Flexibility is a hidden axis of biomechanical diversity in fishes.

Nearly all fish have flexible bodies that bend as a result of internal muscular forces and external fluid forces that are dynamically coupled with the mechanical properties of the body. Swimming is therefore strongly influenced by the body's flexibility, yet we do not know how fish species vary in their flexibility and in their ability to modulate flexibility with muscle activity. A more fundamental problem is our lack of knowledge about how any of these differences in flexibility translate into swimming performance. Thus, flexibility represents a hidden axis of diversity among fishes that may have substantial impacts on swimming performance. Although engineers have made substantial progress in understanding these fluid-structure interactions using physical and computational models, the last biological review of these interactions and how they give rise to fish swimming was carried out more than 20 years ago. In this Review, we summarize work on passive and active body mechanics in fish, physical models of fish and bioinspired robots. We also revisit some of the first studies to explore flexural stiffness and discuss their relevance in the context of more recent work. Finally, we pose questions and suggest future directions that may help reveal important links between flexibility and swimming performance.

Connecting materials, performance and evolution: a case study of the glue of moth-catching spiders (Cyrtarachninae).

Morphological structures and extended phenotypes are made possible by materials that are encoded by the genome. Nearly all biomaterials are viscoelastic, which means that to understand performance, one must understand the strain rate-dependent properties of these materials in relevant ecological interactions, as the behavior of a material can vary dramatically and rapidly. Spider silks are an example of materials whose properties vary substantially intra- and inter-specifically. Here, we focus on aggregate silk, which functions as a biological adhesive. As a case study to understand how a material manifests from genome through organism to ecology, we highlight moth-specialist spiders, the Cyrtarachninae, and their glues as an ideal experimental system to investigate the relationship between genomics and ecologically variable performance of a biological material. There is a clear eco-evolutionary innovation that Cyrtarachne akirai and related species have evolved, a unique trait not found in other spiders, a glue which overcomes the scales of moths. By examining traditional orb-weavers, C. akirai and other subfamily members using biomechanical testing and genomic analysis, we argue that we can track the evolution of this novel bioadhesive and comment on the selection pressures influencing prey specialization. The importance of the ecological context of materials testing is exemplified by the poor performance of C. akirai glue on glass and the exceptional spreading ability and adhesive strength on moths. The genetic basis for these performance properties is experimentally tractable because spider silk genes are minimally pleiotropic and advances in genomic technologies now make possible the discovery of complete silk gene sequences.

Scaling of swimming performance in baleen whales.

The scale dependence of locomotor factors has long been studied in comparative biomechanics, but remains poorly understood for animals at the upper extremes of body size. Rorqual baleen whales include the largest animals, but we lack basic kinematic data about their movements and behavior below the ocean surface. Here, we combined morphometrics from aerial drone photogrammetry, whale-borne inertial sensing tag data and hydrodynamic modeling to study the locomotion of five rorqual species. We quantified changes in tail oscillatory frequency and cruising speed for individual whales spanning a threefold variation in body length, corresponding to an order of magnitude variation in estimated body mass. Our results showed that oscillatory frequency decreases with body length (∝length-0.53) while cruising speed remains roughly invariant (∝length0.08) at 2 m s-1 We compared these measured results for oscillatory frequency against simplified models of an oscillating cantilever beam (∝length-1) and an optimized oscillating Strouhal vortex generator (∝length-1). The difference between our length-scaling exponent and the simplified models suggests that animals are often swimming non-optimally in order to feed or perform other routine behaviors. Cruising speed aligned more closely with an estimate of the optimal speed required to minimize the energetic cost of swimming (∝length0.07). Our results are among the first to elucidate the relationships between both oscillatory frequency and cruising speed and body size for free-swimming animals at the largest scale.

The notochord in Atlantic salmon (Salmo salar L.) undergoes profound morphological and mechanical changes during development.

We present the development of the notochord of the Atlantic salmon (Salmo salar L.), from early embryo to sexually mature fish. Over the salmon's lifespan, profound morphological changes occur. Cells and gross structures of the notochord reorganize twice. In the embryo, the volume of the notochord is dominated by large, vacuolated chordocytes; each cell can be modeled as a hydrostat organized into a larger cellular-hydrostat network, structurally bound together with desmosomes. After the embryo hatches and grows into a fry, vacuolated chordocytes disappear, replaced by extracellular lacunae. The formation of mineralized, segmental chordacentra stiffens the notochord and creates intervertebral joints, where tissue strain during lateral bending is now focused. As development proceeds towards the parr stage, a process of devacuolization and intracellular filament accumulation occur, forming highly dense, non-vacuolated chordocytes. As extracellular lacunae enlarge, they are enclosed by dense filamentous chordocytes that form transverse intervertebral septa, which are connected to the intervertebral ligaments, and a longitudinal notochordal strand. In the vertebral column of pelagic adults, large vacuolated chordocytes reappear; cells of this secondary population have a volume up to 19 000 times larger than the primary vacuolated chordocytes of the early notochord. In adults the lacunae have diminished in relative size. Hydrostatic pressure within the notochord increases significantly during growth, from 525 Pa in the alevins to 11 500 Pa in adults, at a rate of increase with total body length greater than that expected by static stress similarity. Pressure and morphometric measurements were combined to estimate the stress in the extracellular material of the notochordal sheath and intervertebral ligaments and the flexural stiffness of the axial skeleton. The functional significance of the morphological changes in the axial skeleton is discussed in relation to the different developmental stages and locomotor behavior changes over the lifespan of the fish.

Automatic control: the vertebral column of dogfish sharks behaves as a continuously variable transmission with smoothly shifting functions.

During swimming in dogfish sharks, Squalus acanthias, both the intervertebral joints and the vertebral centra undergo significant strain. To investigate this system, unique among vertebrates, we cyclically bent isolated segments of 10 vertebrae and nine joints. For the first time in the biomechanics of fish vertebral columns, we simultaneously characterized non-linear elasticity and viscosity throughout the bending oscillation, extending recently proposed techniques for large-amplitude oscillatory shear (LAOS) characterization to large-amplitude oscillatory bending (LAOB). The vertebral column segments behave as non-linear viscoelastic springs. Elastic properties dominate for all frequencies and curvatures tested, increasing as either variable increases. Non-linearities within a bending cycle are most in evidence at the highest frequency, 2.0 Hz, and curvature, 5 m-1 Viscous bending properties are greatest at low frequencies and high curvatures, with non-linear effects occurring at all frequencies and curvatures. The range of mechanical behaviors includes that of springs and brakes, with smooth transitions between them that allow for continuously variable power transmission by the vertebral column to assist in the mechanics of undulatory propulsion.

Special Prey, Special Glue: NMR Spectroscopy on Aggregate Glue Components of Moth-Specialist Spiders, Cyrtarachninae.

Orb-weaver spiders produce upwards of seven different types of silk, each with unique material properties. We focus on the adhesive within orb-weaving spider webs, aggregate glue silk. These droplets are composed of three main components: water, glycoproteins, and a wide range of low molecular mass compounds (LMMCs). These LMMCs are known to play a crucial role in maintaining the material properties of the glycoproteins, aid in water absorption from the environment, and increase surface adhesion. Orb-weavers within the Cyrtarachninae subfamily are moth specialists and have evolved glue droplets with novel material properties. This study investigated the biochemical composition and diversity of the LMMCs present in the aggregate glue of eight moth-specialist species and compared them with five generalist orb-weavers using nuclear magnetic resonance (NMR) spectroscopy. We hypothesized that the novel drying ability of moth-specialist glue was accompanied by novel LMMCs and lower overall percentages by silk weight of LMMCs. We measured no difference in LMMC weight by the type of prey specialization, but observed novel compositions in the glue of all eight moth-catching species. Further, we quantified the presence of a previously reported but unidentified compound that appears in the glue of all moth specialists. These silks can provide insight into the functions of bioadhesives and inform our own synthetic adhesives.

Behavior and Bioadhesives: How Bolas Spiders, Mastophora hutchinsoni, Catch Moths.

Spiders use various combinations of silks, adhesives, and behaviors to ensnare and trap prey. A common but difficult to catch prey in most spider habitats are moths. They easily escape typical orb-webs because their bodies are covered in sacrificial scales that flake off when in contact with the web's adhesives. This defense is defeated by spiders of the sub-family of Cyrtarachninae, moth-catching specialists who combine changes in orb-web structure, predatory behavior, and chemistry of the aggregate glue placed in those webs. The most extreme changes in web structure are shown by bolas spiders, who create a solitary capture strand containing only one or two glue droplets at the end of a single thread. They prey on male moths by releasing pheromones to draw them within range of their bolas, which they flick to ensnare the moth. We used a high-speed video camera to capture the behavior of the bolas spider Mastophora hutchinsoni. We calculated the kinematics of spiders and moths in the wild to model the physical and mechanical properties of the bolas during prey capture, the behavior of the moth, and how these factors lead to successful prey capture. We created a numerical model to explain the mechanical behavior of the bolas silk during prey capture. Our kinematic analysis shows that the material properties of the aggregate glue bolas of M. hutchinsoni are distinct from that of the other previously analyzed moth-specialist, Cyrtarachne akirai. The spring-like behavior of the M. hutchinsoni bolas suggests it spins a thicker liquid.

Sink and swim: kinematic evidence for lifting-body mechanisms in negatively buoyant electric rays Narcine brasiliensis.

Unlike most batoid fishes, electric rays neither oscillate nor undulate their body disc to generate thrust. Instead they use body-caudal-fin (BCF) locomotion. In addition, these negatively buoyant rays perform unpowered glides as they sink in the water column. In combination, BCF swimming and unpowered gliding are opposite ends on a spectrum of swimming, and electric rays provide an appropriate study system for understanding how the performance of each mode is controlled hydrodynamically. We predicted that the dorso-ventrally flattened body disc generates lift during both BCF swimming and gliding. To test this prediction, we examined 10 neonate lesser electric rays, Narcine brasiliensis, as they swam and glided. From video, we tracked the motion of the body, disc, pelvic fins and tail. By correlating changes in the motions of those structures with swimming performance, we have kinematic evidence that supports the hypothesis that the body disc is generating lift. Most importantly, both the pitch of the body disc and the tail, along with undulatory frequency, interact to control horizontal swimming speed and Strouhal number during BCF swimming. During gliding, the pitch of the body disc and the tail also interact to control the speed on the glide path and the glide angle.

Biorobotic insights into neuromechanical coordination of undulatory swimming.

Skin sensors on an eel-like robot couple external hydrodynamic pressure with internal neural patterns for robust swimming.

Embodied Computational Evolution: Feedback Between Development and Evolution in Simulated Biorobots.

Given that selection removes genetic variance from evolving populations, thereby reducing exploration opportunities, it is important to find mechanisms that create genetic variation without the disruption of adapted genes and genomes caused by random mutation. Just such an alternative is offered by random epigenetic error, a developmental process that acts on materials and parts expressed by the genome. In this system of embodied computational evolution, simulated within a physics engine, epigenetic error was instantiated in an explicit genotype-to-phenotype map as transcription error at the initiation of gene expression. The hypothesis was that transcription error would create genetic variance by shielding genes from the direct impact of selection, creating, in the process, masquerading genomes. To test this hypothesis, populations of simulated embodied biorobots and their developmental systems were evolved under steady directional selection as equivalent rates of random mutation and random transcriptional error were covaried systematically in an 11 × 11 fully factorial experimental design. In each of the 121 different experimental conditions (unique combinations of mutation and transcription error), the same set of 10 randomly created replicate populations of 60 individuals were evolved. Selection for the improved locomotor behavior of individuals led to increased mean fitness of populations over 100 generations at nearly all levels and combinations of mutation and transcription error. When the effects of both types of error were partitioned statistically, increasing transcription error was shown to increase the final genetic variance of populations, incurring a fitness cost but acting on variance independently and differently from genetic mutation. Thus, random epigenetic errors in development feed back through selection of individuals with masquerading genomes to the population's genetic variance over generational time. Random developmental processes offer an additional mechanism for exploration by increasing genetic variation in the face of steady, directional selection.

Morphological Evolution: Bioinspired Methods for Analyzing Bioinspired Robots.

To fully understand the evolution of complex morphologies, analyses cannot stop at selection: It is essential to investigate the roles and interactions of multiple processes that drive evolutionary outcomes. The challenges of undertaking such analyses have affected both evolutionary biologists and evolutionary roboticists, with their common interests in complex morphologies. In this paper, we present analytical techniques from evolutionary biology, selection gradient analysis and morphospace walks, and we demonstrate their applicability to robot morphologies in analyses of three evolutionary mechanisms: randomness (genetic mutation), development (an explicitly implemented genotype-to-phenotype map), and selection. In particular, we applied these analytical techniques to evolved populations of simulated biorobots-embodied robots designed specifically as models of biological systems, for the testing of biological hypotheses-and we present a variety of results, including analyses that do all of the following: illuminate different evolutionary dynamics for different classes of morphological traits; illustrate how the traits targeted by selection can vary based on the likelihood of random genetic mutation; demonstrate that selection on two selected sets of morphological traits only partially explains the variance in fitness in our biorobots; and suggest that biases in developmental processes could partially explain evolutionary dynamics of morphology. When combined, the complementary analytical approaches discussed in this paper can enable insight into evolutionary processes beyond selection and thereby deepen our understanding of the evolution of robotic morphologies.

Heads and tails: The notochord develops differently in the cranium and caudal fin of Atlantic Salmon (Salmo salar, L.).

While it is well known that the notochord of bony fishes changes over developmental time, less is known about how it varies across different body regions. In the development of the Atlantic salmon, Salmo salar L., cranial and caudal ends of the notochord are overlaid by the formation of the bony elements of the neurocranium and caudal fin, respectively. To investigate, we describe how the notochord of the cranium and caudal fin changes from embryo to spawning adult, using light microscopy, SEM, TEM, dissection, and CT scanning. The differences are dramatic. In contrast to the abdominal and caudal regions, at the ends of the notochord vertebrae never develop. While the cranial notochord builds a tapering, unsegmented cone of chordal bone, the urostylic notochordal sheath never ossifies: adjacent, irregular bony elements form from the endoskeleton of the caudal fin. As development progresses, two previously undescribed processes occur. First, the bony cone of the cranial notochord, and its internal chordocytes, are degraded by chordoclasts, an undescribed function of the clastic cell type. Second, the sheath of the urostylic notochord creates transverse septae that partly traverse the lumen in an irregular pattern. By the adult stage, the cranial notochord is gone. In contrast, the urostylic notochord in adults is robust, reinforced with septae, covered by irregularly shaped pieces of cellular bone, and capped with an opistural cartilage that develops from the sheath of the urostylic notochord. A previously undescribed muscle, with its origin on the opistural cartilage, inserts on the lepidotrich ventral to it.

Rumors of Our Death .

Núñez and colleagues (2019) question whether cognitive science still exists "as a coherent academic field with a well-defined and cohesive interdisciplinary research program." This worry may be premature on two grounds. First, we are not convinced that the Lakatosian criterion of coalescence around a core framework is the best standard for judging whether a field is well-defined and productive. Second, although we acknowledge that cognitive science is not as visible as we would like, we doubt that this low profile accurately reflects the state of actual research and teaching programs based on the cognitive science approach.

Evolution of behavior and neural control of the fast-start escape response.

The fast-start startle behavior is the primary mechanism of rapid escape in fishes and is a model system for examining neural circuit design and musculoskeletal function. To develop a dataset for evolutionary analysis of the startle response, the kinematics and muscle activity patterns of the fast-start were analyzed for four fish species at key branches in the phylogeny of vertebrates. Three of these species (Polypterus palmas, Lepisosteus osseus, and Amia calva) represent the base of the actinopterygian radiation. A fourth species (Oncorhynchus mykiss) provided data for a species in the central region of the teleost phylogeny. Using these data, we explored the evolution of this behavior within the phylogeny of vertebrates. To test the hypothesis that startle features are evolutionarily conservative, the variability of motor patterns and kinematics in fast-starts was described. Results show that the evolution of the startle behavior in fishes, and more broadly among vertebrates, is not conservative. The fast-start has undergone substantial change in suites of kinematics and electromyogram features, including the presence of either a one- or a two-stage kinematic response and change in the extent of bilateral muscle activity. Comparative methods were used to test the evolutionary hypothesis that changes in motor control are correlated with key differences in the kinematics and behavior of the fast-start. Significant evolutionary correlations were found between several motor pattern and behavioral characters. These results suggest that the startle neural circuit itself is not conservative. By tracing the evolution of motor pattern and kinematics on a phylogeny, it is shown that major changes in the neural circuit of the startle behavior occur at several levels in the phylogeny of vertebrates.

Axial systems and their actuation: new twists on the ancient body of craniates.

Craniate animals--vertebrates and their jawless sister taxa--have evolved a body axis with powerful muscles, a distributed nervous system to control those muscles, and an endoskeleton that starts at the head and ends at the caudal fin. The body axis undulates, bends, twists, or holds firm, depending on the behavior. In this introduction to the special issue on axial systems and their actuation, we provide an overview of the latest research on how the body axis functions, develops, and evolves. Based on this research, we hypothesize that the body axis of craniates has three primary, post-cranial modules: precaudal, caudal, and tail. The term "module" means a portion of the body axis that functions, develops, and evolves in relative independence from other modules; "relative independence" means that structures and processes within a module are more tightly correlated in function, development, and behavior than the same processes are among modules.

Jumping sans legs: does elastic energy storage by the vertebral column power terrestrial jumps in bony fishes?

Despite having no obvious anatomical modifications to facilitate movement over land, numerous small fishes from divergent teleost lineages make brief, voluntary terrestrial forays to escape poor aquatic conditions or to pursue terrestrial prey. Once stranded, these fishes produce a coordinated and effective "tail-flip" jumping behavior, wherein lateral flexion of the axial body into a C-shape, followed by contralateral flexion of the body axis, propels the fish into a ballistic flight-path that covers a distance of multiple body lengths. We ask: how do anatomical structures that evolved in one habitat generate effective movement in a novel habitat? Within this context, we hypothesized that the mechanical properties of the axial skeleton play a critical role in producing effective overland movement, and that tail-flip jumping species demonstrate enhanced elastic energy storage through increased body flexural stiffness or increased body curvature, relative to non-jumping species. To test this hypothesis, we derived a model to predict elastic recoil work from the morphology of the vertebral (neural and hemal) spines. From ground reaction force (GRF) measurements and high-speed video, we calculated elastic recoil work, flexural stiffness, and apparent material stiffness of the body for Micropterus salmoides (a non-jumper) and Kryptolebias marmoratus (adept tail-flip jumper). The model predicted no difference between the two species in work stored by the vertebral spines, and GRF data showed that they produce the same magnitude of mass-specific elastic recoil work. Surprisingly, non-jumper M. salmoides has a stiffer body than tail-flip jumper K. marmoratus. Many tail-flip jumping species possess enlarged, fused hypural bones that support the caudal peduncle, which suggests that the localized structures, rather than the entire axial skeleton, may explain differences in terrestrial performance.

Built for speed: strain in the cartilaginous vertebral columns of sharks.

In most bony fishes vertebral column strain during locomotion is almost exclusively in the intervertebral joints, and when these joints move there is the potential to store and release strain energy. Since cartilaginous fishes have poorly mineralized vertebral centra, we tested whether the vertebral bodies undergo substantial strain and thus may be sites of energy storage during locomotion. We measured axial strains of the intervertebral joints and vertebrae in vivo and ex vivo to characterize the dynamic behavior of the vertebral column. We used sonomicrometry to directly measure in vivo and in situ strains of intervertebral joints and vertebrae of Squalus acanthias swimming in a flume. For ex vivo measurements, we used a materials testing system to dynamically bend segments of vertebral column at frequencies ranging from 0.25 to 1.00 Hz and a range of physiologically relevant curvatures, which were determined using a kinematic analysis. The vertebral centra of S. acanthias undergo strain during in vivo volitional movements as well as in situ passive movements. Moreover, when isolated segments of vertebral column were tested during mechanical bending, we measured the same magnitudes of strain. These data support our hypothesis that vertebral column strain in lateral bending is not limited to the intervertebral joints. In histological sections, we found that the vertebral column of S. acanthias has an intracentral canal that is open and covered with a velum layer. An open intracentral canal may indicate that the centra are acting as tunics around some sections of a hydrostat, effectively stiffening the vertebral column. These data suggest that the entire vertebral column of sharks, both joints and centra, is mechanically engaged as a dynamic spring during locomotion.

Are you positive? Electric dipole polarity discrimination in the yellow stingray, Urobatis jamaicensis.

It is well established that elasmobranchs can detect dipole electric fields. However, it is unclear whether they can discriminate between the anode and cathode. To investigate this subject, we employed a behavioral assay to determine the discriminatory ability of the yellow stingray, Urobatis jamaicensis. We conditioned stingrays with food rewards to bite either the anode (n=5) or the cathode (n=6) of a direct-current dipole located on the floor of an experimental tank. All individuals successfully performed the task after 18 to 22 days. Stingrays were then tested in experimental sessions when they were rewarded only after they identified the correct pole. Stingrays successfully discriminated between the poles at a rate greater than chance, ranging among individuals from a mean of 66% to 93% correct. During experimental sessions, stingrays conditioned to distinguish the anode performed similarly to those conditioned to distinguish the cathode. We hypothesize that the ability to discriminate anode from cathode is physiologically encoded, but its utility in providing spatial information under natural conditions remains to be demonstrated. The ability to discriminate polarity may eliminate ambiguity in induction-based magnetoreception and facilitate navigation with respect to the geomagnetic field.

Swimming fundamentals: turning performance of leopard sharks (Triakis semifasciata) is predicted by body shape and postural reconfiguration.

Turns are essential maneuvers that sharks employ when foraging, feeding, and migrating. How well any individual performs in turning is determined, in part, by the static form and postural reconfiguration of its body. Since the importance of postural reconfiguration in determining turning performance is not well understood, our goal was to examine how body form and posture correlate with turning performance in juvenile leopard sharks, Triakis semifasciata. From videos of sharks turning laterally in yaw, performance was measured as turning radius, turning angle, angular speed of the head, and translational speed of the body along its path. Body form variables included the body's length, mass, width, second moment of area, and mass moment of inertia. Postural variables included body-bending coefficient, body flexion at different longitudinal positions, and lag time between body flexion and turning of the center of rotation. Using step-wise linear regression followed by multiple regression, each performance variable was regressed onto three pools of independent variables: (i) all form variables alone, (ii) all postural variables alone, and (iii) a combination of all form and postural variables. From these correlations, it appears that turning performance may be controlled primarily by the magnitude and timing of the flexion of the body. In other words, sharks alter how they turn by changing the pattern in which they bend their bodies; the body acts as a dynamically reconfiguring rudder.