Mason N. Dean

The evolution of cranial design, diet, and feeding mechanisms in batoid fishes

The batoid fishes (electric rays, sawfishes, skates, guitarfishes, and stingrays) are a trophically and morphologically diverse clade in which the observed range of diets is a product of a feeding mechanism with few parts and therefore a limited number of functional interactions. This system allows an intriguing comparison to the complex network of associations in the feeding apparatus of bony fishes and an anatomically simple framework for investigations of the mechanisms underlying the evolution of functional and phenotypic diversity. We quantified morphology from reconstructed CT scans of 40 batoid species, representing more than half of the extant genera. We used pairwise comparisons to evaluate the extent of coevolution among components of the feeding apparatus and among morphologies and diets. These relationships were then used to predict diets in poorly studied taxa and in a reconstruction of the batoid ancestor. Although functionally there are fewer examples of convergence in the batoid feeding mechanism than in bony fishes, our data show multiple evolutions of similar dietary compositions underlain by a broad morphological diversity. Elements of the feeding apparatus evolved independently of one another, suggesting that decoupling components of the head skeleton created separate but interacting evolutionary modules that allowed trophic diversification. Our data imply that food habits exhibit strong independent and convergent evolution and that suites of morphologies are associated with certain diets; however, lack of behavioral data for this clade, and one example of divergent diets underlain by convergent morphology, caution against the assumption of simplistic relationships between form and function. We therefore urge future work to ground truth our study by testing the functional, dietary and evolutionary hypotheses suggested by our data.

Hard prey, soft jaws and the ontogeny of feeding mechanics in the spotted ratfish Hydrolagus colliei

The spotted ratfish Hydrolagus colliei is a holocephalan fish that consumes hard prey (durophagy) but lacks many morphological characters associated with durophagy in other cartilaginous fishes. We investigated its feeding biomechanics and biting performance to determine whether it can generate bite forces comparable with other durophagous elasmobranchs, how biting performance changes over ontogeny (21–44u200acm SL) and whether biomechanical modelling can accurately predict feeding performance in holocephalans. Hydrolagus colliei can generate absolute and mass-specific bite forces comparable with other durophagous elasmobranchs (anterior=104u200aN, posterior=191u200aN) and has the highest jaw leverage of any cartilaginous fish studied. Modelling indicated that cranial geometry stabilizes the jaw joint by equitably distributing forces throughout the feeding mechanism and that positive allometry of bite force is due to hyperallometric mechanical advantage. However, bite forces measured through tetanic stimulation of the adductor musculature increased isometrically. The jaw adductors of H. colliei fatigued more rapidly than those of the piscivorous spiny dogfish Squalus acanthias as well. The feeding mechanism of H. colliei is a volume-constrained system in which negative allometry of cranial dimensions leaves relatively less room for musculature. Jaw adductor force, however, is maintained through ontogenetic changes in muscle architecture.

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.

Ontogeny of the tessellated skeleton: insight from the skeletal growth of the round stingray Urobatis halleri

The majority of the skeleton of elasmobranch fishes (sharks, rays and relatives) is tessellated: uncalcified cartilage is overlain by a superficial rind of abutting, mineralized, hexagonal blocks called tesserae. We employed a diversity of imaging techniques on an ontogenetic series of jaw samples to investigate the development of the tessellated skeleton in a stingray (Urobatis halleri). We compared these data with the cellular changes that characterize cartilage calcification in bony skeletons. Skeletal growth is characterized by the appearance of tesserae as well as changes in chondrocyte shape, arrangement and density. Yolk sac embryos (35–56 mm disc width, DW) have untessellated lower jaw tissue wrapped in perichondrium and densely packed with chondrocytes. Chondrocyte density decreases dramatically after yolk sac absorption (histotroph stage: 57–80 mm DW) until the formation of tesserae, which are first visible using our techniques as thin (~60 µm), sub‐perichondral plaques. During the histotroph stage, flattened chondrocytes align parallel to the perichondrium at the tissue periphery, where we believe they are incorporated into developing tesserae to form the cell‐rich laminae observed within tesserae; in older animals peripheral cells in the uncalcified phase are rounder and less uniformly oriented. By parturition (~75 mm DW), cell density and the number of adjoining chondrocyte pairs (an indicator of cell division) have dropped to less than a third of their initial values; these remain low and tesserae continue to grow in size. The tessellated skeleton is a simple solution to the conundrum of growth in an endoskeleton with external mineralization and no remodeling. Although we see parallels with endochondral ossification (e.g. chondrocytes decreasing in density with age), the lack of chondrocyte hypertrophy and the fact that mineralization is sub‐perichondral (not the case in mammalian cartilage) suggest that the similarities end there.

Aerial and aquatic feeding in the silver arawana, Osteoglossum bicirrhosum

SynopsisThe silver arawana, Osteoglossum bicirrhosum, hunts along shorelines and within flooded forests in the Amazon River basin and supplements its limited consumption of aquatic vertebrates by leaping from the water to obtain terrestrial and arboreal prey. We offered O. bicirrhosum prey both suspended above and submerged below the surface of the water. From high-speed digital recordings, we measured kinematic variables associated with the jaws, cranium, pectoral fins, and body during orientation and prey capture. Aquatic and aerial feeding events were kinematically distinct, with aerial events generally involving faster, larger movements and a distinct delay in the onset of lower jaw depression until the head had left the water. The comparatively large gape during leaping may facilitate prey capture by overcoming variability in the apparent position of the prey due to refraction, while the delayed onset of mouth opening may serve to reduce the effects of drag. This distinctive leaping behaviour allows exploitation of the terrestrial prey base, especially during seasonal inundation of the Amazon River basin when the aquatic food base is widely dispersed.

Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis.

The dental anatomy of elasmobranch fishes (sharks, rays and relatives) creates a functional system that is more dynamic than that of mammalian dentition. Continuous dental replacement (where new teeth are moved rostrally to replace older ones) and indirect fibrous attachment of the dentition to the jaw allow teeth to reorient relative to the jaw over both long- and short-term scales, respectively. In this study, we examine the processing behavior and dental anatomy of the lesser electric ray Narcine brasiliensis (Olfers, 1831) to illustrate that the freedom of movement of elasmobranch dentition allows a functional flexibility that can be important for complex prey processing behaviors. From static manipulations of dissected jaws and observations of feeding events in live animals, we show that the teeth rotate during jaw protrusion, resulting in a secondary grasping mechanism that likely serves to hold prey while the buccal cavity is flushed free of sediment. The function of teeth is not always readily apparent from morphology; in addition to short-term reorientation, the long-term dental reorientation during replacement allows a given tooth to serve multiple functions during tooth ontogeny. Unlike teeth inside the mouth, the cusps of external teeth (on the portion of the tooth pad that extends past the occlusal plane) lay flat, such that the labial faces act as a functional battering surface, protecting the jaws during prey excavation.

Husbandry Notes on the Lesser Electric Ray

Abstract The lesser electric ray Narcine brasiliensis is a small member of the electric ray order Torpediniformes (Elasmobranchii: Batoidea). Although common circumglobally in the wild, this genus does not traditionally fare well in captivity. This study expands on methods previously published for captive maintenance of the lesser electric ray in large recirculating systems and outlines the husbandry of this species in displays equivalent to those in public aquaria. Once conditioned, rays will feed readily on polychaetes and shrimp; however, this species is prone to monogenean infestation and subsequent bacterial infections. As a result of parasitic infestation, these rays must be monitored carefully for anorexia. Common warning signs and administration of medication are outlined. Prophylactic treatment with the antihelminthic Praziquantel is required if the animals are to be maintained for any length of time in a closed recirculating system. To reduce ventral abrasion and facilitate capture of natural pr...

The skeleton | Cartilaginous Fish Skeletal Anatomy

Although the clades of cartilaginous fishes can be broadly considered to share a generalized skeletal body plan comprised of the same elements, their skeletons exhibit clade-specific arrangements and morphologies.