Skeletal anatomy of the pectoral fin in mudskipper species from terrestrial and aquatic habitats.

Mudskippers are a group of amphibious fishes in the family Oxudercidae, whose species inhabit a range of habitats from mostly aquatic to mostly terrestrial. Most of our understanding about habitat preference comes from natural history observations, particularly where they are collected (i.e., low intertidal vs. high intertidal regions). Mudskippers have undergone several morphological changes to accommodate a terrestrial life, including major changes to the pectoral and pelvic girdles. These changes result in a novel crutching gait, which mudskippers use to move over land. Though the appendicular morphology and crutching gait of mudskippers have been described in some species, few studies have compared skeletal structures across the family. In our study, we use microcomputed tomography (µCT) scans to compare the skeletal anatomy of 16 species of aquatic and terrestrial mudskippers. Linear discriminant analysis is used to analyze measurements obtained through geometric morphometrics (landmarks). We found bone structures of the pectoral region in the terrestrial group were significantly longer and wider than those in the aquatic group. Furthermore, a significant difference in anatomy is shown between terrestrial and aquatic genera with both axial and appendicular elements contributing to the separation between groups. This work describes the differences in skeletal morphology associated with terrestriality in mudskippers and provides valuable insights into specific anatomical characteristics contributing to their adaptation to novel environments.

It Pays to Be Bumpy: Drag Reducing Armor in the Pacific Spiny Lumpsucker, Eumicrotremus orbis.

Armor is a multipurpose set of structures that has evolved independently at least 30 times in fishes. In addition to providing protection, armor can manipulate flow, increase camouflage, and be sexually dimorphic. There are potential tradeoffs in armor function: increased impact resistance may come at the cost of maneuvering ability; and ornate armor may offer visual or protective advantages, but could incur excess drag. Pacific spiny lumpsuckers (Eumicrotremus orbis) are covered in rows of odontic, cone-shaped armor whorls, protecting the fish from wave driven impacts and the threat of predation. We are interested in measuring the effects of lumpsucker armor on the hydrodynamic forces on the fish. Bigger lumpsuckers have larger and more complex armor, which may incur a greater hydrodynamic cost. In addition to their protective armor, lumpsuckers have evolved a ventral adhesive disc, allowing them to remain stationary in their environment. We hypothesize a tradeoff between the armor and adhesion: little fish prioritize suction, while big fish prioritize protection. Using micro-CT, we compared armor volume to disc area over lumpsucker development and built 3D models to measure changes in drag over ontogeny. We found that drag and drag coefficients decrease with greater armor coverage and vary consistently with orientation. Adhesive disc area is isometric but safety factor increases with size, allowing larger fish to remain attached in higher flows than smaller fish.

Internal vertebral morphology of bony fishes matches the mechanical demands of different environments.

Fishes have repeatedly evolved characteristic body shapes depending on how close they live to the substrate. Pelagic fishes live in open water and typically have narrow, streamlined body shapes; benthic and demersal fishes live close to the substrate; and demersal fishes often have deeper bodies. These shape differences are often associated with behavioral differences: pelagic fishes swim nearly constantly, demersal fishes tend to maneuver near the substrate, and benthic fishes often lie in wait on the substrate. We hypothesized that these morphological and behavioral differences would be reflected in the mechanical properties of the body, and specifically in vertebral column stiffness, because it is an attachment point for the locomotor musculature and a central axis for body bending. The vertebrae of bony fishes are composed of two cones connected by a foramen, which is filled by the notochord. Since the notochord is more flexible than bony vertebral centra, we predicted that pelagic fishes would have narrower foramina or shallower cones, leading to less notochordal material and a stiffer vertebral column which might support continuous swimming. In contrast, we predicted that benthic and demersal fishes would have more notochordal material, making the vertebral column more flexible for diverse behaviors in these species. We therefore examined vertebral morphology in 79 species using micro-computed tomography scans. Six vertebral features were measured including notochordal foramen diameter, centrum body length, and the cone angles and diameters for the anterior and posterior vertebral cones, along with body fineness. Using phylogenetic generalized least squares analyses, we found that benthic and pelagic species differed significantly, with larger foramina, shorter centra, and larger cones in benthic species. Thus, morphological differences in the internal shape of the vertebrae of fishes are consistent with a stiffer vertebral column in pelagic fishes and with a more flexible vertebral column in benthic species.

Interspecific differences in the flow regimes and drag of North Pacific skate egg cases.

Skates are a diverse group of dorso-ventrally compressed cartilaginous fishes found primarily in high-latitude seas. These slow-growing oviparous fishes deposit their fertilized eggs into cases, which then rest on the seafloor. Developing skates remain in their cases for 1-4 years after they are deposited, meaning the abiotic characteristics of the deposition sites, such as current and substrate type, must interact with the capsule in a way to promote long residency. Egg cases are morphologically variable and can be identified to species. Both the gross morphology and the microstructures of the egg case interact with substrate to determine how well a case stays in place on a current-swept seafloor. Our study investigated the egg case hydrodynamics of eight North Pacific skate species to understand how their morphology affects their ability to stay in place. We used a flume to measure maximum current velocity, or "break-away velocity," each egg case could withstand before being swept off the substrate and a tilt table to measure the coefficient of static friction between each case and the substrate. We also used the programming software R to calculate theoretical drag on the egg cases of each species. For all flume trials, we found the morphology of egg cases and their orientation to flow to be significantly correlated with break-away velocity. In certain species, the morphology of the egg case was correlated with flow rate required to dislodge a case from the substrate in addition to the drag experienced in both the theoretical and flume experiments. These results effectively measure how well the egg cases of different species remain stationary in a similar habitat. Parsing out attachment biases and discrepancies in flow regimes of egg cases allows us to identify where we are likely to find other elusive species nursery sites. These results will aid predictive models for locating new nursery habitats and protective policies for avoiding the destruction of these nursery sites.

Body and Tail Coordination in the Bluespot Salamander (Ambystoma laterale) During Limb Regeneration.

Animals are incredibly good at adapting to changes in their environment, a trait envied by most roboticists. Many animals use different gaits to seamlessly transition between land and water and move through non-uniform terrains. In addition to adjusting to changes in their environment, animals can adjust their locomotion to deal with missing or regenerating limbs. Salamanders are an amphibious group of animals that can regenerate limbs, tails, and even parts of the spinal cord in some species. After the loss of a limb, the salamander successfully adjusts to constantly changing morphology as it regenerates the missing part. This quality is of particular interest to roboticists looking to design devices that can adapt to missing or malfunctioning components. While walking, an intact salamander uses its limbs, body, and tail to propel itself along the ground. Its body and tail are coordinated in a distinctive wave-like pattern. Understanding how their bending kinematics change as they regrow lost limbs would provide important information to roboticists designing amphibious machines meant to navigate through unpredictable and diverse terrain. We amputated both hindlimbs of blue-spotted salamanders (Ambystoma laterale) and measured their body and tail kinematics as the limbs regenerated. We quantified the change in the body wave over time and compared them to an amphibious fish species, Polypterus senegalus. We found that salamanders in the early stages of regeneration shift their kinematics, mostly around their pectoral girdle, where there is a local increase in undulation frequency. Amputated salamanders also show a reduced range of preferred walking speeds and an increase in the number of bending waves along the body. This work could assist roboticists working on terrestrial locomotion and water to land transitions.

A Tail of Four Fishes: An Analysis of Kinematics and Material Properties of Elongate Fishes.

The elongate body plan is present in many groups of fishes, and this morphology dictates functional consequences seen in swimming behavior. Previous work has shown that increasing the number of vertebrae, or decreasing the intervertebral joint length, in a fixed length artificial system increases stiffness. Tails with increased stiffness can generate more power from tail beats, resulting in an increased mean swimming speed. This demonstrates the impacts of morphology on both material properties and kinematics, establishing mechanisms for form contributing to function. Here, we wanted to investigate relationships between form and ecological function, such as differences in dietary strategies and habitat preferences among fish species. This study aims to characterize and compare the kinematics, material properties, and vertebral morphology of four species of elongate fishes: Anoplarchus insignis, Anoplarchus purpurescens, Xiphister atropurpureus, and Xiphister mucosus. We hypothesized that these properties would differ among the four species due to their differential ecological niches. To calculate kinematic variables, we filmed these fishes swimming volitionally. We also measured body stiffness by bending the abdominal and tail regions of sacrificed individuals in different stages of dissection (whole body, removed skin, and removed muscle). Finally, we counted the number of vertebrae from CT scans of each species to quantify vertebral morphology. Principal component and linear discriminant analyses suggested that the elongate fish species can be distinguished from one another by their material properties, morphology, and swimming kinematics. With this information combined, we can draw connections between the physical properties of the fishes and their ecological niches.

Foretelling the Flex-Vertebral Shape Predicts Behavior and Ecology of Fishes.

We modeled swimming kinematics and body mechanics of several fish species of varying habitat and body shape based on measurements of internal vertebral morphology. SYNOPSIS: One key evolutionary innovation that separates vertebrates from invertebrates is the notochord, a central element that provides the stiffness needed for powerful movements. Later, the notochord was further stiffened by the vertebrae, cartilaginous, and bony elements, surrounding the notochord. The ancestral notochord is retained in modern vertebrates as intervertebral material, but we know little about its mechanical interactions with surrounding vertebrae. In this study, the internal shape of the vertebrae-where this material is found-was quantified in 16 species of fishes with various body shapes, swimming modes, and habitats. We used micro-computed tomography to measure the internal shape. We then created and mechanically tested physical models of intervertebral joints. We also mechanically tested actual vertebrae of five species. Material testing shows that internal morphology of the centrum significantly affects bending and torsional stiffness. Finally, we performed swimming trials to gather kinematic data. Combining these data, we created a model that uses internal vertebral morphology to make predictions about swimming kinematics and mechanics. We used linear discriminant analysis (LDA) to assess the relationship between vertebral shape and our categorical traits. The analysis revealed that internal vertebral morphology is sufficient to predict habitat, body shape, and swimming mode in our fishes. This model can also be used to make predictions about swimming in fishes not easily studied in the laboratory, such as deep sea and extinct species, allowing the development of hypotheses about their natural behavior.

Meral-Spot Reflectance Signals Weapon Performance in the Mantis Shrimp Neogonodactylus oerstedii (Stomatopoda).

During animal contests over resources, opponents often signal their fighting ability in an attempt to avoid escalating to physical attack. A reliable signal is beneficial to receivers because it allows them to avoid injuries from engaging in contests they are unlikely to win. However, a signaler could benefit from deceiving an opponent by signaling greater fighting ability or greater aggressive intent than the signaler possesses. Therefore, the reliability of agonistic signals has long intrigued researchers. We investigated whether a colored patch, the meral spot, signals weapon performance in the stomatopod Neogonodactylus oerstedii. During fights over possession of refuges, stomatopods can injure or even kill opponents with their ultrafast strike. We found that darker meral spots correlate with higher strike impulse, which reflects the total force integrated over time. Furthermore, we demonstrate that stomatopods that strike more often with both appendages have darker meral spots and that the first hit in a two-appendage strike has a greater mean strike impulse than that of a single-appendage strike. This indicates that stomatopods with darker meral spots tend to invest more energy in each strike. Our results provide evidence that stomatopods use total reflectance as an honest signal of weapon performance or aggressive intent. This improves our understanding of the evolution of agonistic signals.

Three-dimensional movements of the pectoral fin during yaw turns in the Pacific spiny dogfish, Squalus suckleyi.

Fish pectoral fins move in complex ways, acting as control surfaces to affect force balance during swimming and maneuvering. Though objectively less dynamic than their actinopterygian relatives, shark pectoral fins undergo complex conformational changes and movements during maneuvering. Asynchronous pectoral fin movement is documented during yaw turning in at least two shark species but the three-dimensional (3D) rotation of the fin about the body axes is unknown. We quantify the 3D actuation of the pectoral fin base relative to the body axes. We hypothesized that Pacific spiny dogfish rotate pectoral fins with three degrees of freedom relative to the body during volitional turning. The pectoral fin on the inside of the turn is consistently protracted, supinated and depressed. Additionally, turning angular velocity increased with increasing fin rotation. Estimated drag on the fin increased and the shark decelerated during turning. Based on these findings, we propose that Pacific spiny dogfish uses drag-based turning during volitional swimming. Post-mortem muscle stimulation revealed depression, protraction and supination of the pectoral fin through stimulation of the ventral and cranial pterygoideus muscles. These data confirm functional hypotheses about pectoral fin musculature and suggest that Pacific spiny dogfish actively rotate pectoral fins to facilitate drag-based turning.This article has an associated First Person interview with the first author of the paper.

Long-axis twisting during locomotion of elongate fishes.

Fish live in a complex world and must actively adapt their swimming behavior to a range of environments. Most studies of swimming kinematics focus on two-dimensional properties related to the bending wave that passes from head to tail. However, fish also twist their bodies three dimensionally around their longitudinal axis as the bending wave passes down the body. We measured and characterized this movement, which we call 'wobble', in six species of elongate fishes (Anoplarchus insignis, Xiphister mucosus, Lumpenus sagitta, Pholis laeta, Apodichthys flavidus and Ronquilus jordani) from three different habitats (intertidal, nearshore and subtidal) using custom video analysis software. Wobble and bending are synchronized, with a phase shift between the wobble wave and bending wave. We found that species from the same habitats swim in similar ways, even if they are more closely related to species from different habitats. In nearshore species, the tail wobbles the most but, in subtidal and intertidal species, the head wobbles more than or the same as the tail. We also wanted to understand the relationship between wobble and the passive mechanics of the fish bodies. Therefore, we measured torsional stiffness and modulus along the body and found that modulus increases from head to tail in all six species. As wobble does not correlate with the passive properties of the body, it may play a different role in swimming behavior of fishes from different habitats.