Christopher P. J. Sanford

Evolution and ecology of feeding in elasmobranchs.

Paleozoic chondrichthyans had a large gape, numerous spike-like teeth, limited cranial kinesis, and a non-suspensory hyoid, suggesting a feeding mechanism dominated by bite and ram. Modern sharks are characterized by a mobile upper jaw braced by a suspensory hyoid arch that is highly kinetic. In batoids, the upper jaw is dissociated from the cranium permitting extensive protrusion of the jaws. Similar to actinopterygians, the evolution of highly mobile mandibular and hyoid elements has been correlated with extensive radiation of feeding modes in elasmobranchs, particularly that of suction. Modern elasmobranchs possess a remarkable variety of feeding modes for a group containing so few species. Biting, suction or filter-feeding may be used in conjunction with ram to capture prey, with most species able to use a combination of behaviors during a strike. Suction-feeding has repeatedly arisen within all recent major elasmobranch clades and is associated with a suite of morphological and behavioral specializations. Prey capture in a diverse assemblage of purported suction-feeding elasmobranchs is investigated in this study. Drop in water pressure measured in the mouth and at the location of the prey shows that suction inflow drops off rapidly with distance from the predators mouth. Elasmobranchs specializing in suction-feeding may be limited to bottom associated prey and because of their small gape may have a diet restricted to relatively small prey. Behavior can affect performance and overcome constraints imposed by the fluid medium. Suction performance can be enhanced by proximity to a substrate or by decreasing distance from predator to prey using various morphological and/or behavioral characteristics. Benthic suction-feeders benefit by the increased strike radius due to deflection of water flow when feeding close to a substrate, and perhaps require less accuracy when capturing prey. Suction and ram-suction-feeding elasmobranchs can also use suction inflow to draw prey to them from a short distance, while ram-feeding sharks must accelerate and overtake the prey. The relationship between feeding strategy and ecology may depend in part on ecological, mechanistic or evolutionary specialization. Mechanistic suction-feeding specialist elasmobranchs are primarily benthic, while most epibenthic and pelagic elasmobranchs are generalists and use ram, suction, and biting to catch a diversity of prey in various habitats. Some shark species are considered to be ecological specialists in choosing certain kinds of prey over others. Batoids are evolutionary specialists in having a flattened morphology and most are generalist feeders. Filter-feeding elasmobranchs are ecological, mechanistic, and evolutionary specialists.

Evolution of Motor Patterns: Aquatic Feeding in Salamanders and Ray-Finned Fishes

Patterns of muscle activity (motor patterns) have generally been found to be strongly conserved during the evolution of aquatic feeding behavior within closely related groups of fishes and salamanders. We conducted a test of the generality of motor pattern conservation with a much broader phylogenetic scope than has been done previously. Activity patterns of three cranial muscles were quantified from electromyographic (EMG) recordings made during suction feeding in a salamander (Ambystoma mexicanum) and 4 widely divergent species of ray-finned fishes (Amia calva, Notopterus chitala, Micropterus salmoides and Lepomis macrochirus). General features of the motor pattern were the same in all species, but multivariate and univariate analyses of variance revealed highly significant differences among the 5 species in the average muscle activity pattern, indicating that the motor pattern has not been precisely conserved among these 5 taxa. Five of eight EMG variables that describe the intensity and timing of muscle activity differed among species. Only the intensity of activity of the adductor mandibulae appears to be a strongly conserved feature of the suction feeding motor pattern in anamniotes. A discriminant function analysis of the 8 EMG variables successfully classified about two thirds of the feeding incidents as belonging to the correct species. In contrast to the results of previous studies of closely related taxa, we found that numerous quantitative differences exist among species, indicating that functionally significant details of suction feeding motor patterns have changed during evolution, whereas several general features of the pattern have been conserved.

Hydrodynamics of prey capture in sharks: effects of substrate

In suction feeding, a volume of water is drawn into the mouth of a predator. Previous studies of suction feeding in fishes have shown that significant fluid velocities are confined to a region within one mouth width from the mouth. Therefore, the predator must be relatively close to the prey to ensure capture success. Here, theoretical modelling is combined with empirical data to unravel the mechanism behind feeding on a substrate. First, we approached the problem theoretically by combining the stream functions of two sinks. Computational fluid dynamics modelling is then applied to make quantitative predictions regarding the effects of substrate proximity on the feeding hydrodynamics of a benthic shark. An oblique circular cylinder and a shark head model were used. To test the models, we used digital particle image velocimetry to record fluid flow around the mouth of white-spotted bamboo sharks, Chiloscyllium plagiosum, during suction feeding on the substrate and in the water column. Empirical results confirmed the modelling predictions: the length of the flow field can be doubled due to passive substrate effects during prey capture. Feeding near a substrate extends the distance over which suction is effective and a predator strike can be effective further from the prey.

Suction Generation in White-Spotted Bamboo Sharks Chiloscyllium Plagiosum

SUMMARY After the divergence of chondrichthyans and teleostomes, the structure of the feeding apparatus also diverged leading to alterations in the suction mechanism. In this study we investigated the mechanism for suction generation during feeding in white-spotted bamboo sharks, Chiloscyllium plagiosum and compared it with that in teleosts. The internal movement of cranial elements and pressure in the buccal, hyoid and pharyngeal cavities that are directly responsible for suction generation was quantified using sonomicrometry and pressure transducers. Backward stepwise multiple linear regressions were used to explore the relationship between expansion and pressure, accounting for 60–96% of the variation in pressure among capture events. The progression of anterior to posterior expansion in the buccal, hyoid and pharyngeal cavities is accompanied by the sequential onset of subambient pressure in these cavities as prey is drawn into the mouth. Gape opening triggers the onset of subambient pressure in the oropharyngeal cavities. Peak gape area coincides with peak subambient buccal pressure. Increased velocity of hyoid area expansion is primarily responsible for generating peak subambient pressure in the buccal and hyoid regions. Pharyngeal expansion appears to function as a sink to receive water influx from the mouth, much like that of compensatory suction in bidirectional aquatic feeders. Interestingly, C. plagiosum generates large suction pressures while paradoxically compressing the buccal cavity laterally, delaying the time to peak pressure. This represents a fundamental difference from the mechanism used to generate suction in teleost fishes. Interestingly, pressure in the three cavities peaks in the posterior to anterior direction. The complex shape changes that the buccal cavity undergoes indicate that, as in teleosts, unsteady flow predominates during suction feeding. Several kinematic variables function together, with great variation over long gape cycles to generate the low subambient pressures used by C. plagiosum to capture prey.

Functional morphology of the “tongue-bite” in the osteoglossomorph fish Notopterus

Osteoglossomorph fishes are characterized by having three sets of jaws: a mandibular jaw apparatus (MJA) anteriorly, a pharyngeal jaw apparatus (PJA) posteriorly, and a tongue‐bite apparatus (TBA) associated with basihyal and parasphenoid teeth. The TBA is a novel complex feature of the head that characterizes osteoglossomorph fishes and provides a case study in the origin of novel functions and roles in the vertebrate musculoskeletal system.

Is a convergently derived muscle-activity pattern driving novel raking behaviours in teleost fishes?

SUMMARY Behavioural differences across prey-capture and processing mechanisms may be governed by coupled or uncoupled feeding systems. Osteoglossomorph and salmonid fishes process prey in a convergently evolved tongue-bite apparatus (TBA), which is musculoskeletally coupled with the primary oral jaws. Altered muscle-activity patterns (MAPs) in these coupled jaw systems could be associated with the independent origin of a novel raking behaviour in these unrelated lineages. Substantial MAP changes in the evolution of novel behaviours have rarely been quantified so we examined MAP differences across strikes, chewing and rakes in a derived raking salmonid, the rainbow trout, Oncorhynchus mykiss. Electromyography, including activity onset timing, duration, mean amplitude and integrated area from five feeding muscles revealed significant differences between behaviour-specific MAPs. Specifically, early activity onset in the protractor hyoideus and adductor mandibularis muscles characterised raking, congruent with a recent biomechanical model of the component-mechanisms driving the raking preparatory and power-stroke phases. Oncorhynchus raking MAPs were then compared with a phylogenetically derived osteoglossomorph representative, the Australian arowana, Scleropages jardinii. In both taxa, early onset of protractor hyoideus and adductor mandibularis activity characterised the raking preparatory phase, indicating a convergently derived MAP, while more subtle inter-lineage divergence in raking MAPs resulted from onset-timing and duration differences in sternohyoideus and hypaxialis activity. Convergent TBA morphologies are thus powered by convergently derived MAPs, a phenomenon not previously demonstrated in feeding mechanisms. Between lineages, differences in TBA morphology and associated differences in the functional coupling of jaw systems appear to be important factors in shaping the diversification of raking behaviours.

Congruence between muscle activity and kinematics in a convergently derived prey-processing behavior

Quantification of anatomical and physiological characteristics of the function of a musculoskeletal system may yield a detailed understanding of how the organizational levels of morphology, biomechanics, kinematics, and muscle activity patterns (MAPs) influence behavioral diversity. Using separate analyses of these organizational levels in representative study taxa, we sought patterns of congruence in how organizational levels drive behavioral modulation in a novel raking prey-processing behavior found in teleosts belonging to two evolutionarily distinct lineages. Biomechanically divergent prey (elusive, robust goldfish and sedentary, malleable earthworms) were fed to knifefish, Chitala ornata (Osteoglossomorpha) and brook trout, Salvelinus fontinalis (Salmoniformes). Electromyography recorded MAPs from the hyoid protractor, jaw adductor, sternohyoideus, epaxialis, and hypaxialis musculature, while sonomicrometry sampled deep basihyal kinesis and contractile length dynamics in the basihyal protractor and retractor muscles. Syntheses of our results with recent analyses of cranial morphology and raking kinematics showed that raking in Salvelinus relies on an elongated cranial out lever, extensive cranial elevation and a curved cleithrobranchial ligament (CBL), and that both raking MAPs and kinematics remain entirely unmodulated-a highly unusual trait, particularly among feeding generalists. Chitala had a shorter CBL and a raking power stroke involving increased retraction of the elongated pectoral girdle during raking on goldfish. The raking MAP was also modulated in Chitala, involving an extensive overlap between muscle activity of the preparatory and power stroke phases, driven by shifts in hypaxial timing and recruitment of the hyoid protractor muscle. Sonomicrometry revealed that the protractor hyoideus muscle stored energy from retraction of the pectoral girdle for ca. 5-20 ms after onset of the power stroke and then hyper-extended. This mechanism of elastic recoil in Chitala, which amplifies retraction of the basihyal during raking on goldfish without a significant increase in recruitment of the hypaxialis, suggests a unique mechanism of modulation based on performance-enhancing changes in the design and function of the musculoskeletal system.

Rhythmic chewing with oral jaws in teleost fishes: a comparison with amniotes.

SUMMARY Intra-oral prey processing (chewing) using the mandibular jaws occurs more extensively among teleost fishes than previously documented. The lack of muscle spindles, γ-motoneurons and periodontal afferents in fishes makes them useful for testing hypotheses regarding the relationship between these sensorimotor components and rhythmic chewing in vertebrates. Electromyography (EMG) data from the adductor mandibulae (AM) were used to quantify variation in chew cycle duration in the bowfin Amia, three osteoglossomorphs (bony-tongues), four salmonids and one esocid (pike). All species chewed prey using their oral jaw in repetitive trains of between 3 and 30 consecutive chews, a pattern that resembles cyclic chewing in amniote vertebrates. Variance in rhythmicity was compared within and between lineages using coefficients of variation and Levenes test for homogeneity of variance. These comparisons revealed that some teleosts exhibit degrees of rhythmicity that are comparable to mammalian mastication and higher than in lepidosaurs. Moreover, chew cycle durations in fishes, as in mammals, scale positively with mandible length. Chewing among basal teleosts may be rhythmic because it is stereotyped and inflexible, the result of patterned interactions between sensory feedback and a central pattern generator, because the lack of a fleshy tongue renders jaw–tongue coordination unnecessary and/or because stereotyped opening and closing movements are important for controlling fluid flow in the oral cavity.

Biomechanics of a convergently derived prey-processing mechanism in fishes: evidence from comparative tongue bite apparatus morphology and raking kinematics

SUMMARY A tongue-bite apparatus (TBA) governs raking behaviors in two major and unrelated teleost lineages, the osteoglossomorph and salmoniform fishes. We present data on comparative morphology and kinematics from two representative species, the rainbow trout (Oncorhynchus mykiss) and the Australian arowana (Scleropages jardinii), which suggest that both the TBA and raking are convergently derived in these lineages. Similar TBA morphologies were present, except for differences in TBA dentition and shape of the novel cleithrobranchial ligament (CBL), which is arc-shaped in O. mykiss and straight in S. jardinii. Eight kinematic variables were used to quantify motion magnitude and maximum-timing in the kinematic input mechanisms of the TBA. Five variables differed inter-specifically (pectoral girdle retraction magnitude and timing, cranial and hyoid elevation and gape-distance timing), yet an incomplete taxon separation across multivariate kinematic space demonstrated an overall similarity in raking behavior. An outgroup analysis using bowfin (Amia calva) and pickerel (Esox americanus) to compare kinematics of raking with chewing and prey-capture provided robust quantitative evidence of raking being a convergently derived behavior. Support was also found for the notion that raking more likely evolved from the strike, a functionally distinct behavior, than from chewing, an alternative prey-processing behavior. Based on raking kinematic and muscle-activity data, we propose biomechanical models of the three input mechanisms that govern kinematics of the basihyal output mechanism during the raking power stroke: (1) cranial elevation protracts the upper TBA jaw from the lower (basihyal) TBA jaw; (2) basihyal retraction is caused directly by contraction of the sternohyoideus (SH); (3) hypaxial shortening, relayed via the pectoral girdle and SH–CBL complex, is an indirect basihyal retraction mechanism modeled as a four-bar linkage. These models will aid future analyses mapping structural and functional traits to the evolution of behaviors.

Kinematics of ribbon‐fin locomotion in the bowfin, Amia calva

An elongated dorsal and/or anal ribbon-fin to produce forward and backward propulsion has independently evolved in several groups of fishes. In these fishes, fin ray movements along the fin generate a series of waves that drive propulsion. There are no published data on the use of the dorsal ribbon-fin in the basal freshwater bowfin, Amia calva. In this study, frequency, amplitude, wavelength, and wave speed along the fin were measured in Amia swimming at different speeds (up to 1.0 body length/sec) to understand how the ribbon-fin generates propulsion. These wave properties were analyzed to (1) determine whether regional specialization occurs along the ribbon-fin, and (2) to reveal how the undulatory waves are used to control swimming speed. Wave properties were also compared between swimming with sole use of the ribbon-fin, and swimming with simultaneous use of the ribbon and pectoral fins. Statistical analysis of ribbon-fin kinematics revealed no differences in kinematic patterns along the ribbon-fin, and that forward propulsive speed in Amia is controlled by the frequency of the wave in the ribbon-fin, irrespective of the contribution of the pectoral fin. This study is the first kinematic analysis of the ribbon-fin in a basal fish and the model species for Amiiform locomotion, providing a basis for understanding ribbon-fin locomotion among a broad range of teleosts.