Cheryl D. Wilga

Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks

Sharks as a group have a long history as highly successful predatory fishes. Although, the number of recent studies on their diet, feeding behavior, feeding mechanism, and mechanics have increased, many areas still require additional investigation. Dietary studies of sharks are generally more abundant than those on feeding activity patterns, and most of the studies are confined to relatively few species, many being carcharhiniform sharks. These studies reveal that sharks are generally asynchronous opportunistic feeders on the most abundant prey item, which are primarily other fishes. Studies of natural feeding behavior are few and many observations of feeding behavior are based on anecdotal reports. To capture their prey sharks either ram, suction, bite, filter, or use a combination of these behaviors. Foraging may be solitary or aggregate, and while cooperative foraging has been hypothesized it has not been conclusively demonstrated. Studies on the anatomy of the feeding mechanism are abundant and thorough, and far exceed the number of functional studies. Many of these studies have investigated the functional role of morphological features such as the protrusible upper jaw, but only recently have we begun to interpret the mechanics of the feeding apparatus and how it affects feeding behavior. Teeth are represented in the fossil record and are readily available in extant sharks. Therefore much is known about their morphology but again functional studies are primarily theoretical and await experimental analysis. Recent mechanistic approaches to the study of prey capture have revealed that kinematic and motor patterns are conserved in many species and that the ability to modulate feeding behavior varies greatly among taxa. In addition, the relationship of jaw suspension to feeding behavior is not as clear as was once believed, and contrary to previous interpretations upper jaw protrusibility appears to be related to the morphology of the upper jaw-chondrocranial articulation rather than the type of jaw suspension. Finally, we propose a set of specific hypotheses including: (1) The functional specialization for suction feeding hypothesis that morphological and functional specialization for suction feeding has repeatedly arisen in numerous elasmobranch lineages, (2) The aquatic suction feeding functional convergence hypothesis that similar hydrodynamic constraints in bony fishes and sharks result in convergent morphological and functional specializations for suction feeding in both groups, (3) The feeding modulation hypothesis that suction capture events in sharks are more stereotyped and therefore less modulated compared to ram and bite capture events, and (4) The independence of jaw suspension and feeding behavior hypothesis whereby the traditional categorization of jaw suspension types in sharks is not a good predictor of jaw mobility and prey capture behavior. Together with a set of questions these hypotheses help to guide future research on the feeding biology of sharks.

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.

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.

Eating without hands or tongue: specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes

The ability to separate edible from inedible portions of prey is integral to feeding. However, this is typically overlooked in favour of prey capture as a driving force in the evolution of vertebrate feeding mechanisms. In processing prey, cartilaginous fishes appear handicapped because they lack the pharyngeal jaws of most bony fishes and the muscular tongue and forelimbs of most tetrapods. We argue that the elaborate cranial muscles of some cartilaginous fishes allow complex prey processing in addition to their usual roles in prey capture. The ability to manipulate prey has evolved twice along different mechanical pathways. Batoid chondrichthyans (rays and relatives) use elaborate lower jaw muscles to process armored benthic prey, separating out energetically useless material. In contrast, megacarnivorous carcharhiniform and lamniform sharks use a diversity of upper jaw muscles to control the jaws while gouging, allowing for reduction of prey much larger than the gape. We suggest experimental methods to test these hypotheses empirically.

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.

Prey handling using whole-body fluid dynamics in batoids.

Fluid flow generated by body movements is a foraging tactic that has been exploited by many benthic species. In this study, the kinematics and hydrodynamics of prey handling behavior in little skates, Leucoraja erinacea, and round stingrays, Urobatis halleri, are compared using kinematics and particle image velocimetry. Both species use the body to form a tent to constrain the prey with the pectoral fin edges pressed against the substrate. Stingrays then elevate the head, which increases the volume between the body and the substrate to generate suction, while maintaining pectoral fin contact with the substrate. Meanwhile, the tip of the rostrum is curled upwards to create an opening where fluid is drawn under the body, functionally analogous to suction-feeding fishes. Skates also rotate the rostrum upwards although with the open rostral sides and the smaller fin area weaker fluid flow is generated. However, skates also use a rostral strike behavior in which the rostrum is rapidly rotated downwards pushing fluid towards the substrate to potentially stun or uncover prey. Thus, both species use the anterior portion of the body to direct fluid flow to handle prey albeit in different ways, which may be explained by differences in morphology. Rostral stiffness and pectoral fin insertion onto the rostrum differ between skates and rays and this corresponds to behavioral differences in prey handling resulting in distinct fluid flow patterns. The flexible muscular rostrum and greater fin area of stingrays allow more extensive use of suction to handle prey while the stiff cartilaginous rostrum of skates lacking extensive fin insertion is used as a paddle to strike prey as well as to clear away sand cover.

Evolution of asynchronous motor activity in paired muscles: effects of ecology, morphology, and phylogeny

Many studies of feeding behavior have implanted electrodes unilaterally (in muscles on only one side of the head) to determine the basic motor patterns of muscles controlling the jaws. However, bilateral implantation has the potential to achieve a more comprehensive understanding of modification of the motor activity that may be occurring between the left and right sides of the head. In particular, complex processing of prey is often characterized by bilaterally asynchronous and even unilateral activation of the jaw musculature. In this study, we bilaterally implant feeding muscles in species from four orders of elasmobranchs (Squaliformes, Orectolobiformes, Carcharhiniformes, Rajoidea) in order to characterize the effects of type of prey, feeding behavior, and phylogeny on the degree of asynchronous muscle activation. Electrodes were implanted in three of the jaw adductors, two divisions of the quadratomandibularis and the preorbitalis, as well as in a cranial elevator in sharks, the epaxialis. The asynchrony of feeding events (measured as the degree to which activity of members of a muscle pair is out of phase) was compared across species for capture versus processing and simple versus complex prey, then interpreted in the contexts of phylogeny, morphology, and ecology to clarify determinants of asynchronous activity. Whereas capture and processing of prey were characterized by statistically similar degrees of asynchrony for data pooled across species, events involving complex prey were more asynchronous than were those involving simple prey. The two trophic generalists, Squalus acanthias and Leucoraja erinacea, modulated the degree of asynchrony according to type of prey, whereas the two behavioral specialists, Chiloscyllium plagiosum and Mustelus canis, activated the cranial muscles synchronously regardless of type of prey. These differences in jaw muscle activity would not have been detected with unilateral implantation. Therefore, we advocate bilateral implantation in studies of cranial muscle function in fishes, particularly when investigating behaviors associated with processing complex prey. Incorporating this methodology will provide a more detailed understanding of the coordination and evolution of paired-muscle function in the feeding apparatus relative to behavioral and ecological performance.

Jaws for a spiral-tooth whorl: CT images reveal novel adaptation and phylogeny in fossil Helicoprion

New CT scans of the spiral-tooth fossil, Helicoprion, resolve a longstanding mystery concerning the form and phylogeny of this ancient cartilaginous fish. We present the first three-dimensional images that show the tooth whorl occupying the entire mandibular arch, and which is supported along the midline of the lower jaw. Several characters of the upper jaw show that it articulated with the neurocranium in two places and that the hyomandibula was not part of the jaw suspension. These features identify Helicoprion as a member of the stem holocephalan group Euchondrocephali. Our reconstruction illustrates novel adaptations, such as lateral cartilage to buttress the tooth whorl, which accommodated the unusual trait of continuous addition and retention of teeth in a predatory chondrichthyan. Helicoprion exemplifies the climax of stem holocephalan diversification and body size in Late Palaeozoic seas, a role dominated today by sharks and rays.

Ontogeny of head and caudal fin shape of an apex marine predator: The tiger shark (Galeocerdo cuvier)

How morphology changes with size can have profound effects on the life history and ecology of an animal. For apex predators that can impact higher level ecosystem processes, such changes may have consequences for other species. Tiger sharks (Galeocerdo cuvier) are an apex predator in tropical seas, and, as adults, are highly migratory. However, little is known about ontogenetic changes in their body form, especially in relation to two aspects of shape that influence locomotion (caudal fin) and feeding (head shape). We captured digital images of the heads and caudal fins of live tiger sharks from Southern Florida and the Bahamas ranging in body size (hence age), and quantified shape of each using elliptical Fourier analysis. This revealed changes in the shape of the head and caudal fin of tiger sharks across ontogeny. Smaller juvenile tiger sharks show an asymmetrical tail with the dorsal (upper) lobe being substantially larger than the ventral (lower) lobe, and transition to more symmetrical tail in larger adults, although the upper lobe remains relatively larger in adults. The heads of juvenile tiger sharks are more conical, which transition to relatively broader heads over ontogeny. We interpret these changes as a result of two ecological transitions. First, adult tiger sharks can undertake extensive migrations and a more symmetrical tail could be more efficient for swimming longer distances, although we did not test this possibility. Second, adult tiger sharks expand their diet to consume larger and more diverse prey with age (turtles, mammals, and elasmobranchs), which requires substantially greater bite area and force to process. In contrast, juvenile tiger sharks consume smaller prey, such as fishes, crustaceans, and invertebrates. Our data reveal significant morphological shifts in an apex predator, which could have effects for other species that tiger sharks consume and interact with. J. Morphol. 277:556–564, 2016.

Anatomy and muscle activity of the dorsal fins in bamboo sharks and spiny dogfish during turning maneuvers.

Stability and procured instability characterize two opposing types of swimming, steady and maneuvering, respectively. Fins can be used to manipulate flow to adjust stability during swimming maneuvers either actively using muscle control or passively by structural control. The function of the dorsal fins during turning maneuvering in two shark species with different swimming modes is investigated here using musculoskeletal anatomy and muscle function. White‐spotted bamboo sharks are a benthic species that inhabits complex reef habitats and thus have high requirements for maneuverability. Spiny dogfish occupy a variety of coastal and continental shelf habitats and spend relatively more time cruising in open water. These species differ in dorsal fin morphology and fin position along the body. Bamboo sharks have a larger second dorsal fin area and proportionally more muscle insertion into both dorsal fins. The basal and radial pterygiophores are plate‐like structures in spiny dogfish and are nearly indistinguishable from one another. In contrast, bamboo sharks lack basal pterygiophores, while the radial pterygiophores form two rows of elongated rectangular elements that articulate with one another. The dorsal fin muscles are composed of a large muscle mass that extends over the ceratotrichia overlying the radials in spiny dogfish. However, in bamboo sharks, the muscle mass is divided into multiple distinct muscles that insert onto the ceratotrichia. During turning maneuvers, the dorsal fin muscles are active in both species with no differences in onset between fin sides. Spiny dogfish have longer burst durations on the outer fin side, which is consistent with opposing resistance to the medium. In bamboo sharks, bilateral activation of the dorsal in muscles could also be stiffening the fin throughout the turn. Thus, dogfish sharks passively stiffen the dorsal fin structurally and functionally, while bamboo sharks have more flexible dorsal fins, which result from a steady swimming trade off. J. Morphol. 274:1288–1298, 2013.