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.
more »
« less
Fishes can use axial muscles as anchors or motors for powerful suction feeding
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.
more »
« less
- NSF-PAR ID:
- 10192790
- Date Published:
- Journal Name:
- The Journal of Experimental Biology
- Volume:
- 223
- Issue:
- 18
- ISSN:
- 0022-0949
- Page Range / eLocation ID:
- jeb225649
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Studies of vertebrate feeding have predominantly focused on the bones and muscles of the head, not the body. Yet, postcranial musculoskeletal structures like the spine and pectoral girdle are anatomically linked to the head, and may also have mechanical connections through which they can contribute to feeding. The feeding roles of postcranial structures have been best studied in ray-finned fishes, where the body muscles, vertebral column, and pectoral girdle attach directly to the head and help expand the mouth during suction feeding. Therefore, I use the anatomy and motion of the head–body interface in these fishes to develop a mechanical framework for studying postcranial functions during feeding. In fish the head and body are linked by the vertebral column, the pectoral girdle, and the body muscles that actuate these skeletal systems. The morphology of the joints and muscles of the cranio-vertebral and hyo-pectoral interfaces may determine the mobility of the head relative to the body, and ultimately the role of these interfaces during feeding. The postcranial interfaces can function as anchors during feeding: the body muscles and joints minimize motion between the head and body to stabilize the head or transmit forces from the body. Alternatively, the postcranial interfaces can be motors: body muscles actuate motion between the head and body to generate power for feeding motions. The motor function is likely important for many suction-feeding fishes, while the anchor function may be key for bite- or ram-feeding fishes. This framework can be used to examine the role of the postcranial interface in other vertebrate groups, and how that role changes (or not) with morphology and feeding behaviors. Such studies can expand our understanding of muscle function, as well as the evolution of vertebrate feeding behaviors across major transitions such as the invasion of land and the emergence of jaws.more » « less
-
null (Ed.)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.more » « less
-
more » « less
Abstract Living gars are a small clade of seven species that occupy an important position on the actinopterygian phylogenetic tree as members of Holostei, sister‐group to teleosts, and exhibit many plesiomorphic traits used to interpret and reconstruct early osteichthyan feeding mechanisms. Previous studies of gar feeding kinematics have focused on the ram‐based, lateral‐snapping mode of prey capture found in the narrow‐snouted
Lepisosteus genus, whereas this study focuses on a member of the broad‐snoutedAtractosteus sister‐genus, the alligator gar (Atractosteus spatula , Lacépède, 1803). High‐speed videography reveals that the feeding system of alligator gars is capable of rapid expansion from anterior to posterior, timed in a way to generate suction, counteract the effects of a bow‐wave during ram‐feeding, and direct a unidirectional flow of water through the feeding system. Reconstructed contrast‐enhanced μCT‐based cranial anatomy and three‐dimensional modeling of linkage mechanics show that a lateral‐sliding palatoquadrate, flexible intrasuspensorial joint, pivoting interhyal, and retractable pectoral girdle increase the range of motion and expansive capabilities of the alligator gar feeding mechanism. Reconstructions of muscular anatomy, inferences from in vivo kinematics, and in situ manipulations show that input from the hyoid constrictors and hypaxials play an important role in decoupling and modulating the dual roles of the sternohyoideus during feeding: hyoid retraction (jaw opening) and hyoid rotation (pharyngeal expansion). The alligator gar possesses an intricate feeding mechanism, capable of precise control with plesiomorphic muscles that represent one of the many ways the ancestral osteichthyan feeding mechanism has been modified for prey capture. -
null (Ed.)Synopsis Most predatory ray-finned fishes swallow their food whole, which can pose a significant challenge, given that prey items can be half as large as the predators themselves. How do fish transport captured food from the mouth to the stomach? Prior work indicates that, in general, fish use the pharyngeal jaws to manipulate food into the esophagus, where peristalsis is thought to take over. We used X-Ray Reconstruction of Moving Morphology to track prey transport in channel catfish (Ictalurus punctatus). By reconstructing the 3D motions of both the food and the catfish, we were able to track how the catfish move food through the head and into the stomach. Food enters the oral cavity at high velocities as a continuation of suction and stops in the approximate location of the branchial basket before moving in a much slower, more complex path toward the esophagus. This slow phase coincides with little motion in the head and no substantial mouth opening or hyoid depression. Once the prey is in the esophagus, however, its transport is surprisingly tightly correlated with gulping motions (hyoid depression, girdle retraction, hypaxial shortening, and mouth opening) of the head. Although the transport mechanism itself remains unknown, to our knowledge, this is the first description of synchrony between cranial expansion and esophageal transport in a fish. Our results provide direct evidence of prey transport within the esophagus and suggest that peristalsis may not be the sole mechanism of esophageal transport in catfish.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.225649
