Micro- and macroevolutionary decoupling of cichlid jaws: a test of Liem's key innovation hypothesis

The extent to which elements of functional systems can change independently (modularity) likely influences the diversification of lineages. Major innovations in organismal design, like the pharyngeal jaw in cichlid fishes, may be key to a group's success when they relax constraints on diversification by increasing phenotypic modularity. In cichlid fishes, pharyngeal jaw modifications that enhanced the ability to breakdown prey may have freed their oral jaws from serving their ancestral dual role as a site of both prey capture and prey processing. This functional decoupling that allowed the oral jaws to become devoted solely to prey capture has been hypothesized to have permitted the two sets of cichlid jaws to evolve independently. We tested the hypothesis that oral and pharyngeal jaw mechanics are evolutionarily decoupled both within and among Neotropical Heroine cichlids. In the trophically polymorphic species Herichthys minckleyi, molariforms that exhibit enlarged molarlike pharyngeal jaw teeth were found to have approximately 400% greater lower jaw mass compared to H. minckleyi with the alternative papilliform pharyngeal morphology. However, oral jaw gape, lower jaw velocity ratios, anterior jaw linkage mechanics, and jaw protrusion did not differ between the morphotypes. In 40 other Heroine species, there was a weak correlation between oral jaw mechanics and pharyngeal jaw mass when phylogenetic history was ignored. Yet, after expansion of the cytochrome b phylogeny for Heroines, change in oral jaw mechanics was found to be independent of evolutionary change in pharyngeal jaw mass based on independent contrasts. Evolutionary decoupling of oral and pharyngeal jaw mechanics has likely played a critical role in the unparalleled trophic diversification of cichlid fishes.     

Terrestrial feeding in the Mudskipper Periophthalmus (Pisces: Teleostei): A cineradiographic analysis

Mudskipping gobies (Periophthalminae) are among the most terrestrial of amphibious fishes. Specializations associated with terrestrial prey capture and deglutition have been studied in Periophthalmus koelreuteri by light and X-ray cinematography which permits direct visualization of pharyngeal jaw movement during deglutition. Anatomical specializations of the pharyngeal jaws are described and include depressible teeth, a large ventral process on ceratobranchial five, and muscular modifications.
Multiple terrestrial feedings occur by Periophthalmus without a return to the water, and cineradiography reveals that the buccal cavity is often filled with air during terrestrial excursions in contrast to some previous hypotheses. Transport of the prey into the oesophagus occurs primarily by anteroposterior movement of the upper pharyngeal jaw. The lower pharyngeal jaw plays a limited role in food transport and may serve primarily to hold and position prey. The bite between upper and lower pharyngeal jaws occurs between the anterior teeth, and both jaws are protracted together during raking of food into the oesophagus. Functional specializations correlated with terrestrial feeding include obligatory use of pharyngeal jaws for swallowing even small prey items and positioning of the prey in the pharynx by pharyngeal jaw and hyoid movements alone.
This analysis of terrestrial feeding allows hypotheses of design constraints imposed by the aquatic medium on fishes to be raised and tested.     

Kinematics of the jaw and hyolingual apparatus during feeding in Caiman crocodilus

Movements of the neck, jaws, and hyolingual apparatus during inertial feeding in Caiman crocodilus were studied by cineradiography. Analysis reveals two kinds of cycles: inertial bites (reposition, kill/crush, and transport) and swallowing cycles. They differ in their gape profile and in displacement of the neck, cranium, and hyolingual apparatus. Inertial bites are initiated by an elevation of the neck and cranium; the head is then retracted backward, the prey simultaneously being lifted by the hyolingual apparatus. Next the lower jaw is depressed, and the prey is rapidly pushed further upward by the hyolingual apparatus. Thereafter fast mouth-closure occurs with the neck and cranium being abruptly depressed, the lower jaw elevated, and the hyolingual apparatus rapidly retracted ventrally. Depression of the neck and cranium thrusts the head forward and impacts the backward moving prey more posteriorly in the oral cavity. Swallowing cycles initially involve movement of the hyoid in front of the prey followed by rapid posteroventrad retraction of the hyoid, forcing the prey into the esophagus during opening and closing of the mouth. After mouth-closure, the hyoid apparatus is again protracted. Jaws, neck, tongue, and hyoid apparatus play an active role during intertial feeding sequences. At the beginning of a feeding sequence, the hyolingual apparatus mainly moves dorsoventrally, whereas toward the end of a sequence anteroposterior displacements of the hyoid are prominent. © 1992 Wiley-Liss, Inc.     

Decoupled jaws promote trophic diversity in cichlid fishes

Functional decoupling of oral and pharyngeal jaws is widely considered to have expanded the ecological repertoire of cichlid fishes. But, the degree to which the evolution of these jaw systems is decoupled and whether decoupling has impacted trophic diversification remains unknown. Focusing on the large Neotropical radiation of cichlids, we ask whether oral and pharyngeal jaw evolution is correlated and how their evolutionary rates respond to feeding ecology. In support of decoupling, we find relaxed evolutionary integration between the two jaw systems, resulting in novel trait combinations that potentially facilitate feeding mode diversification. These outcomes are made possible by escaping the mechanical trade-off between force transmission and mobility, which characterizes a single jaw system that functions in isolation. In spite of the structural independence of the two jaw systems, results using a Bayesian, state-dependent, relaxed-clock model of multivariate Brownian motion indicate strongly aligned evolutionary responses to feeding ecology. So, although decoupling of prey capture and processing functions released constraints on jaw evolution and promoted trophic diversity in cichlids, the natural diversity of consumed prey has also induced a moderate degree of evolutionary integration between the jaw systems, reminiscent of the original mechanical trade-off between force and mobility.     

Patterns of Evolution in the Feeding Mechanism of Actinopterygian Fishes

SYNOPSIS. Structural and functional patterns in the evolutionof the actinopterygian feeding mechanism are discussed in thecontext of the major monophyletic lineages of ray-finned fishes.A tripartite adductor mandibulae contained in a maxillary-palatoquadratechamber and a single mechanism of mandibular depression mediatedby the obliquus inferioris, sternohyoideus, and hyoid apparatusare primitive features of the Actinopterygii. Halecostome fishesare characterized by having an additional mechanism of mandibulardepression, the levator operculi—opercular series coupling,and a maxilla which swings anteriorly during prey capture. Theseinnovations provide the basis for feeding by inertial suctionwhich is the dominant mode of prey capture throughout the halecostomeradiation. A remarkably consistent kinematic profile occursin all suction-feeding halecostomes. Teleost fishes possessa number of specializations in the front jaws including a geniohyoideusmuscle, loss of the primitive suborbital adductor component,and a mobile premaxilla. Structural innovations in teleost pharyngealjaws include fusion of the dermal tooth plates with endoskeletalgill arch elements, the occurrence of a pharyngeal retractormuscle, and a shift in the origin of the pharyngohyoideus. Thesespecializations relate to increased functional versatility ofthe pharyngeal jaw apparatus as demonstrated by an electromyographicstudy of pharyngeal muscle activity in Esox and Ambloplites.The major feature of the evolution of the actinopterygian feedingmechanism is the increase in structural complexity in both thepharyngeal and front jaws. Structural diversification is a functionof the number of independent biomechanical pathways governingmovement.     

Shape analysis of the jaws between two minnow species over ontogeny

This study compares sand shiner (Notropis stramineus ) and silverjaw (Ericymba buccata ) minnows, in terms of the morphological shape changes of the upper, lower, and pharyngeal jaws over ontogeny. These two species of minnows initially feed on midge larvae and undergo an ontogenic prey shift. The traditional morphometrics measured—total length, snout‐to‐vent length, eye diameter, premaxilla length, lower jaw length, gape—were regressed onto total length to test for allometry. Digital pictures were processed with tpsDig and further analyzed with MorphoJ utilizing a regular geometric morphometrics procedure using principle component analyses. We examined gut contents for 16 fish of each species. For the silverjaw minnows, we found all jaw variables to exhibit positive allometric growth with increasing total length, while most of the jaw variables for the sand shiner exhibited negative allometric growth with increasing total length. This correlates with an ontogenic prey shift for both species. Sand shiner minnows have been found to be more omnivorous, feeding on algae later in life, while silverjaw minnows undergo a prey shift to larger invertebrates. These species lack oral dentition causing an increased reliance on the pharyngeal apparatus. Principle component analyses revealed elongation of pharyngeal jaw elements in the silverjaw minnows and a relative shortening and bulking of pharyngeal jaws in the sand shiner minnows. The ontogenic dietary shifts observed in these two species provide possible explanation for the morphological changes over ontogeny in jaw elements, which are likely enabling these species to occupy the same habitat with little niche overlap.     

Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae

The Labridae is one of the most structurally and functionally diversified fish families on coral and rocky reefs around the world, providing a compelling system for examination of evolutionary patterns of functional change. Labrid fishes have evolved a diverse array of skull forms for feeding on prey ranging from molluscs, crustaceans, plankton, detritus, algae, coral and other fishes. The species richness and diversity of feeding ecology in the Labridae make this group a marine analogue to the cichlid fishes. Despite the importance of labrids to coastal reef ecology, we lack evolutionary analysis of feeding biomechanics among labrids. Here, we combine a molecular phylogeny of the Labridae with the biomechanics of skull function to reveal a broad pattern of repeated convergence in labrid feeding systems. Mechanically fast jaw systems have evolved independently at least 14 times from ancestors with forceful jaws. A repeated phylogenetic pattern of functional divergence in local regions of the labrid tree produces an emergent family-wide pattern of global convergence in jaw function. Divergence of close relatives, convergence among higher clades and several unusual 'breakthroughs' in skull function characterize the evolution of functional complexity in one of the most diverse groups of reef fishes.     

Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei,Perciformes)

Summary The feeding mechanisms of four species of the teleostean family Labridae (Cheilinus fasciatus, C. trilobatus, Oxycheilinus bimaculatus, and O. unifasciatus) were modeled using four-bar linkage theory from mechanical engineering. The predictions of four-bar linkage models regarding the kinematics of feeding were compared to the movements observed with high speed cinematography (200 frames/s). A four-bar linkage was an accurate model of the mechanism by which upper jaw protrusion, maxillary rotation, and gape increase occur in each species. A four-bar mechanism of hyoid depression was an accurate predictor of hyoid depression when simultaneous cranial elevation and sternohyoideus contraction were simulated. Morphometrics of the linkage systems of the jaws and hyoid were collected for 12 labrid species. These data were used to calculate the transmission of force and motion through the musculoskeletal linkages. Several measures of mechanical advantage and displacement advantage were compared, including both traditional lever ratios and transmission coefficients of four-bar linkages. Alternative designs of the feeding mechanisms maximize force or velocity for the capture of different prey types. High velocity transmission of both the jaw and hyoid systems is characteristic of those species that feed on evasive prey, whereas species that feed on benthic invertebrates favor increased force transmission in both systems. Quantitative models of biomechanical systems supply criteria for functionally relevant morphometrics, and aid in calculating the capacity for transmission of force and velocity in musculoskeletal systems.     

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. J. Morphol. 2010. © 2009 Wiley‐Liss, Inc.     

Morphology and function of the feeding apparatus of Pelusios castaneus (Chelonia; Pleurodira)

Feeding mechanics of vertebrates depend on physical constraints of the surrounding media, water or air. Such functions are inseparably combined with form. The aim of this study is to show this linkage for the pleurodiran freshwater turtle Pelusios castaneus and, additionally, to point out the major functional and biomechanical distinctions between aquatic and terrestrial feeding turtles as well as several intermediate forms. Gross morphological investigations of skull, hyoid, tongue, and connected musculature, as well as scanning electron microscopy of the tongue surface, show typical features of an aquatic feeder, e.g., strongly developed hyoid apparatus vs. a small tongue with only moderate papillae, and massive jaw and hyoid musculature. Additionally, the special function of the esophagus during feeding is investigated to elucidate the problems of a bidirectional feeder. The esophagus is highly distensible in order to store the excess water sucked in during feeding until the prey is fixed by the jaws. The distension is probably achieved by a coincidence of active (branchial horn) as well as passive (water) components. P. castaneus is a feeding generalist, and is well adapted to the aquatic medium in terms of its functional as well as morphological features.     

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.     

Feeding ecology underlies the evolution of cichlid jaw mobility

The fish feeding apparatus is among the most diverse functional systems in vertebrates. While morphological and mechanical variations of feeding systems are well studied, we know far less about the diversity of the motions that they produce. We explored patterns of feeding movements in African cichlids from Lakes Malawi and Tanganyika, asking whether the degree of kinesis is associated with dietary habits of species. We used geometric morphometrics to measure feeding kinesis as trajectories of shape change, based on 326 high‐speed videos in 56 species. Cranial morphology was significantly related to feeding movements, both of which were distributed along a dietary axis associated with prey evasiveness. Small‐mouthed cichlids that feed by scraping algae and detritus from rocks had low kinesis strikes, while large‐mouthed species that eat large, evasive prey (fishes and shrimps) generated the greatest kinesis. Despite having higher overall kinesis, comparisons of trajectory shape (linearity) revealed that cichlids that eat mobile prey also displayed more kinematically conserved, or efficient, feeding motions. Our work indicates that prey evasiveness is strongly related to the evolution of cichlid jaw mobility, suggesting that this same relationship may explain the origins and diversity of highly kinetic jaws that characterize the super‐radiation of spiny‐rayed fishes.     

Functional analysis of a specialized prey processing behavior: winnowing by surfperches (Teleostei: Embiotocidae).

Several surfperches (Embiotocidae), including the black surfperch, Embiotoca jacksoni, exhibit a specialized prey handling behavior known as winnowing, in which ingested food and non-nutritive debris are separated within the oropharyngeal cavity. Prey items are swallowed, and unpalatable material is ejected from the mouth. Winnowing is believed to play an important role in the partitioning of food resources among sympatric embiotocids. We present a mechanistic model for this separative prey processing based on high-speed video analysis, cineradiography, electromyography, and buccal and opercular cavity pressure transducer recording. Winnowing by embiotocids is characterized by premaxillary protrusions repeated cyclically with reduced oral gape. Protrusion is accompanied by depression of the hyoid apparatus and adduction of the opercula. Alternating expansion and contraction of the buccal and opercular cavities generate regular pressure waveforms that indicate bidirectional water flow during processing. Separation of food from debris by Embiotoca jacksoni occurs in three phases. The prey-debris bolus is transported anteriorly and posteriorly within the oropharyngeal cavity and is then sheared by the pharyngeal jaws. Mechanical processing is complemented by the rinsing action of water currents during hydraulic prey transport. The feeding apparatus of Embiotoca jacksoni is functionally versatile, although not obviously specialized relative to that of nonwinnowing surfperches. Protrusion of the premaxillae and depression of the hyoid apparatus are critical to both prey capture and subsequent prey processing. The pharyngeal jaws exhibit kinematic patterns during separation of food from debris distinct from those observed during mastication of uncontaminated prey. This behavioral flexibility facilitates resource partitioning and the coexistence of E. jacksoni in sympatric embiotocid assemblages.     

Functional morphology of the pharyngeal jaw apparatus in perciform fishes: An experimental analysis of the haemulidae

A new mechanical model for function of the pharyngeal jaw apparatus in generalized perciform fishes is developed from work with the family Haemulidae. The model is based on anatomical observations, patterns of muscle activity during feeding (electromyography), and the actions of directly stimulated muscles. The primary working stroke of the pharyngeal apparatus involves simultaneous upper jaw depression and retraction against a stabilized and elevating lower jaw. The working stroke is characterized by overlapping activity in most branchial muscles and is resolved into three phases. Four muscles (obliquus dorsalis 3, levator posterior, levator externus 3/4, and obliquus posterior) that act to depress the upper jaws become active in the first phase. Next, the retractor dorsalis, the only upper jaw retracting muscle, becomes active. Finally, there is activity in several muscles (transversus ventrales, pharyngocleithralis externus, pharyngohyoideus, and protractor pectoralis) that attach to the lower jaws. The combined effect of these muscles is to elevate and stabilize the lower jaws against the depressing and retracting upper jaws. The model identifies a novel mechanism of upper jaw depression, here proposed to be the primary component of the perciform pharyngeal jaw bite. The key to this mechanism is the joint between the epibranchial and toothed pharyngobranchial of arches 3 and 4. Dorsal rotation of epibranchials 3 and 4 about the insertion of the obliquus posterior depresses the lateral border of pharyngobranchials 3 and 4 (upper jaw). The obliquus dorsalis 3 muscle crosses the epibranchial-pharyngo-branchial joint in arches 3 and 4, and several additional muscles effect epibranchial rotation. Five upper jaw muscles cause upper jaw depression upon electrical stimulation: the obliquus dorsalis 3, levator posterior, levator externus 3/4, obliquus posterior, and transversus dorsalis. This result directly contradicts previous interpretations of function for the first three muscles. The presence of strong depression of the upper pharyngeal jaws explains the ability of many generalized perciform fishes to crush hard prey in their pharyngeal apparatus.     

Morphological convergence of pharyngeal jaw structure in durophagous perciform fish

This study investigated the ecomorphology of pharyngeal jaw structure and durophagy in three families of marine teleosts: the Sciaenidae, Haemulidae and Carangidae. Regressions of the bone and muscle mass of pharyngeal jaws were generated to elucidate the differences associated with eating hard-bodied and soft-bodied prey; within-family comparisons revealed significant differences in masses of bones and muscles involved with processing the former. Generally, the durophagous species − Trachinotus carolinus (Carangidae), Pogonias cromis (Sciaenidae) and Anisotremus surinamensis (Haemulidae) − had heavier and stronger pharyngeal toothplates and larger protractor pectoralis muscles, with masses of these musculoskeletal elements ranging from five times to nearly an order of magnitude larger than those of their soft-prey feeding relatives. Pogonias cromis and T. carolinus demonstrate convergence in the ontogeny and morphological modification of the pharyngeal toothplates and protractor pectoralis muscles that enhance crushing ability. In the Haemulidae, moderate size increases in a few pharyngeal jaw elements (and larger overall body size in A. surinamensis ) are sufficient for durophagy. Morphospace analysis of six species from the three families illustrates the strong functional association between the biomechanical properties of prey and the relative sizes of biting and transport mechanisms.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80 , 147−165.     

Functional morphology of durophagy in black carp,Mylopharyngodon piceus

The black carp, Mylopharyngodon piceus (Osteichthyes: Cyprinidae), crushes its snail and other molluscan prey with robust pharyngeal jaws and strong bite forces. Using gross morphology, histological sectioning, and X‐ray reconstruction of moving morphology (XROMM), we investigated structural, behavioral, and mechanical aspects of pharyngeal jaw function in black carp. Strut‐like trabeculae in their pharyngeal jaws support large, molariform teeth. The teeth occlude with a hypertrophied basioccipital process that is also reinforced with stout trabeculae. A keratinous chewing pad is firmly connected to the basioccipital process by a series of small bony projections from the base of the pedestal. The pharyngeal jaws have no bony articulations with the skull, and their position is controlled by five paired muscles and one unpaired median muscle. Black carp can crush large molluscs, so we used XROMM to compare pharyngeal jaw postures as fish crushed ceramic tubes of increasing sizes. We found that black carp increase pharyngeal jaw gape primarily by ventral translation of the jaws, with ventral rotation and lateral flaring of the jaws also increasing the space available to accommodate large prey items. A stout, robust ligament connects left and right jaws together firmly, but allows some rotation of the jaws relative to each other. Contrasting with the pharyngeal jaw mechanism of durophagous perciforms with fused left and right lower pharyngeal jaws, we hypothesize that this ligamentous connection may serve to decouple tensile and compressive forces, with the tensile forces borne by the ligament and the compressive forces transferred to the prey. J. Morphol. 276:1422–1432, 2015. © 2015 Wiley Periodicals, Inc.     

Exploring feeding behaviour in deep‐sea dragonfishes (Teleostei: Stomiidae): jaw biomechanics and functional significance of a loosejaw

Deep‐sea dragonfishes (family Stomiidae) possess spectacular morphologies adapted to capturing large prey items in a seascape largely devoid of biomass, including large fang‐like teeth set on extremely long jaws. Perhaps the most intriguing aspect of dragonfish morphology is a lack of a floor to the oral cavity (i.e. there is no skin between the mandibular rami) in species of three dragonfish genera. The present study aimed to investigate the kinematic properties and performance of lower‐jaw adduction in stomiid fishes and to infer what functional advantages or constraints the ‘loosejaw’ confers. A computation model based on dynamic equilibrium predicted very fast jaw adduction for all species at gapes ranging from 90–120° in 66.6–103 ms. Simulations demonstrated that forces resisting lower‐jaw adduction in dragonfishes, and long‐jawed fishes in general, are substantially greater than those in fishes with shorter jaws. These forces constrain inlever length, resulting in relatively high mechanical advantages to attain fast adduction velocities. By reducing the surface area of the lower‐jaw system, loosejaws drastically reduce resistive forces. This has permitted loosejaw dragonfishes to evolve lower mechanical advantages that produce high displacement velocities with an extremely long jaw, a distinct asset in capturing large and scarce resources in the deep‐sea. In addition, loosejaws require a substantially reduced adductor mass to close long jaws at high velocities. These results reveal that the loosejaw condition is an adaptation that expands the morphological boundaries imposed by the dynamic limitations of a long jaw. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 224–240.     

Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea)

Protrusion of the jaws during feeding is common in Batoidea (rays, skates, sawfishes, and guitarfishes), members of which possess a highly modified jaw suspension. The lesser electric ray, Narcine brasiliensis, preys primarily on polychaete annelids using a peculiar and highly derived mechanism for jaw protraction. The ray captures its prey by protruding its jaws beneath the substrate and generating subambient buccal pressure to suck worms into its mouth. Initiation of this protrusion is similar to that proposed for other batoids, in that the swing of the distal ends of the hyomandibulae is transmitted to Meckel's cartilage. A "scissor-jack" model of jaw protrusion is proposed for Narcine, in which the coupling of the upper and lower jaws, and extremely flexible symphyses, allow medial compression of the entire jaw complex. This results in a shortening of the distance between the right and left sides of the jaw arch and ventral extension of the jaws. Motion of the skeletal elements involved in this extreme jaw protrusion is convergent with that described for the wobbegong shark, Orectolobus maculatus. Narcine also exhibits asymmetrical protrusion of the jaws from the midline during processing, accomplished by unequal depression of the hyomandibulae. Lower jaw versatility is a functional motif in the batoid feeding mechanism. The pronounced jaw kinesis of N. brasiliensis is partly a function of common batoid characteristics: euhyostylic jaw suspension (decoupling the jaws from the hyoid arch) and complex and subdivided cranial musculature, affording fine motor control. However, this mechanism would not be possible without the loss of the basihyal in narcinid electric rays. The highly protrusible jaw of N. brasiliensis is a versatile and maneuverable feeding apparatus well-suited for the animal's benthic feeding lifestyle.     

Ecomorphological relationships among Caribbean tetraodontiform fishes

The anatomy of the oral jaw apparatus, lever-arm mechanics and the diet of six species of Caribbean fishes in the order Tetraodontiformes were investigated to explore the relationships between trophic morphology and feeding habit in these fishes. Tetraodontiforms use their oral jaw apparatus to capture and reduce a broad range of prey types such as plankton, polychaete worms, holothuroids, sea urchins, crabs, molluscs, gorgonians and algae. The different feeding habits of tetraodontiforms are reflected by differences in the morphological and biomechanical features of their oral jaw apparatus that appear to enhance their abilities to feed on hard prey organisms. Species that bite and crush hard, benthic prey organisms had more massive bones and muscles, longer jaw-opening in-levers, and higher jaw-closing lever ratios than the planktivorous, suction-feeding species. Masses of the jaw and suspensorium bones and lower jaw adductor muscles as well as the jaw-opening in-levers and jaw-closing lever ratios of crushers were greater than those of biters. In contrast, the mass of the adductor muscle of the upper jaw did not vary among species with different diets, indicating that this muscle may not be central to the factors that determine patterns of prey use in these fishes. The diversity of feeding behaviours and the wide range of feeding habits among fishes in the order Tetraodontiformes illustrate the versatility of the oral jaw apparatus as a single functional feeding system in fishes.     

Functional design and evolution of the pharyngeal jaw apparatus in euteleostean fishes

Functional and structural patterns in the pharyngeal jaw apparatus of euteleostean fishes are described and analysed as a case study of the transformation of a complex biological design. The sequential acquisition of structural novelties in the pharyngeal apparatus is considered in relation to both current hypotheses of euteleostean phylogeny and patterns of pharyngeal jaw function. Several euteleostean clades are corroborated as being monophyletic, and morphologically conservative features of the pharyngeal jaw apparatus are recognized. Functional analysis, using cinematography and electromyography, reveals four distinct patterns of muscle activity during feeding in primitive euteleosts (Esox) and in derived euteleostean fishes(Perca, Micropterus, Ambloplites, Pomoxis). The initial strike, buccal manipulation, pharyngeal manipulation, and the pharyngeal transport of prey into the oesophagus all involve unique muscle activity patterns that must be distinguished in analyses of pharyngeal jaw function. During pharyngeal transport, the upper and lower pharyngeal jaws are simultaneously protracted and retracted by the action of dorsal and ventral musculoskeletal gill arch couplings. The levator externus four and retractor dorsalis muscles, anatomical antagonists, overlap for 70–90°of their activity period. Levatores externi one and two are the main protractors of the upper pharyngeal jaws in the acanthopterygian fishes studied. The major features of pharyngeal jaw movement in primitive euteleosts are retained in many derived clades in spite of a dramatic structural reorganization of the pharyngeal region. Homologous muscles have radically changed their relative activity periods while pharyngeal jaw kinematics have been modified relatively little. Patterns of transformation of activity may thus bear little direct relationship to the sequence of structural modification in the evolution of complex designs. Overall function of a structural system may be maintained, however, through co-ordinated modifications of the timing of muscle activity and anatomical reorientation of the musculoskeletal system. Deeper understanding of the principles underlying the origin and transformation of functional design in vertebrates awaits further information on the acquisition of both structural and functional novelties at successive hierarchical levels within monophyietic clades. This is suggested as a key goal of future research in functional and evolutionary morphology.