Swimming muscles power suction feeding in largemouth bass

Significance Over one-half of all vertebrate species are ray-finned fishes. Across this extraordinary diversity, the most common feeding mode is suction feeding: rapid expansion of the mouth to suck in water and food. Here, we find that the power required for suction expansion is generated primarily by the axial swimming muscles. Rather than being restricted to the low power capacity of the small cranial muscles, suction-feeding fishes have co-opted the massive swimming muscles for this powerful feeding behavior. Therefore, the evolution of axial muscles in ray-finned fishes should now be considered in the context of feeding as well as locomotion, changing our perspective on musculoskeletal form and function in over 30,000 species. Most aquatic vertebrates use suction to capture food, relying on rapid expansion of the mouth cavity to accelerate water and food into the mouth. In ray-finned fishes, mouth expansion is both fast and forceful, and therefore requires considerable power. However, the cranial muscles of these fishes are relatively small and may not be able to produce enough power for suction expansion. The axial swimming muscles of these fishes also attach to the feeding apparatus and have the potential to generate mouth expansion. Because of their large size, these axial muscles could contribute substantial power to suction feeding. To determine whether suction feeding is powered primarily by axial muscles, we measured the power required for suction expansion in largemouth bass and compared it to the power capacities of the axial and cranial muscles. Using X-ray reconstruction of moving morphology (XROMM), we generated 3D animations of the mouth skeleton and created a dynamic digital endocast to measure the rate of mouth volume expansion. This time-resolved expansion rate was combined with intraoral pressure recordings to calculate the instantaneous power required for suction feeding. Peak expansion powers for all but the weakest strikes far exceeded the maximum power capacity of the cranial muscles. The axial muscles did not merely contribute but were the primary source of suction expansion power and generated up to 95% of peak expansion power. The recruitment of axial muscle power may have been crucial for the evolution of high-power suction feeding in ray-finned fishes.