Unusual kinematics and jaw morphology associated with piscivory in the poeciliid, Belonesox belizanus.

Piscivory in fishes is often associated with the evolution of highly elongate jaws that achieve a large mouth opening, or gape. Belonesox belizanus, the pike killifish, has independently evolved this morphology, which is derived from short-jawed poeciliids within the Cyprinodontiformes. Using kinematic analysis of high-speed video footage, we observed a novel aspect of the elongate jaws of Belonesox; the premaxilla rotates dorsally during mouth opening, while the lower jaw rotates ventrally. Anatomical study revealed that this unusual motion is facilitated by the architecture of the premaxillomandibular ligament, prominent within cyprinodontiforms. In Belonesox, it allows force to be transferred from the lower jaw directly to the premaxilla, thereby causing it to rotate dorsally. This dorsal rotation of the premaxilla appears to be assisted by a mediolateral twisting of the maxilla during jaw opening. Twisting maxillae are found in members of the group such as Fundulus, but are lost in Gambusia. Models revealed that elongate jaws partially account for the enlarged gape, but enhanced rotation at the quadrato-mandibular joint was equally important. The large gape is therefore created by: (i) the convergent evolution of elongate jaws; (ii) enhanced jaw rotation, facilitated by loss of a characteristic cyprinodontiform trait, the lip membrane; and (iii) premaxilla rotation in a novel direction, facilitated by the retention and co-option of additional cyprinodontiform traits, the premaxillomandibular ligament and a twisting maxilla.

The intramandibular joint in Girella: a mechanism for increased force production?

Intramandibular joints (IMJ) are novel articulations between bony elements of the lower jaw that have evolved independently in multiple fish lineages and are typically associated with biting herbivory. This novel joint is hypothesized to function by augmenting oral jaw expansion during mouth opening, which would increase contact between the tooth-bearing area of the jaws and algal substratum during feeding, resulting in more effective food removal from the substrate. Currently, it is not understood if increased flexibility in a double-jointed mandible also results in increased force generation during herbivorous biting and/or scraping. Therefore, we selected the herbivore Girella laevifrons for a mechanical study of the IMJ lower jaw lever system. For comparative purposes, we selected Graus nigra, a non-IMJ-bearing species, from a putative sister genus. Shortening of the lower jaw, during flexion at the IMJ, resulted in a more strongly force-amplifying closing lever system in the lower jaw, even in the absence of notable changes to the sizes of the muscles that power the lever system. To explain how the IMJ itself functions, we use a four-bar linkage that models the transmission of force and velocity to and through the lower jaw via the IMJ. When combined, the functionally interrelated lever and linkage models predict velocity to be amplified during jaw opening, whereas jaw closing is highly force modified by the presence of the IMJ. Moreover, the function of the IMJ late during jaw closure provides enough velocity to detach sturdy and resilient prey. Thus, this novel jaw system can alternate between amplifying the force or the velocity exerted onto the substrate where food items are attached. This unique mechanical configuration supports the argument that IMJs are functional innovations that have evolved to meet novel mechanical challenges and constraints placed on the feeding apparatus by attached and sturdy food sources.

Prey capture kinematics and four-bar linkages in the bay pipefish, Syngnathus leptorhynchus.

Because of their modified cranial morphology, syngnathid pipefishes have been described as extreme suction feeders. The presumption is that these fishes use their elongate snout much like a pipette in capturing planktonic prey. In this study, we quantify the contribution of suction to the feeding strike and quantitatively describe the prey capture mechanics of the bay pipefish Syngnathus leptorhynchus, focusing specifically on the role of both cranial elevation and snout movement. We used high-speed video to capture feeding sequences from nine individuals feeding on live brine shrimp. Sequences were digitized in order to calculate kinematic variables that could be used to describe prey capture. Prey capture was very rapid, from 2 to 6 ms from the onset of cranial rotation. We found that suction contributed at most about one-eighth as much as ram to the reduction of the distance between predator and prey. This movement of the predator was due almost exclusively to movement of the snout and neurocranium rather than movement of the whole body. The body was positioned ventral and posterior to the prey and the snout was rotated dorsally by as much as 21 degrees, thereby placing the mouth immediately behind the prey for capture. The snout did not follow the identical trajectory as the neurocranium, however, and reached a maximum angle of only about 10 degrees. The snout consists, in part, of elongate suspensorial elements and the linkages among these elements are retained despite changes in shape. Thus, when the neurocranium is rotated, the four-bar linkage that connects this action with hyoid depression simultaneously acts to expand and straighten the snout relative to the neurocranium. We confirm the presence of a four-bar linkage that facilitates these kinematics by couplings between the pectoral girdle, urohyal, hyoid complex, and the neurocranium-suspensorium complex.

Premaxillary movements in cyprinodontiform fishes: an unusual protrusion mechanism facilitates "picking" prey capture.

Premaxillary protrusion is hypothesized to confer a number of feeding advantages to teleost fishes; however, most proposed advantages relate to enhanced stealth or suction production during prey capture. Cyprinodontiformes exhibit an unusual form of premaxillary protrusion where the descending process of the premaxilla does not rotate anteriorly to occlude the sides of the open mouth during prey capture. Instead, the premaxilla is protruded such that it gives the impression of a beak during prey capture. We quantified premaxillary kinematics during feeding in four cyprinodontiform taxa and compared them with three percomorph taxa to identify any performance consequences of this protrusion mechanism. Individual prey capture events were recorded using digital high-speed video at 250-500 frames per second (n >or= 4 individuals, >or= 4 strikes per individual). Species differed in the timing of movement and the maximum displacement of the premaxilla during the gape cycle and in the contribution of the premaxilla to jaw closing. Cyprinodontiform taxa produced less premaxillary protrusion than the percomorph taxa, and were consistently slower in the time to maximum gape. Further, it appears cyprinodontiforms can alter the contribution of the premaxilla to mouth closure on an event-specific basis. We were able to demonstrate that, within at least one species, this variability is associated with the location of the prey (bottom vs. water column). Cyprinodontiform upper jaw movements likely reflect increased dexterity associated with a foraging ecology where prey items are "picked" from a variety of locations: the bottom, water column, or surface. We postulate that dexterity requires slow, precisely controlled jaw movements; thus, may be traded off for some aspects of suction-feeding performance, such as protrusion distance and speed.

Morphology of a picky eater: a novel mechanism underlies premaxillary protrusion and retraction within cyprinodontiforms.

Upper jaw protrusion is hypothesized to improve feeding performance in teleost fishes by enhancing suction production and stealth of the feeding event. However, many cyprinodontiform fishes (mid-water feeders, such as mosquitofish, killifish, swordtails, mollies and pupfish) use upper jaw protrusion for "picking" prey out of the water column or off the substrate; this feeding mode may require improved jaw dexterity, but does not necessarily require increased stealth and/or suction production. We describe functional aspects of the bones, muscles and ligaments of the anterior jaws in three cyprinodontiform genera: Fundulus (Fundulidae), Gambusia and Poecilia (Poeciliidae). All three genera possess a premaxillomandibular ligament that connects the premaxilla of the upper jaw to the mandible. The architecture of this ligament is markedly different from the upper-lower jaw connections previously described for basal atherinomorphs or other teleosts, and this loose ligamentous connection allows for more pronounced premaxillary protrusion in this group relative to closely related outgroup taxa. Within poeciliids, a novel insertion of the second division of the adductor mandibulae (A2) onto the premaxilla has also evolved, which allows this jaw adductor to actively retract the premaxilla during mouth closing. This movement is in contrast with most other teleosts, where the upper jaw is retracted passively via pressure applied by the adduction of the lower jaw. We postulate that this mechanism of premaxillary protrusion mediates the cyprinodontiforms' ability to selectively pick specific food items from the water column, surface or bottom, as a picking-based feeding mechanism requires controlled and coordinated "forceps-like" movements of the upper and lower jaws. This mechanism is further refined in some poeciliids, where direct muscular control of the premaxillae may facilitate picking and/or scraping material from the substrate.

Extremely fast prey capture in pipefish is powered by elastic recoil.

The exceptionally high speed at which syngnathid fishes are able to rotate their snout towards prey and capture it by suction is potentially caused by a catapult mechanism in which the energy previously stored in deformed elastic elements is suddenly released. According to this hypothesis, tension is built up in tendons of the post-cranial muscles before prey capture is initiated. Next, an abrupt elastic recoil generates high-speed dorsal rotation of the head and snout, rapidly bringing the mouth close to the prey, thus enabling the pipefish to be close enough to engulf the prey by suction. However, no experimental evidence exists for such a mechanism of mechanical power amplification during feeding in these fishes. To test this hypothesis, inverse dynamical modelling based upon kinematic data from high-speed videos of prey capture in bay pipefish Syngnathus leptorhynchus, as well as electromyography of the muscle responsible for head rotation (the epaxial muscle) was performed. The remarkably high instantaneous muscle-mass-specific power requirement calculated for the initial phase of head rotation (up to 5795 W kg(-1)), as well as the early onset times of epaxial muscle activity (often observed more than 300 ms before the first externally discernible prey capture motion), support the elastic power enhancement hypothesis.

Quantification of flow during suction feeding in bluegill sunfish.

Nearly all aquatic-feeding vertebrates use some amount of suction to capture prey items. Suction prey capture occurs by accelerating a volume of water into the mouth and taking a prey item along with it. Yet, until recently, we lacked the necessary techniques and analytical tools to quantify the flow regime generated by feeding fish. We used a new approach; Digital Particle Image Velocimetery (DPIV) to measure several attributes of the flow generated by feeding bluegill sunfish. We found that the temporal pattern of flow was notably compressed during prey capture. Flow velocity increased rapidly to its peak within 20 ms of the onset of the strike, and this peak corresponded to the time that the prey entered the mouth during capture. The rapid acceleration and deceleration of water suggests that timing is critical for the predator in positioning itself relative to the prey so that it can be drawn into the mouth along with the water. We also found that the volume of water affected by suction was spatially limited. Only rarely did we measure significant flow beyond 1.75 cm of the mouth aperture (in 20 cm fish), further emphasizing the importance of mechanisms, like locomotion, that place the fish mouth in close proximity to the prey. We found that the highest flows towards the mouth along the fish midline were generated not immediately in front of the open mouth, but approximately 0.5 cm anterior to the mouth opening. Away from the midline the peak in flow was closer to the mouth. We propose that this pattern indicates the presence of a bow wave created by the locomotor efforts of the fish. In this scheme, the bow wave acts antagonistically to the flow of water generated by suction, the net effect being to push the region of peak flow away from the open mouth. The peak was located farther from the mouth opening in strikes accompanied by faster locomotion, suggesting faster fish created larger bow waves.

Linking cranial kinematics, buccal pressure, and suction feeding performance in largemouth bass.

The rate and magnitude of buccal expansion are thought to determine the pattern of water flow and the change in buccal pressure during suction feeding. Feeding events that generate higher flow rates should induce stronger suction pressure and allow predators to draw prey from further away. We tested these expectations by measuring the effects of prey capture kinematics on suction pressure and the effects of the latter on the distance from which prey were drawn-termed suction distance. We simultaneously, but not synchronously, recorded 500-Hz video and buccal pressure from 199 sequences of four largemouth bass, Micropterus salmoides, feeding on goldfish. From the video, we quantified several kinematic variables associated with the head and jaws of the feeding bass that were hypothesized to affect pressure. In a multiple regression, kinematic data accounted for 79.7% of the variation among strikes in minimum pressure. Faster mouth opening and hyoid depression were correlated with lower pressures, a larger area under the pressure curve, and a faster rate of pressure reduction. In contrast, buccal pressure variables explained only 16.5% of the variation in suction distance, and no single pressure variable had a significant relationship with suction distance. Thus, although expected relationships between head kinematics and buccal pressure were confirmed, suction distance was only weakly related to buccal pressure. Three explanations are considered. First, bass may not attempt to maximize the distance from which prey are drawn. Second, the response of prey items to suction-induced flow depends on prey behavior and orientation and is, therefore, subject to considerable variation. Third, previous theoretical work indicates that water velocity decays exponentially with distance from the predator's mouth, indicating that variation among strikes in flow at the mouth opening is compressed away from the mouth. These findings are consistent with other recent data and suggest that suction distance is a poor metric of suction feeding performance.

Using functional morphology to examine the ecology and evolution of specialization.

Researchers strive to understand what makes species different, and what allows them to survive in the time and space that they do. Many models have been advanced which encompass an array of ecological, evolutionary, mathematical, and logical principles. The goal has been to develop ecological theories that can, among other things, make specific and robust predictions about how and where organisms should live and what organisms should utilize. The role of functional morphology is often an under-appreciated parameter of these models. A more complete understanding of how anatomical features work to allow the organism to accomplish certain tasks has allowed us to revisit some of these ideas with a new perspective. We illustrate our view of this role for functional morphology in ecology by considering the issue of specialization: we attempt to align several definitions of specialization based upon shared ecological and evolutionary principles, and we summarize theoretical predictions regarding why an organism might specialize. Kinematic studies of prey capture in several types of fishes are explored with regard to the potential ecological and evolutionary consequences of specialization, most notably in the area of trade-offs. We suggest that a functional morphological perspective can increase our understanding of the ecological concepts of specialization and it consequences. The kinds of data that functional morphologists collect can help us to quantify organismal performance associated with specialization and the union of functional morphology with ecology can help us to better understand not just how but why organisms interact in the manner that they do.