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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.

 

ABSTRACT Suction feeding in ray-finned fishes involves powerful buccal cavity expansion to accelerate water and food into the mouth. Previous XROMM studies in largemouth bass (Micropterus salmoides), bluegill sunfish (Lepomis macrochirus) and channel catfish (Ictalurus punctatus) have shown that more than 90% of suction power in high performance strikes comes from the axial musculature. Thus, the shape of the axial muscles and skeleton may affect suction feeding mechanics. Royal knifefish (Chitala blanci) have an unusual postcranial morphology, with a ventrally flexed vertebral column and relatively large mass of epaxial muscle. Based on their body shape, we hypothesized that royal knifefish would generate high power strikes by utilizing large neurocranial elevation, vertebral column extension and epaxial shortening. As predicted, C. blanci generated high suction expansion power compared with the other three species studied to date (up to 160 W), which was achieved by increasing both the rate of volume change and the intraoral subambient pressure. The large epaxial muscle (25% of body mass) shortened at high velocities to produce large neurocranial elevation and vertebral extension (up to 41 deg, combined), as well as high muscle mass-specific power (up to 800 W kg−1). For the highest power strikes, axial muscles generated 95% of the power, and 64% of the axial muscle mass consisted of the epaxial muscles. The epaxial-dominated suction expansion of royal knifefish supports our hypothesis that postcranial morphology may be a strong predictor of suction feeding biomechanics. 

Suction feeding in ray-finned fishes requires substantial muscle power for fast and forceful prey capture. The axial musculature located immediately behind the head has been long known to contribute some power for suction feeding, but recent XROMM and fluoromicrometry studies found nearly all the axial musculature (over 80%) provides effectively all (90–99%) of the power for high-performance suction feeding. The dominance of axial power suggests a new framework for studying the musculoskeletal biomechanics of fishes: the form and function of axial muscles and bones should be analysed for power production in feeding (or at least as a compromise between swimming and feeding), and cranial muscles and bones should be analysed for their role in transmitting axial power and coordinating buccal expansion. This new framework is already yielding novel insights, as demonstrated in four species for which suction power has now been measured. Interspecific comparisons suggest high suction power can be achieved in different ways: increasing the magnitude of suction pressure or the rate of buccal volume change, or both (as observed in the most powerful of these species). Our framework suggests that mechanical and evolutionary interactions between the head and the body, and between the swimming and feeding roles of axial structures, may be fruitful areas for continued study. 

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. 

Tetrapods use their neck to move the head three-dimensionally, relative to the body and limbs. Fish lack this anatomical neck, yet during feeding many species elevate (dorsally rotate) the head relative to the body. Cranial elevation is hypothesized to result from the craniovertebral and cranial-most intervertebral joints acting as a neck, by dorsally rotating (extending). However, this has never been tested due to the difficulty of visualizing and measuring vertebral motion in vivo . I used X-ray reconstruction of moving morphology to measure three-dimensional vertebral kinematics in rainbow trout ( Oncorhynchus mykiss ) and Commerson's frogfish ( Antennarius commerson ) during feeding. Despite dramatically different morphologies, in both species dorsoventral rotations extended far beyond the craniovertebral and cranial intervertebral joints. Trout combine small (most less than 3°) dorsal rotations over up to a third of their intervertebral joints to elevate the neurocranium. Frogfish use extremely large (often 20–30°) rotations of the craniovertebral and first intervertebral joint, but smaller rotations occurred across two-thirds of the vertebral column during cranial elevation. Unlike tetrapods, fish rotate large regions of the vertebral column to rotate the head. This suggests both cranial and more caudal vertebrae should be considered to understand how non-tetrapods control motion at the head–body interface. 

ABSTRACT Some fishes rely on large regions of the dorsal (epaxial) and ventral (hypaxial) body muscles to power suction feeding. Epaxial and hypaxial muscles are known to act as motors, powering rapid mouth expansion by shortening to elevate the neurocranium and retract the pectoral girdle, respectively. However, some species, like catfishes, use little cranial elevation. Are these fishes instead using the epaxial muscles to forcefully anchor the head, and if so, are they limited to lower-power strikes? We used X-ray imaging to measure epaxial and hypaxial length dynamics (fluoromicrometry) and associated skeletal motions (XROMM) during 24 suction feeding strikes from three channel catfish ( Ictalurus punctatus ). We also estimated the power required for suction feeding from oral pressure and dynamic endocast volume measurements. Cranial elevation relative to the body was small (<5 deg) and the epaxial muscles did not shorten during peak expansion power. In contrast, the hypaxial muscles consistently shortened by 4–8% to rotate the pectoral girdle 6–11 deg relative to the body. Despite only the hypaxial muscles generating power, catfish strikes were similar in power to those of other species, such as largemouth bass ( Micropterus salmoides ), that use epaxial and hypaxial muscles to power mouth expansion. These results show that the epaxial muscles are not used as motors in catfish, but suggest they position and stabilize the cranium while the hypaxial muscles power mouth expansion ventrally. Thus, axial muscles can serve fundamentally different mechanical roles in generating and controlling cranial motion during suction feeding in fishes. 

Synopsis Locomotion in most tetrapods involves coordinated efforts between appendicular and axial musculoskeletal systems, where interactions between the limbs and the ground generate vertical (GV), horizontal (GH), and mediolateral (GML) ground-reaction forces that are transmitted to the axial system. Snakes have a complete absence of external limbs and represent a fundamental shift from this perspective. The axial musculoskeletal system of snakes is their primary structure to exert, transmit, and resist all motive and reaction forces for propulsion. Their lack of limbs makes them particularly dependent on the mechanical interactions between their bodies and the environment to generate the net GH they need for forward locomotion. As organisms that locomote on their bellies, the forces that enable the various modes of snake locomotion involve two important structures: the integument and the ribs. Snakes use the integument to contact the substrate and produce a friction-reservoir that exceeds their muscle-induced propulsive forces through modulation of scale stiffness and orientation, enabling propulsion through variable environments. XROMM work and previous studies suggest that the serially repeated ribs of snakes change their cross-sectional body shape, deform to environmental irregularities, provide synergistic stabilization for other muscles, and differentially exert and transmit forces to control propulsion. The costovertebral joints of snakes have a biarticular morphology, relative to the unicapitate costovertebral joints of other squamates, that appears derived and not homologous with the ancestral bicapitate ribs of Amniota. Evidence suggests that the biarticular joints of snakes may function to buttress locomotor forces, similar to other amniotes, and provide a passive mechanism for resisting reaction forces during snake locomotion. Future comparisons with other limbless lizard taxa are necessary to tease apart the mechanics and mechanisms that produced the locomotor versatility observed within Serpentes. 

Synopsis In ray-finned fishes, the sternohyoideus (SH) is among the largest muscles in the head region and, based on its size, can potentially contribute to the overall power required for suction feeding. However, the function of the SH varies interspecifically. In largemouth bass (Micropterus salmoides) and several clariid catfishes, the SH functions similarly to a stiff ligament. In these species, the SH remains isometric and transmitts power from the hypaxial musculature to the hyoid apparatus during suction feeding. Alternatively, the SH can shorten and contribute muscle power during suction feeding, a condition observed in the bluegill sunfish (Lepomis macrochirus) and one clariid catfish. An emerging hypothesis centers on SH muscle size as a predictor of function: in fishes with a large SH, the SH shortens during suction feeding, whereas in fish with a smaller SH, the muscle may remain isometric. Here, we studied striped surfperch (Embiotoca lateralis), a species in which the SH is relatively large at 8.8% of axial muscle mass compared with 4.0% for L. macrochirus and 1.7% for M. salmoides, to determine whether the SH shortens during suction feeding and is, therefore, bifunctional—both transmitting and generating power—or remains isometric and only transmits power. We measured skeletal kinematics of the neurocranium, urohyal, and cleithrum with Video Reconstruction of Moving Morphology, along with muscle strain and shortening velocity in the SH and epaxial muscles, using a new method of 3D external marker tracking. We found mean SH shortening during suction feeding strikes (n = 22 strikes from four individual E. lateralis) was 7.2 ± 0.55% (±SEM) of initial muscle length. Mean peak speed of shortening was 4.9 ± 0.65 lengths s−1, and maximum shortening speed occurred right around peak gape when peak power is generated in suction feeding. The cleithrum of E. lateralis retracts and depresses but the urohyal retracts and depresses even more, a strong indicator of a bifunctional SH capable of not only generating its own power but also transmitting hypaxial power to the hyoid. While power production in E. lateralis is still likely dominated by the axial musculature, since even the relatively large SH of E. lateralis is only 8.8% of axial muscle mass, the SH may contribute a meaningful amount of power given its continual shortening just prior to peak gape across all strikes. These results support the finding from other groups of fishes that a large SH muscle, relative to axial muscle mass, is likely to both generate and transmit power during suction feeding.