Adam P. Summers

Stiffening the stingray skeleton - an investigation of durophagy in myliobatid stingrays (Chondrichthyes, batoidea, myliobatidae).

ABSTRACT

Kinematic analysis of suction feeding in the nurse shark, Ginglymostoma cirratum (Orectolobiformes, Ginglymostomatidae)

Abstract Inertial suction feeding is known to occur in some sharks, but the sequence and temporal kinematics of head and jaw movements have not been defined. We investigated the feeding kinematics of a suction feeding shark, the nurse shark Ginglymostoma cirratum, to test for differences in the timing and magnitude of feeding components with other shark taxa when sharks were fed pieces of bony fish. Thirteen kinematic variables were measured from high-speed video recordings. Food capture in this species consists of expansive, compressive, and recovery phases, as in most other sharks, but there is little or no cranial elevation. Mean time to maximum gape (32 msec) is the fastest recorded for an elasmobranch fish. Other relatively rapid events include mandibular depression (26 msec), elevation (66 msec), and total bite time (100 msec). Buccal valves assist the unidirectional flow of water into the mouth and out of the gill chambers. Food capture under these experimental conditions appears to be a stereotyped modal action pattern but with significant interindividual variability in timing of kinematic events. Ginglymostoma cirratum exhibits a suite of specializations for inertial suction feeding that include (1) the formation of a small, anteriorly directed mouth that is approximately round and laterally enclosed by modified labial cartilages; (2) small teeth; (3) buccal valves to prevent the backflow of water; and (4) extremely rapid buccal expansion. Sharks that capture food by inertial suction have faster and more stereotyped capture behavior than sharks that primarily ram feed. Inertial suction feeding, which has evolved multiple times in sharks, represents an example of functional convergence with inertial suction feeding bony fishes.

Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles.

Studies of aquatic prey capture in vertebrates have demonstrated remarkable convergence in kinematics between diverse vertebrate taxa. When feeding in water, most vertebrates employ large-amplitude hyoid depression to expand the oral cavity and suck in water along with the prey. In contrast, vertebrates feeding on land exhibit little or no hyoid depression. In this study we compared the kinematics of terrestrial and aquatic prey capture within one species of turtle, Terrapene carolina, in order to determine whether an individual species can modulate the magnitude of hyoid depression between air and water. High-speed video (250 frames per second) showed that hyoid depression was over three times greater in aquatic than in terrestrial feedings, indicating that T. carolina is able to modulate hyoid depression magnitude depending on the medium in which feeding occurs. In addition, we observed medium-dependent modulation of hyoid depression in another turtle, Heosemys grandis, and large-amplitude hyoid depression during aquatic feeding in Kinosternon leucostomum, Platysternon megacephalum, and juvenile Chelydra serpentina. In all of these turtles, hyoid depression produced oral cavity expansion during aquatic feeding, but the earthworm prey were never sucked toward the predators. Prey were captured by neck extension (ram feeding), and we conclude that the function of hyoid depression during aquatic feeding in cryptodire turtles is to prevent the forward motion of the predator from pushing the prey away (compensatory suction). Aquatic feeding is probably the primitive condition for all extant turtles, and thus terrestrial feeding in T. carolina and other turtles is a secondarily derived characteristic. We conclude from this historical pattern that it is not appropriate to use extant turtles in attempts to reconstruct the terrestrial feeding mechanisms of primitive amniotes.

SPIDER DRAGLINE SILK: CORRELATED AND MOSAIC EVOLUTION IN HIGH-PERFORMANCE BIOLOGICAL MATERIALS

Abstract The evolution of biological materials is a critical, yet poorly understood, component in the generation of biodiversity. For example, the diversification of spiders is correlated with evolutionary changes in the way they use silk, and the material properties of these fibers, such as strength, toughness, extensibility, and stiffness, have profound effects on ecological function. Here, we examine the evolution of the material properties of dragline silk across a phylogenetically diverse sample of species in the Araneomorphae (true spiders). The silks we studied are generally stronger than other biological materials and tougher than most biological or man-made fibers, but their material properties are highly variable; for example, strength and toughness vary more than fourfold among the 21 species we investigated. Furthermore, associations between different properties are complex. Some traits, such as strength and extensibility, seem to evolve independently and show no evidence of correlation or trade-off across species, even though trade-offs between these properties are observed within species. Material properties retain different levels of phylogenetic signal, suggesting that traits such as extensibility and toughness may be subject to different types or intensities of selection in several spider lineages. The picture that emerges is complex, with a mosaic pattern of trait evolution producing a diverse set of materials across spider species. These results show that the properties of biological materials are the target of selection, and that these changes can produce evolutionarily and ecologically important diversity.

Linkage mechanics and power amplification of the mantis shrimp's strike

SUMMARY Mantis shrimp (Stomatopoda) generate extremely rapid and forceful predatory strikes through a suite of structural modifications of their raptorial appendages. Here we examine the key morphological and kinematic components of the raptorial strike that amplify the power output of the underlying muscle contractions. Morphological analyses of joint mechanics are integrated with CT scans of mineralization patterns and kinematic analyses toward the goal of understanding the mechanical basis of linkage dynamics and strike performance. We test whether a four-bar linkage mechanism amplifies rotation in this system and find that the rotational amplification is approximately two times the input rotation, thereby amplifying the velocity and acceleration of the strike. The four-bar model is generally supported, although the observed kinematic transmission is lower than predicted by the four-bar model. The results of the morphological, kinematic and mechanical analyses suggest a multi-faceted mechanical system that integrates latches, linkages and lever arms and is powered by multiple sites of cuticular energy storage. Through reorganization of joint architecture and asymmetric distribution of mineralized cuticle, the mantis shrimps raptorial appendage offers a remarkable example of how structural and mechanical modifications can yield power amplification sufficient to produce speeds and forces at the outer known limits of biological systems.

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.

Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondrichthyes)

SUMMARY Elasmobranchs, particularly sharks, function at speed and size extremes, exerting large forces on their cartilaginous skeletons while swimming. This casts doubt on the generalization that cartilaginous skeletons are mechanically inferior to bony skeletons, a proposition that has never been experimentally verified. We tested mineralized vertebral centra from seven species of elasmobranch fishes: six sharks and one axially undulating electric ray. Species were chosen to represent a variety of morphologies, inferred swimming speeds and ecological niches. We found vertebral cartilage to be as stiff and strong as mammalian trabecular bone. Inferred swimming speed was a good, but not infallible, predictor of stiffness and strength. Collagen content was also a good predictor of material stiffness and strength, although proteoglycan was not. The mineral fraction in vertebral cartilage was similar to that in mammalian trabecular bone and was a significant predictor of material properties.

The evolution of tendon — morphology and material properties

Phylogenetically, tendinous tissue first appears in the invertebrate chordate Branchiostoma as myosepta. This two-dimensional array of collagen fibers is highly organized, with fibers running along two primary axes. In hagfish the first linear tendons appear and the myosepta have developed specialized regions with unidirectional fiber orientation-a linear tendon within the flat sheet of myoseptum. Tendons react to compressive load by first forming a fibrocartilaginous pad, and under severe stress, sesamoid bones. Evidence for this ability to react to load first arises in the cartilaginous fish, here documented in a tendon from the jaw of a hard-prey crushing stingray. Sesamoid bones are common in bony fish and also in tetrapods. Tendons will also calcify under tensile loads in some groups of birds, and this reaction to load is seen in no other vertebrates. We conclude that the evolutionary history of tendon gives us insight into the use of model systems for investigating tendon biology. Using mammal and fish models may be more appropriate than avian models because of the apparent evolution of a novel reaction to tensile loads in birds.

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 (21–44 cm 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=104 N, posterior=191 N) 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.

The material properties of acellular bone in a teleost fish.

SUMMARY Several lineages of teleost fishes have independently derived skeletons composed solely of acellular bone, a tissue without obvious advantages over bone that has osteocytes in the matrix. There is no consensus for the functional role of acellular bone, as factors such as salinity, activity level and gross morphology have been shown to be poor predictors of acellularity. We used a three-point bending method to test the hypothesis that the material stiffness (elastic modulus) of acellular bone is higher than that of cellular bone, which could be evidence that material properties were a selective pressure in the evolution of this unusual skeletal material. The acellular ribs of Myoxocephalus polyacanthocephalus are curved, hollow beams that decrease in size both distally and posteriorly along the rib series. First and second moments of area decreased distally and caudally in all individuals. Youngs modulus (E) ranged from 3.67 to 8.40 GPa, with a mean of 6.48 GPa. The flexural stiffness (EI) differed significantly between ribs, and the hollow cylinder morphology increased the flexural stiffness by 12.0% over a solid, circular cross-section rod with the same area. Contrary to our expectations, acellular bone is not stiffer by virtue of fewer lacunae but instead falls at the very low end of the range of stiffness seen in cellular bone. There remains the possibility that other properties (e.g. fatigue resistance, toughness) are higher in acellular bone.