More Like this

1. Bifunctional Role of the Sternohyoideus Muscle During Suction Feeding in Striped Surfperch, Embiotoca lateralis

   https://doi.org/10.1093/iob/obaa021  

   Lomax, J J ; Martinson, T F ; Jimenez, Y E ; Brainerd, E L ( January 2020 , Integrative Organismal Biology)

   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
2. Fishes can use axial muscles as anchors or motors for powerful suction feeding

   https://doi.org/10.1242/jeb.225649  

   Camp, Ariel L. ; Olsen, Aaron M. ; Hernandez, L. Patricia ; Brainerd, Elizabeth L. ( September 2020 , The Journal of Experimental Biology)

   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
3. What Fish Can Teach Us about the Feeding Functions of Postcranial Muscles and Joints

   https://doi.org/10.1093/icb/icz005  

   Camp, Ariel L ( April 2019 , Integrative and Comparative Biology)

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

   https://doi.org/10.1038/s41598-021-88828-x  

   Jimenez, Yordano E. ; Marsh, Richard L. ; Brainerd, Elizabeth L. ( May 2021 , Scientific Reports)

   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.

    

   more » « less
5. A new conceptual framework for the musculoskeletal biomechanics and physiology of ray-finned fishes

   https://doi.org/10.1242/jeb.243376  

   Camp, A.L. ; Brainerd, E.L. ( March 2022 , Journal of experimental biology)

   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. 

   more » « less