Tough and Stretchy: Mechanical Properties of the Alimentary Tract in a Fish Without a Stomach.

The mechanical properties of intestinal tissues determine how a thin-walled structure exerts forces on food and absorbs the force of food as it enters and travels down the gut. These properties are critically important in durophagous and stomachless fish, which must resist the potential damage to foreign bodies (e.g., shells fragments) in their diet. We test the hypothesis that the mechanical properties of the alimentary tract will differ along its length. We predict that the proximal region of the gut should be the strongest and most extensible to handle the large influx of prey often associated with stomachless fish that lack a storage depot. We developed a custom inflation technique to measure the passive mechanical properties of the whole intestine of the stomachless shiner perch, Cymatogaster aggregata. We show that mechanical properties differ significantly along the length of the alimentary tract when inflated to structural failure, with 25-46% greater maximal stress, strain, extension ratio, and toughness at the proximal (25%) position. We also find that the alimentary tissues (excluding the heavily muscular rectum) are generally highly extensible and anisotropic, and do not differ in wall circumference or thickness along the alimentary tract. These findings contribute to our knowledge of the mechanical properties of fish intestinal tissues and guide future studies of factors influencing the evolution of fish alimentary systems.

Les propriétés mécaniques des tissus intestinaux déterminent la manière dont une structure à paroi mince exerce des forces sur les aliments et absorbe leur force lorsque ceux-ci pénètrent et descendent dans l'intestin. Ces propriétés sont d'une importance capitale chez les poissons durophages et ceux sans estomac qui doivent résister aux possibles dommages que peuvent provoquer l'ingestion de corps étrangers (comme des fragments de coquilles) lorsqu'ils s'alimentent. Nous testons l'hypothèse selon laquelle les propriétés mécaniques du tube digestif diffèrent sur sa longueur. Nous prédisons que la région proximale de l'intestin devrait être la plus solide et la plus extensible pour gérer le grand afflux de proies souvent associé aux poissons sans estomac qui n'ont pas de capacité de stockage. Nous avons élaboré une technique de gonflage propre pour mesurer les propriétés mécaniques passives de l'ensemble de l'intestin de la perche méné dépourvue d'estomac, Cymatogaster aggregata. Nous montrons que les propriétés mécaniques diffèrent significativement le long du tube digestif lorsqu'il est gonflé jusqu'à une défaillance structurelle, avec une contrainte maximale, une déformation, un rapport d'extension et une résistance supérieurs de 25 à 46% à la position proximale (25%). Nous constatons également que les tissus de l'appareil digestif (à l'exclusion du rectum fortement musclé) sont généralement très extensibles et anisotropes, et ne diffèrent pas par la circonférence ou l'épaisseur de la paroi le long du tube digestif. Ces résultats contribuent à notre connaissance des propriétés mécaniques des tissus intestinaux des poissons et orientent les futures études sur les facteurs influençant l'évolution des systèmes alimentaires des poissons.

Locomotory transition from water to sand and its effects on undulatory kinematics in sand lances (Ammodytidae).

Sand lances, fishes in the genus Ammodytes, exhibit a peculiar burrowing behavior in which they appear to swim rapidly into the substrate. They use posteriorly propagated undulations of the body to move in both water, a Newtonian fluid, and in sand, a non-Newtonian, granular substrate. In typical aquatic limbless locomotion, undulations of the body push against water, which flows because it is incapable of supporting the static stresses exerted by the animal, thus the undulations move in world space (slipping wave locomotion). In typical terrestrial limbless locomotion, these undulations push against substrate irregularities and move relatively little in world space (non-slipping wave locomotion). We used standard and X-ray video to determine the roles of slipping wave and non-slipping wave locomotion during burrowing in sand lances. We find that sand lances in water use slipping wave locomotion, similar to most aquatic undulators, but switch to non-slipping waves once they burrow. We identify a progression of three stages in the burrowing process: first, aquatic undulations similar to typical anguilliform locomotion (but without head yaw) push the head into the sand; second, more pronounced undulations of the aquatic portion of the body push most of the animal below ground; third, the remaining above-ground portion of the body ceases undulation and the subterranean portion takes over, transitioning to non-slipping wave locomotion. We find no evidence that sand lances use their body motions to fluidize the sand. Instead, as soon as enough of the body is underground, they undergo a kinematic shift and locomote like terrestrial limbless vertebrates.

Whole-body lift and ground effect during pectoral fin locomotion in the northern spearnose poacher (Agonopsis vulsa).

The northern spearnose poacher, Agonopsis vulsa, is a benthic, heavily armored fish that swims primarily using pectoral fins. High-speed kinematics, whole-body lift measurements, and flow visualization were used to study how A. vulsa overcomes substantial negative buoyancy while generating forward thrust. Kinematics for five freely swimming poachers indicate that individuals tend to swim near the bottom (within 1cm) with a consistently small (less than 1 degrees ) pitch angle of the body. When the poachers swam more than 1cm above the bottom, however, body pitch angles were higher and varied inversely with speed, suggesting that lift may help overcome negative buoyancy. To determine the contribution of the body to total lift, fins were removed from euthanized fish (n=3) and the lift and drag from the body were measured in a flume. Lift and drag were found to increase with increasing flow velocity and angle of attack (ANCOVA, p<0.0001 for both effects). Lift force from the body was found to supply approximately half of the force necessary to overcome negative buoyancy when the fish were swimming more than 1cm above the bottom. Lastly, flow visualization experiments were performed to examine the mechanism of lift generation for near-bottom swimming. A vortex in the wake of the pectoral fins was observed to interact strongly with the substratum when the animals approached the bottom. These flow patterns suggest that, when swimming within 1cm of the bottom, poachers may use hydrodynamic ground effect to augment lift, thereby counteracting negative buoyancy.

The material properties of acellular bone in a teleost fish.

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. Young's 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.

Patterns of axial and appendicular movements during aquatic walking in the salamander Siren lacertina.

Most studies of salamander locomotion have focused either on swimming or terrestrial walking, but some salamanders also use limb-based locomotion while submerged under water (aquatic walking). In this study we used video motion analysis to describe the aquatic walking gait of Siren lacertina, an elongate salamander with reduced forelimbs and no hindlimbs. We found that S. lacertina uses a bipedal-undulatory gait, which combines alternating use of the forelimbs with a traveling undulatory wave. Each forelimb is in contact with the substrate for about 50% of the stride cycle and forelimbs have little temporal overlap in contact intervals. We quantified the relative timing and frequency of limb and tail movements and found that, unlike the terrestrial gaits of most salamanders, axial and appendicular movements are decoupled during aquatic walking. We found no significant relationship between stride frequency and aquatic walking velocity, but we did find a statistically significant relationship between tailbeat frequency and aquatic walking velocity, which suggests that aquatic walking speed is mainly modulated by axial movements. By comparing axial wavespeed and distance traveled per tailbeat during swimming (forelimbs not used) and aquatic walking (forelimbs used), we found lower wavespeed and greater distance traveled per tailbeat during aquatic walking. These findings suggest that the reduced forelimbs of S. lacertina contribute to forward propulsion during aquatic walking.