to the discovery of helical fiber orientations that homogenize fiber velocities during swimming, but does such a strain gradient also exist and pose a problem for suction feeding? We measured muscle strain in bluegill sunfish, Lepomis macrochirus, and found that suction feeding produces a gradient of longitudinal strain that, unlike the mediolateral gradient for locomotion, occurs along the dorsoventral axis. A dorsoventral strain gradient within a muscle with fiber architecture shown to counteract a mediolateral gradient suggests that bluegill sunfish should not be able to generate high power outputs from the axial muscle during suction feeding—yet prior work shows that they do, up to 438 W kg−1. Solving this biomechanical paradox may be critical to understanding how many fishes have co-opted ‘swimming’ muscles into a suction feeding powerhouse.