Morphology and evolution of the jaw suspension in lamniform sharks.

The morphology of the jaw suspension and jaw protrusion mechanism in lamniform sharks is described and mapped onto a cladogram to investigate how changes in jaw suspension and protrusion have evolved. This has revealed that several evolutionary modifications in the musculoskeletal apparatus of the jaws have taken place among lamniform sharks. Galeomorph sharks (Carcharhiniformes, Lamniformes, Orectolobiformes, and Heterodontiformes) have paired ethmopalatine ligaments connecting the ethmoid process of the upper jaw to the ethmoid region of the cranium. Basal lamniform sharks also acquired a novel single palatonasal ligament connecting the symphysis of the upper jaw to the cranium mid-ventral to the nasal capsule. Sharks in the family Lamnidae subsequently lost the original paired ethmopalatine ligament while retaining the novel palatonasal ligament. Thus, basal lamniform taxa (Mitsukurina owstoni, Carcharius taurus, Alopias vulpinnis) have increased ligamentous support of the lateral region of the upper jaw while derived species (Lamnidae) have lost this lateral support but gained anterior support. In previous studies the morphology of the jaw suspension has been shown to play a major role in the mechanism of upper jaw protrusion in elasmobranchs. The preorbitalis is the primary muscle effecting upper jaw protrusion in squalean (sister group to galeomorphs) and carcharhiniform (sister group to lamniforms) sharks. The preorbitalis originates from the quadratomandibularis muscle and inserts onto the nasal capsule in squalean and carcharhiniform sharks. Carcharhiniform sharks have evolved a subdivided preorbitalis muscle with the new division inserting near the ethmoid process of the palatoquadrate (upper jaw). Alopid sharks have also independently evolved a partially subdivided preorbitalis with the new division inserting at the base of the ethmoid process and surrounding connective tissue. Lamnid sharks have retained the two preorbitalis divisions but have modified both of the insertion points. The original ventral preorbitalis division now inserts onto the connective tissue surrounding the mid-region of the upper jaw, while the new dorsal preorbitalis division inserts onto the surrounding connective tissue and skin at a more posterior position on the upper jaw. The retractor muscle of the jaws, the levator hyomandibularis, has also been modified during the evolution of lamniform sharks. In most sharks, including basal lamniforms, the levator hyomandibularis inserts onto the hyomandibula and functions to retract the jaws after protrusion. In alopid and lamnid sharks the levator hyomandibularis inserts primarily onto the upper and lower jaws around the jaw joint and is a more direct route for retracting the jaws. Thus, there has been at least one instance of character loss (ethmopalatine ligament), acquisition (palatonasal ligament), subdivision (preorbitalis), and modification (ventral preorbitalis, dorsal preorbitalis, and levator hyomandibularis) in the ligaments and muscles associated with the jaw suspension and jaw protrusion mechanism in lamniform sharks. While derived lamniform sharks (Lamna nasus, Carcharodon carcharius, and Isurus oxyrinchus) lost the ancestral passive lateral support of the ethmoid articulation of the upper jaw, they simultaneously acquired muscular support by way of the levator hyomandibularis, which provides a dynamic mechanism for lateral support. The evolution of multiple divisions of preorbitalis insertions onto the palatoquadrate and modification of the levator hyomandibularis insertion directly onto the jaws provides an active mechanism for multiple protractions and retractions of the upper jaw, which is advantageous in those sharks that gouge or saw pieces from large oversized prey items.

Biomechanics: hydrodynamic function of the shark's tail.

The tail of most sharks has an elongated upper lobe that differs from the externally symmetrical tail structure common among bony fishes, but the hydrodynamic purpose of this asymmetric tail shape is unclear. Here we quantify water flow patterns in the wakes of freely swimming dogfish sharks and find that they have a ring-within-a-ring vortex structure, in contrast to the single rings shed by symmetrical fish tails. The branched-ring vortex is generated by the inclined angle of the tail's trailing edge and by its motion at an angle to the horizontal body axis; the vortex directs water backwards and downwards, which may increase the shark's vertical manoeuvrability.

Function of the heterocercal tail in sharks: quantitative wake dynamics during steady horizontal swimming and vertical maneuvering.

The function of the heterocercal tail in sharks has long been debated in the literature. Previous kinematic data have supported the classical theory which proposes that the beating of the heterocercal caudal fin during steady horizontal locomotion pushes posteroventrally on the water, generating a reactive force directed anterodorsally and causing rotation around the center of mass. An alternative model suggests that the heterocercal shark tail functions to direct reaction forces through the center of mass. In this paper, we quantify the function of the tail in two species of shark and compare shark tail function with previous hydrodynamic data on the heterocercal tail of sturgeon Acipenser transmontanus. To address the two models of shark heterocercal tail function, we applied the technique of digital particle image velocimetry (DPIV) to quantify the wake of two species of shark swimming in a flow tank. Both steady horizontal locomotion and vertical maneuvering were analyzed. We used DPIV with both horizontal and vertical light sheet orientations to quantify patterns of wake velocity and vorticity behind the heterocercal tail of leopard sharks (Triakis semifasciata) and bamboo sharks (Chiloscyllium punctatum) swimming at 1.0Ls(-1), where L is total body length. Two synchronized high-speed video cameras allowed simultaneous measurement of shark body position and wake structure. We measured the orientation of tail vortices shed into the wake and the orientation of the central jet through the core of these vortices relative to body orientation. Analysis of flow geometry indicates that the tail of both leopard and bamboo shark generates strongly tilted vortex rings with a mean jet angle of approximately 30 degrees below horizontal during steady horizontal swimming. The corresponding angle of the reaction force is much greater than body angle (mean 11 degrees ) and the angle of the path of motion of the center of mass (mean approximately 0 degrees ), thus strongly supporting the classical model of heterocercal tail function for steady horizontal locomotion. Vortex jet angle varies significantly with body angle changes during vertical maneuvering, but sharks show no evidence of active reorientation of jet angle relative to body angle, as was seen in a previous study on the function of sturgeon tail. Vortex jet orientation is significantly more inclined than the relatively horizontal jet generated by sturgeon tail vortex rings, demonstrating substantial differences in function in the heterocercal tails of sharks and sturgeon. We present a summary of forces on a swimming shark integrating data obtained here on the tail with previous data on pectoral fin and body function. Body orientation plays a critical role in the overall force balance and compensates for torques generated by the tail. The pectoral fins do not generate lift during steady horizontal locomotion, but play an important hydrodynamic role during vertical maneuvering.

Functional morphology of the pectoral fins in bamboo sharks, Chiloscyllium plagiosum: benthic vs. pelagic station-holding.

Bamboo sharks (Chiloscyllium plagiosum) are primarily benthic and use their relatively flexible pectoral and pelvic fins to rest on and move about the substrate. We examined the morphology of the pectoral fins and investigated their locomotory function to determine if pectoral fin function during both benthic station-holding and pelagic swimming differs from fin function described previously in leopard sharks, Triakis semifasciata. We used three-dimensional kinematics and digital particle image velocimetry (DPIV) to quantify pectoral fin function in five white-spotted bamboo sharks, C. plagiosum, during four behaviors: holding station on the substrate, steady horizontal swimming, and rising and sinking during swimming. During benthic station-holding in current flow, bamboo sharks decrease body angle and adjust pectoral fin angle to shed a clockwise fluid vortex. This vortex generates negative lift more than eight times that produced during open water vertical maneuvering and also results in an upstream flow that pushes against the posterior surface of the pectoral fin to oppose drag. In contrast, there is no evidence of significant lift force in the wake of the pectoral fin during steady horizontal swimming. The pectoral fin is held concave downward and at a negative dihedral angle during steady horizontal swimming, promoting maneuverability rather than stability, although this negative dihedral angle is much less than that observed previously in sturgeon and leopard sharks. During sinking, the pectoral fins are held concave upward and shed a clockwise vortex with a negative lift force, while in rising the pectoral fin is held concave downward and sheds a counterclockwise vortex with a positive lift force. Bamboo sharks appear to sacrifice maneuverability for stability when locomoting in the water column and use their relatively flexible fins to generate strong negative lift forces when holding position on the substrate and to enhance stability when swimming in the water column.

Durophagy in sharks: feeding mechanics of the hammerhead Sphyrna tiburo.

This study investigates the motor pattern and head movements during feeding of a durophagus shark, the bonnethead Sphyrna tiburo, using electromyography and simultaneous high-speed video. Sphyrna tiburo feeds almost exclusively on hard-shelled crabs, with shrimp and fish taken occasionally. It captures crabs by ram feeding, then processes or reduces the prey by crushing it between molariform teeth, finally transporting the prey by suction for swallowing. The prey-crushing mechanism is distinct from that of ram or bite capture and suction transport. This crushing mechanism is accomplished by altering the duration of jaw adductor muscle activity and modifying jaw kinematics by the addition of a second jaw-closing phase. In crushing events, motor activity of the jaw adductor muscles continues (biting of the prey occurs as the jaws close and continues after the jaws have closed) throughout a second jaw-closing phase, unlike capture and transport events during which motor activity (biting) ceases at jaw closure. Sphyrna tiburo is able to take advantage of a resource (hard prey) that is not readily available to most sharks by utilizing a suite of durophagous characteristics: molariform teeth, a modified jaw protrusor muscle, altered jaw adductor activity and modified jaw kinematics. Sphyrna tiburo is a specialist feeder on crab prey as demonstrated by the lack of differences in kinematic or motor patterns when offered prey of differing hardness and its apparent lack of ability to modulate its behavior when feeding on other prey. Functional patterns are altered and coupled with modifications in dental and jaw morphology to produce diverse crushing behaviors in elasmobranchs.

Three-dimensional kinematics and wake structure of the pectoral fins during locomotion in leopard sharks Triakis semifasciata.

The classical theory of locomotion in sharks proposes that shark pectoral fins are oriented to generate lift forces that balance the moment produced by the oscillating heterocercal tail. Accordingly, previous studies of shark locomotion have used fixed-wing aircraft as a model assuming that sharks have similar stability and control mechanisms. However, unlike airplanes, sharks are propelled by undulations of the body and tail and have considerable control of pectoral fin motion. In this paper, we use a new approach to examine the function of the pectoral fins of leopard sharks, Triakis semifasciata, during steady horizontal swimming at speeds of 0.5-2.0ls(-1), where l is total body length, and during vertical maneuvering (rising and sinking) in the water column. The planar orientation of the pectoral fin was measured using three-dimensional kinematics, while fluid flow in the wake of the pectoral fin and forces exerted on the water by the fin were quantified using digital particle image velocimetry (DPIV). Steady horizontal swimming in leopard sharks is characterized by continuous undulations of the body with a positive body tilt to the flow that decreases from a mean of 11 degrees to 0.6 degrees with increasing flow speeds from 0. 5 to 2.0ls(-1). Three-dimensional analysis showed that, during steady horizontal locomotion, the pectoral fins are cambered, concave downwards, at a negative angle of attack that we predict to generate no significant lift. Leopard shark pectoral fins are also oriented at a substantial negative dihedral angle that amplifies roll moments and hence promotes rapid changes in body position. Vortices shed from the trailing edge of the pectoral fin were detected only during vertical maneuvering. Starting vortices are produced when the posterior plane of the pectoral fin is actively flipped upwards or downwards to initiate rising or sinking, respectively, in the water column. The starting vortex produced by the pectoral fin induces a pitching moment that reorients the body relative to the flow. Body and pectoral fin surface angle are altered significantly when leopard sharks change vertical position in the water column. Thus, locomotion in leopard sharks is not analogous to flight in fixed-wing aircraft. Instead, a new force balance for swimming leopard sharks is proposed for steady swimming and maneuvering. Total force balance on the body is adjusted by altering the body angle during steady swimming as well as during vertical maneuvering, while the pectoral fins appear to be critical for initiating maneuvering behaviors, but not for lift production during steady horizontal locomotion.