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Swimming muscles power suction feeding in largemouth bass
A.L. Camp*, T.J. Roberts, and E.L. Brainerd
Brown University, Providence, RI, USA
*Author for correspondence: Ariel Camp | Published article | Press release
Ray-finned fishes include over 30,000 species, and most of these fishes capture their food by suction: rapidly and forcefully expanding the mouth cavity so that water and food are accelerated inside (Movie 1). While most vertebrates rely on cranial muscles to generate feeding behaviors, it has long been recognized that both the cranial and boy muscles of fish may be contributing power for suction feeding. However, the cranial muscles of fish are relatively small (Figure 1), leading to the hypothesis that they may not be able to generate sufficient power for suction feeding, and that the large body muscles may also contribute some power to feeding.
Movie 1: External video of largemouth bass suction feeding strike. This has been slowed down 10 times, and was originally recorded at 300 frames per second.
We used X-Ray Reconstruction of Moving Morphology (XROMM) to measure the power required for suction feeding in largemouth bass (Micropterus salmoides), and compare it to the power available from cranial and body muscles. We first generated XROMM animations of the cranial skeleton (Movie 2), and then created a dynamic digital endocast to measure the volume of the mouth throughout the strike from these animations (Movie 3). These time-resolved measurements of pressure inside the mouth to calculate the power required for suction expansion in largemouth bass.
Movie 2: XROMM animation of the cranial skeleton during the suction feeding strike of a largemouth bass. This medial perspective provides a view of the inside of the mouth, and has been slowed down 10 times from real-time.
Suction expansion power was then compared to the maximum power capacity of the cranial and body muscles, estimated from muscle mass and literature values of mass-specific power output. Even assuming this maximum power capacity, all the cranial muscle together could have only powered the weakest recorded strikes. When in vivo measurements of muscle shortening were incorporated to calculate a velocity-corrected power capacity, the resulting cranial muscle power was negligible and could not have powered any strike (Figure 2). The body muscles did not merely contribute to suction expansion, but were essential for generating nearly all of the required peak expansion power.
Movie 3: Dynamic digital endocast used to measure change in mouth volume. The endocast (right) is of a 3D polygon fit to the shape of the mouth cavity, so that as the cranial skeleton expands (left), the polygon also expands and changes shape. Measuring the volume of the polygon at every frame provides the volume of the mouth cavity at each time step. This video has been slowed down 10 times from real-time.
We do not believe that largemouth bass are unique in using body muscles for feeding, but that many fishes exceed the limited power available from the small cranial muscles by instead using the massive body muscles to power suction feeding. Therefore, we need to now consider the structure and evolution of these body muscles from a new perspective, as both swimming and feeding muscles.
