New insights from serranid fishes on the role of trade-offs in suction-feeding diversification.

Suction feeding is central to prey capture in the vast majority of ray-finned fishes and has been well studied from a detailed, mechanistic perspective. Several major trade-offs are thought to have shaped the diversification of suction-feeding morphology and behavior, and have become well established in the literature. We revisited several of these expectations in a study of prey capture morphology and kinematics in 30 species of serranid fishes, a large, ecologically variable group that exhibits diverse combinations of suction and forward locomotion. We find that: (1) diversity among species in the morphological potential to generate suction changes drastically across the range of attack speeds that species use, with all species that use high-speed attacks having low capacity to generate suction, whereas slow-speed attackers exhibit the full range of suction abilities (this pattern indicates a more complex 'ram-suction continuum' than previously recognized); (2) there is no trade-off between the mechanical advantage of the lower jaw opening lever and the speed of jaw depression, revealing that this simple interpretation of lever mechanics fails to predict kinematic diversity; (3) high-speed attackers show increased cranial excursions, potentially to compensate for a decrease in accuracy; (4) the amount of jaw protrusion is positively related to attack speed, but not suction capacity; and (5) a principal component analysis revealed three significant multivariate axes of kinematic variation among species. Two of the three axes were correlated with the morphological potential to generate suction, indicating important but complex relationships between kinematics and suction potential. These results are consistent with other recent studies that show that trade-offs derived from simple biomechanical models may be less of a constraint on the evolutionary diversification of fish feeding systems than previously thought.

Suction feeding mechanics, performance, and diversity in fishes.

Despite almost 50 years of research on the functional morphology and biomechanics of suction feeding, no consensus has emerged on how to characterize suction-feeding performance, or its morphological basis. We argue that this lack of unity in the literature is due to an unusually indirect and complex linkage between the muscle contractions that power suction feeding, the skeletal movements that underlie buccal expansion, the sharp drop in buccal suction pressure that occurs during expansion, the flow of water that enters the mouth to eliminate the pressure gradient, and the forces that are ultimately exerted on the prey by this flow. This complexity has led various researchers to focus individually on suction pressure, flow velocity, or the distance the prey moves as metrics of suction-feeding performance. We attempt to integrate a mechanistic view of the ability of fish to perform these components of suction feeding. We first discuss a model that successfully relates aspects of cranial morphology to the capacity to generate suction pressure in the buccal cavity. This model is a particularly valuable tool for studying the evolution of the feeding mechanism. Second, we illustrate the multidimensional nature of suction-feeding performance in a comparison of bluegill, Lepomis macrochirus, and largemouth bass, Micropterus salmoides, two species that represent opposite ends of the spectrum of performance in suction feeding. As anticipated, bluegills had greater accuracy, lower peak flux into the mouth, and higher flow velocity and acceleration of flow than did bass. While the differences between species in accuracy of strike and peak water flux were substantial, peak suction velocity and acceleration were only about 50% higher in bluegill, a relatively modest difference. However, a hydrodynamic model of the forces that suction feeders exert on their prey shows that this difference in velocity is amplified by a positive effect of the smaller mouth aperture of bluegill on force exerted on the prey. Our model indicates that the pressure gradient in front of a fish that is feeding by suction, associated with the gradient in water velocity, results in a force on the prey that is larger than drag or acceleration reaction. A smaller mouth aperture results in a steeper pressure gradient that exerts a greater force on the prey, even when other features of the suction flow are held constant. Our work shows that some aspects of suction-feeding performance can be determined from morphology, but that the complexity of the behavior requires a diversity of perspectives to be used in order to adequately characterize performance.