Roi Holzman

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.

Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes.

Although coral reefs are renowned biodiversity hotspots it is not known whether they also promote the evolution of exceptional ecomorphological diversity. We investigated this question by analysing a large functional morphological dataset of trophic characters within Labridae, a highly diverse group of fishes. Using an analysis that accounts for species relationships, the time available for diversification and model uncertainty we show that coral reef species have evolved functional morphological diversity twice as fast as non-reef species. In addition, coral reef species occupy 68.6% more trophic morphospace than non-reef species. Our results suggest that coral reef habitats promote the evolution of both trophic novelty and morphological diversity within fishes. Thus, the preservation of coral reefs is necessary, not only to safeguard current biological diversity but also to conserve the underlying mechanisms that can produce functional diversity in future.

Jaw protrusion enhances forces exerted on prey by suction feeding fishes.

The ability to protrude the jaws during prey capture is a hallmark of teleost fishes, widely recognized as one of the most significant innovations in their diverse and mechanically complex skull. An elaborated jaw protrusion mechanism has independently evolved multiple times in bony fishes, and is a conspicuous feature in several of their most spectacular radiations, ultimately being found in about half of the approximately 30 000 living species. Variation in jaw protrusion distance and speed is thought to have facilitated the remarkable trophic diversity found across fish groups, although the mechanical consequences of jaw protrusion for aquatic feeding performance remain unclear. Using a hydrodynamic approach, we show that rapid protrusion of the jaws towards the prey, coupled with the spatial pattern of the flow in front of the mouth, accelerates the water around the prey. Jaw protrusion provides an independent source of acceleration from that induced by the unsteady flow at the mouth aperture, increasing by up to 35% the total force exerted on attached, escaping and free-floating passive prey. Despite initiating the strike further away, fishes can increase peak force on their prey by protruding their jaws towards it, compared with a ‘non-protruding’ state, where the distance to prey remains constant throughout the strike. The force requirements for capturing aquatic prey might have served as a selective factor for the evolution of jaw protrusion in modern fishes.

An integrative modeling approach to elucidate suction-feeding performance.

SUMMARY Research on suction-feeding performance has mostly focused on measuring individual underlying components such as suction pressure, flow velocity, ram or the effects of suction-induced forces on prey movement during feeding. Although this body of work has advanced our understanding of aquatic feeding, no consensus has yet emerged on how to combine all of these variables to predict prey-capture performance. Here, we treated the aquatic predator–prey encounter as a hydrodynamic interaction between a solid particle (representing the prey) and the unsteady suction flows around it, to integrate the effects of morphology, physiology, skull kinematics, ram and fluid mechanics on suction-feeding performance. We developed the suction-induced force-field (SIFF) model to study suction-feeding performance in 18 species of centrarchid fishes, and asked what morphological and functional traits underlie the evolution of feeding performance on three types of prey. Performance gradients obtained using SIFF revealed that different trait combinations contribute to the ability to feed on attached, evasive and (strain-sensitive) zooplanktonic prey because these prey types impose different challenges on the predator. The low overlap in the importance of different traits in determining performance also indicated that the evolution of suction-feeding ability along different ecological axes is largely unconstrained. SIFF also yielded estimates of feeding ability that performed better than kinematic traits in explaining natural patterns of prey use. When compared with principal components describing variation in the kinematics of suction-feeding events, SIFF output explained significantly more variation in centrarchid diets, suggesting that the inclusion of more mechanistic hydrodynamic models holds promise for gaining insight into the evolution of aquatic feeding performance.

Scaling of suction-induced flows in bluegill: morphological and kinematic predictors for the ontogeny of feeding performance

SUMMARY During ontogeny, animals undergo changes in size and shape that result in shifts in performance, behavior and resource use. These ontogenetic changes provide an opportunity to test hypotheses about how the growth of structures affects biological functions. In the present study, we ask how ontogenetic changes in skull biomechanics affect the ability of bluegill sunfish, a high-performance suction feeder, to produce flow speeds and accelerations during suction feeding. The flow of water in front of the mouth was measured directly for fish ranging from young-of-year to large adults, using digital particle imaging velocimetry (DPIV). As bluegill size increased, the magnitude of peak flow speed they produced increased, and the effective suction distance increased because of increasing mouth size. However, throughout the size range, the timing of peak fluid speed remained unchanged, and flow was constrained to approximately one gape distance from the mouth. The observed scaling relationships between standard length and peak flow speed conformed to expectations derived from two biomechanical models, one based on morphological potential to produce suction pressure (the Suction Index model) and the other derived from a combination of morphological and kinematic variables (the Expanding Cone model). The success of these models in qualitatively predicting the observed allometry of induced flow speed reveals that the scaling of cranial morphology underlies the scaling of suction performance in bluegill.

Functional Complexity Can Mitigate Performance Trade-Offs

Trade-offs are believed to impose major constraints on adaptive evolution, and they arise when modification of a trait improves one aspect of performance but incurs a cost in another. Here we show that performance costs that result from competing demands on one trait can be mitigated by compensatory changes in other traits, so long as performance has a complex basis. Numerical simulations indicate that increases in the number of traits that determine performance decrease the strength of performance trade-offs. In centrarchid fishes, multiple traits underlie suction feeding performance, and experimental data and hydrodynamic modeling show that combinations of traits evolve to increase the ability to feed on attached prey while mitigating costs to performance on evasive prey. Diet data for centrarchid species reveal a weak trade-off between these prey types, corroborating the results based on hydrodynamic modeling and suggesting that complexity in the functional basis of suction feeding performance enhances trophic diversification. Complexity may thus permit the evolution of combinations of high-performance behaviors that appear to violate underlying trade-offs, such as the ability to exert high suction forces with large gape. This phenomenon may promote morphological, functional, and ecological diversification in the face of the myriad selective demands organisms encounter.

Hydrodynamic starvation in first-feeding larval fishes

Significance A century ago, Johan Hjort described extreme mortality rates (>99%) of marine fish larvae within days of hatching and termed it the “critical period.” Although multiple hypotheses were raised to explain this mass mortality, the mechanisms behind it remained unresolved. Here, we show that first-feeding larvae experience “hydrodynamic starvation,” in which their hydrodynamic environment mechanistically limits their feeding performance. Our study offers an experimentally supported mechanism of starvation in larval fishes, focusing on the physics of suction feeding in low Reynolds numbers, rather than on prey concentrations and encounter. We believe our findings can help to better understand the early life history of marine fish and the selective forces they experience during the pelagic larval phase. Larval fishes suffer prodigious mortality rates, eliminating 99% of the brood within a few days after first feeding. Hjort (1914) famously attributed this “critical period” of low survival to the larvae’s inability to obtain sufficient food [Hjort (1914) Rapp P-v Réun Cons Int Explor Mer 20:1–228]. However, the cause of this poor feeding success remains to be identified. Here, we show that hydrodynamic constraints on the ubiquitous suction mechanism in first-feeding larvae limit their ability to capture prey, thereby reducing their feeding rates. Dynamic-scaling experiments revealed that larval size is the primary determinant of feeding rate, independent of other ontogenetic effects. We conclude that first-feeding larvae experience “hydrodynamic starvation,” in which low Reynolds numbers mechanistically limit their feeding performance even under high prey densities. Our results provide a hydrodynamic perspective on feeding of larval fishes that focuses on the physical properties of the larvae and prey, rather than on prey concentration and the rate of encounters.

Integrating the determinants of suction feeding performance in centrarchid fishes.

SUMMARY When suction-feeding vertebrates expand their buccal cavity to draw water into their mouth, they also exert a hydrodynamic force on their prey. This force is key to strike success, directly countering forces exerted by escaping or clinging prey. While the ability to produce high flow accelerations in front of the mouth is central to the predators ability to exert high forces on the prey, several mechanisms can contribute to the disparity between the potential and realized performance through their effect on flow and acceleration as experienced by the prey. In the present study, we test how interspecific variation in gape size, mouth displacement speed and the fishs ability to locate prey at the optimal position affect variation in the force exerted on attached prey. We directly measured these forces by allowing bluegill sunfish and largemouth bass to strike at ghost shrimp tethered to a load cell that recorded force at 5000 Hz, while synchronously recording strikes with a 500 Hz video. Strike kinematics of largemouth bass were slower than that of bluegill, as were estimated flow speeds and the force exerted on the prey. This difference in force persisted after taking into account the faster suction flows and accelerations of bluegill, and was only accounted for by considering interspecific differences in gape size, mouth displacement speed and fishs ability to locate the prey at the optimal position. The contribution to interspecific differences in the force exerted on the prey was estimated to be 42% for flow speed, 25% for strike efficiency, 3% for gape size and 30% for mouth displacement speed. Hence, kinematic diversity results in substantial differences in suction performance, beyond those expected based on the capacity to generate a high flow velocity. This functional complexity, in the form of biomechanically independent mechanisms that are recruited for one function, can potentially mitigate performance trade-offs in suction-feeding fishes.

Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes

Morphological diversification does not proceed evenly across the organism. Some body parts tend to evolve at higher rates than others, and these rate biases are often attributed to sexual and natural selection or to genetic constraints. We hypothesized that variation in the rates of morphological evolution among body parts could also be related to the performance consequences of the functional systems that make up the body. Specifically, we tested the widely held expectation that the rate of evolution for a trait is negatively correlated with the strength of biomechanical trade-offs to which it is exposed. We quantified the magnitude of trade-offs acting on the morphological components of three feeding-related functional systems in four radiations of teleost fishes. After accounting for differences in the rates of morphological evolution between radiations, we found that traits that contribute more to performance trade-offs tend to evolve more rapidly, contrary to the prediction. While ecological and genetic factors are known to have strong effects on rates of phenotypic evolution, this study highlights the role of the biomechanical architecture of functional systems in biasing the rates and direction of trait evolution.

Anterior-to-posterior wave of buccal expansion in suction feeding fishes is critical for optimizing fluid flow velocity profile

In fishes that employ suction feeding, coordinating the timing of peak flow velocity with mouth opening is likely to be an important feature of prey capture success because this will allow the highest forces to be exerted on prey items when the jaws are fully extended and the flow field is at its largest. Although it has long been known that kinematics of buccal expansion in feeding fishes are characterized by an anterior-to-posterior wave of expansion, this pattern has not been incorporated in most previous computational models of suction feeding. As a consequence, these models have failed to correctly predict the timing of peak flow velocity, which according to the currently available empirical data should occur around the time of peak gape. In this study, we use a simple fluid dynamic model to demonstrate that the inclusion of an anterior-to-posterior wave of buccal expansion can correctly reproduce the empirically determined flow velocity profile, although only under very constrained conditions, whereas models that do not allow this wave of expansion inevitably predict peak velocity earlier in the strike, when the gape is less than half of its maximum. The conditions that are required to produce a realistic velocity profile are as follows: (i) a relatively long time lag between mouth opening and expansion of the more posterior parts of the mouth, (ii) a short anterior portion of the mouth relative to more posterior sections, and (iii) a pattern of movement that begins slowly and then rapidly accelerates. Greater maximum velocities were generated in simulations without the anterior-to-posterior wave of expansion, suggesting a trade-off between maximizing fluid speed and coordination of peak fluid speed with peak gape.