Abstract

The vast majority of ray-finned fishes capture prey through suction feeding. The basis of this behavior is the generation of subambient pressure through rapid expansion of a highly kinetic skull. Over the last four decades, results from in vivo experiments have elucidated the general relationships between morphological parameters and subambient pressure generation. Until now, however, researchers have been unable to tease apart the discrete contributions of, and complex relationships among, the musculoskeletal elements that support buccal expansion. Fortunately, over the last decade, biorobotic models have gained a foothold in comparative research and show great promise in addressing long-standing questions in vertebrate biomechanics. In this paper, we present BassBot, a biorobotic model of the head of the largemouth bass (Micropterus salmoides). BassBot incorporates a 3D acrylic plastic armature of the neurocranium, maxillary apparatus, lower jaw, hyoid, suspensorium and opercular apparatus. Programming of linear motors permits precise reproduction of live kinematic behaviors including hyoid depression and rotation, premaxillary protrusion, and lateral expansion of the suspensoria. BassBot reproduced faithful kinematic and pressure dynamics relative to live bass. We show that motor program speed has a direct relationship to subambient pressure generation. Like vertebrate muscle, the linear motors that powered kinematics were able to produce larger magnitudes of force at slower velocities and, thus, were able to accelerate linkages more quickly and generate larger magnitudes of subambient pressure. In addition, we demonstrate that disrupting the kinematic behavior of the hyoid interferes with the anterior-to-posterior expansion gradient. This resulted in a significant reduction in subambient pressure generation and pressure impulse of 51% and 64%, respectively. These results reveal the promise biorobotic models have for isolating individual parameters and assessing their role in suction feeding.

Highlights

  • The majority of ray-finned fishes capture prey by suction feeding, a behavior dependent on the generation of subambient pressure through rapid expansion of the buccal cavity (Fig. 1)

  • Robotic kinematic behavior was similar to live bass behavior and generalized kinematic patterns of suction feeding fishes in that the buccal cavity expansion proceeds in an anterior-to-posterior progression, expanding dorsoventrally and laterally to generate subambient pressure

  • Dorsoventral expansion in live and robotic bass was accomplished by ventral rotations of the lower jaw and hyoid relative to the neurocranium

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Summary

Introduction

The majority of ray-finned fishes (actinopterygians) capture prey by suction feeding, a behavior dependent on the generation of subambient pressure through rapid expansion of the buccal cavity (Fig. 1). Rapid expansion of the buccal cavity results from orchestrated movements of linkages that form a highly kinetic skull, including rotation of the lower jaw, ventral rotation and depression of the hyoid apparatus, lateral expansion of the suspensoria, and dorsal rotation of the cranium about the axial skeleton (Alexander, 1967; Lauder, 1980a, 1985) This model of suction feeding is based largely on data from in vivo experimentation on a number of ray-finned fishes, in addition to more recent work on selected elasmobranchs The relationship between the complex motion of musculoskeletal elements in the head and negative pressure generation inside the buccopharyngeal cavity, as well as the discrete contributions to suction generation of each musculoskeletal unit, is still not clear (Sanford and Wainwright, 2002; Wainwright et al, 2007) To address questions such as these and understand the influence of individual components of suction-feeding systems of fishes, it is clear that a new line of attack is required. Studies of feeding systems in live animals are limited in their ability to determine causal relationships between kinematics and suction performance

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