Swimming muscles power suction feeding in largemouth bass

Abstract

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.

Keywords: XROMM; epaxial; hypaxial; muscle power; volume.

Fig. 1.

Muscles of mouth expansion in largemouth bass. Cranial (sternohyoideus, levator arcus palatini, dilator operculi, levator operculi) and axial (epaxialis, hypaxialis) muscles may contribute power to suction expansion, based on their anatomy and published muscle activity patterns.

Fig. 2.

Skeletal motions of suction expansion increase mouth cavity volume. Lateral (Left) and rostral (Right) views of an XROMM animation with the dynamic digital endocast at (A) the onset of a strike, (B) maximum mouth volume, and (C) the endocast alone at maximum mouth volume. Only the left-side bones were animated with XROMM and fit with the endocast; endocast volume was doubled to reflect the volume of the whole mouth cavity (shown by dashed outlines in B and C).

Fig. 3.

Volume, pressure, and expansion power of the mouth cavity during a sample strike. (A) Mouth volume, with skeletal and digital endocast positions at the onset of the strike and at peak mouth volume (indicated by dashed gray lines). (B) Rate of mouth volume change (left axis) and pressure inside the mouth cavity, relative to ambient (right axis). (C) Expansion power calculated as the product of pressure and rate of volume change at each time point.

Fig. 4.

Muscle length and velocity from a sample strike. Muscle length (A) is shown normalized to the mean initial muscle length (L_i), which is listed for each muscle of this individual. Decreasing length values indicate muscle shortening. Muscle velocity (B), initial muscle lengths (L_i) per second, with positive values indicating muscle shortening. The gray bars mark the time and red regions mark the length and velocity values during which expansion power magnitude was within 25% of its maximum.

Fig. 5.

Maximum (P_opt) and velocity-corrected (P_vc) muscle power capacities. Blue bars show P_opt, and boxplots show P_vc. For each muscle, mean (n = 3 fish) P_opt was calculated from bilateral muscle mass, assuming a peak isotonic power output of 216 W/kg (20). The P_vc was calculated from the mean in vivo shortening velocities of each muscle during each strike, and the pooled data from all individuals (n = 29 strikes) are shown in boxplots (open). For comparison, the expansion powers required for these strikes are shown in a boxplot (filled) on the far right. All boxplots represent the 25th and 75th percentiles of the data as the bottom and top borders of the box, the median as a red line, and the whiskers extend 1.5 times the interquartile range. The Inset graph shows the same data, but with the y axis limited to 0.5 W to visualize the power capacities of the smallest three cranial muscles.

Fig. 6.

Comparison of suction expansion power and cranial muscle power capacity. Mouth expansion power of all strikes (black lines) are graphed as a function of time for each individual. The gray dashed line indicates the maximum power capacity (P_opt) of all of the cranial muscles summed together, for each individual. The red line shows the median of the velocity-corrected power capacity (P_vc) of all of the cranial muscles summed together, with the red shaded region extending from the 25th to 75th percentiles.

Fig. S1.

Measurement of cranial muscle lengths, using X-ray reconstruction of moving morphology (XROMM) animations. For each of the four cranial muscles shown above, the length of a representative fiber (red cylinder) was measured from XROMM animations by calculating the distance between the bony attachment sites of each fiber.