Bioinspired Design in Research: Evolution as Beta-Testing.

Modern fishes represent over 400 million years of evolutionary processes that, in many cases, resulted in selection for phenotypes with particular performance advantages. While this certainly occurred without a trajectory for optimization, it cannot be denied that some morphologies allow organisms to be more effective than others at tasks like evading predation, securing food, and ultimately passing on their genes. In this way, evolution generates a series of iterative prototypes with varying but measurable success in accomplishing objectives. Therefore, careful analysis of fundamental properties underlying biological phenomena allow us to fast-track development of bioinspired technologies aiming to accomplish similar objectives. At the same time, bioinspired designs can be a way to explore evolutionary processes, by better understanding the performance space within which a given morphology operates. Through strong interdisciplinary collaborations, we can develop novel bioinspired technologies that not only excel as robotic devices but that teach us something about biology and the rules of life in the process.

An Adaptable Flying Fish Robotic Model for Aero- and Hydrodynamic Experimentation.

Flying fishes (family Exocoetidae) are known for achieving multi-modal locomotion through air and water. Previous work on understanding this animal's aerodynamic and hydrodynamic nature has been based on observations, numerical simulations, or experiments on preserved dead fish, and has focused primarily on flying pectoral fins. The first half of this paper details the design and validation of a modular flying fish inspired robotic model organism (RMO). The second half delves into a parametric aerodynamic study of flying fish pelvic fins, which to date have not been studied in-depth. Using wind tunnel experiments at a Reynolds number of 30,000, we investigated the effect of the pelvic fin geometric parameters on aerodynamic efficiency and longitudinal stability. The pelvic fin parameters investigated in this study include the pelvic fin pitch angle and its location along the body. Results show that the aerodynamic efficiency is maximized for pelvic fins located directly behind the pectoral fins and is higher for more positive pitch angles. In contrast, pitching stability is neither achievable for positive pitching angles nor pelvic fins located directly below the pectoral fin. Thus, there is a clear a trade-off between stability and lift generation, and an optimal pelvic fin configuration depends on the flying fish locomotion stage, be it gliding, taxiing, or taking off. The results garnered from the RMO experiments are insightful for understanding the physics principles governing flying fish locomotion and designing flying fish inspired aerial-aquatic vehicles.

They like to move it (move it): walking kinematics of balitorid loaches of Thailand.

Balitorid loaches are a family of fishes that exhibit morphological adaptations to living in fast flowing water, including an enlarged sacral rib that creates a 'hip'-like skeletal connection between the pelvis and the axial skeleton. The presence of this sacral rib, the robustness of which varies across the family, is hypothesized to facilitate terrestrial locomotion seen in the family. Terrestrial locomotion in balitorids is unlike that of any known fish: the locomotion resembles that of terrestrial tetrapods. Emergence and convergence of terrestrial locomotion from water to land has been studied in fossils; however, studying balitorid walking provides a present-day natural laboratory to examine the convergent evolution of walking movements. We tested the hypothesis that balitorid species with more robust connections between the pelvic and axial skeleton (M3 morphotype) are more effective at walking than species with reduced connectivity (M1 morphotype). We predicted that robust connections would facilitate travel per step and increase mass support during movement. We collected high-speed video of walking in seven balitorid species to analyze kinematic variables. The connection between internal anatomy and locomotion on land are revealed herein with digitized video analysis, µCT scans, and in the context of the phylogenetic history of this family of fishes. Our species sampling covered the extremes of previously identified sacral rib morphotypes, M1 and M3. Although we hypothesized the robustness of the sacral rib to have a strong influence on walking performance, there was not a large reduction in walking ability in the species with the least modified rib (M1). Instead, walking kinematics varied between the two balitorid subfamilies with a generally more 'walk-like' behavior in the Balitorinae and more 'swim-like' behavior in the Homalopteroidinae. The type of terrestrial locomotion displayed in balitorids is unique among living fishes and aids in our understanding of the extent to which a sacral connection facilitates terrestrial walking.

Remoras pick where they stick on blue whales.

Animal-borne video recordings from blue whales in the open ocean show that remoras preferentially adhere to specific regions on the surface of the whale. Using empirical and computational fluid dynamics analyses, we show that remora attachment was specific to regions of separating flow and wakes caused by surface features on the whale. Adhesion at these locations offers remoras drag reduction of up to 71-84% compared with the freestream. Remoras were observed to move freely along the surface of the whale using skimming and sliding behaviors. Skimming provided drag reduction as high as 50-72% at some locations for some remora sizes, but little to none was available in regions where few to no remoras were observed. Experimental work suggests that the Venturi effect may help remoras stay near the whale while skimming. Understanding the flow environment around a swimming blue whale will inform the placement of biosensor tags to increase attachment time for extended ecological monitoring.

Skeletal and muscular pelvic morphology of hillstream loaches (Cypriniformes: Balitoridae).

The rheophilic hillstream loaches (Balitoridae) of South and Southeast Asia possess a range of pelvic girdle morphologies, which may be attributed to adaptations for locomotion against rapidly flowing water. Specifically, the connectivity of the pelvic plate (basipterygium) to the vertebral column via a sacral rib, and the relative size and shape of the sacral rib, fall within a spectrum of three discrete morphotypes: long, narrow rib that meets the basipterygium; thicker, slightly curved rib meeting the basipterygium; and robust crested rib interlocking with the basipterygium. Species in this third category with more robust sacral rib connections between the basipterygium and vertebral column are capable of walking out of water with a tetrapod-like lateral-sequence, diagonal-couplet gait. This behavior has not been observed in species lacking direct skeletal connection between the vertebrae and the pelvis. The phylogenetic positions of the morphotypes were visualized by matching the morphological features onto a novel hypothesis of relationships for the family Balitoridae. The morphotypes determined through skeletal morphology were correlated with patterns observed in the pelvic muscle morphology of these fishes. Transitions towards increasingly robust pelvic girdle attachment were coincident with a more anterior origin on the basipterygium and more lateral insertion of the muscles on the fin rays, along with a reduction of the superficial abductors and adductors with more posterior insertions. These modifications are expected to provide a mechanical advantage for generating force against the ground. Inclusion of the enigmatic cave-adapted balitorid Cryptotora thamicola into the most data-rich balitorid phylogeny reveals its closest relatives, providing insight into the origin of the skeletal connection between the axial skeleton and basipterygium.

Parenting Through Academia as a SICB Member.

The Society for Integrative and Comparative Biology (SICB) has made tremendous improvements to their annual meeting in an effort to promote inclusivity, diversity, and accessibility to all scientists. However, within academia as an institution overall, many scientists face personal challenges that directly compete with the rigorous culture considered a requirement for success as an academic. Among these challenges is balancing parenthood with academic responsibilities, such as conference attendance and productivity. Herein, we present a report of the survey administered to the members of SICB and from discussion held during the Parenting through Academia workshop at the 2020 annual meeting. We hope that this information brings to the Society an opportunity for open collegial discussion, mentorship, and community building, and sheds light on new strategies that could be undertaken to support not only parents, but SICB membership as a whole.

Sucker with a fat lip: The soft tissues underlying the viscoelastic grip of remora adhesion.

Remoras are fishes that attach to a broad range of hosts using an adhesive disc on their head that is derived from dorsal fin elements. Research on the adhesive mechanism of remoras has focused primarily on the skeletal components of the disc and their contribution to generating suction and friction. However, the soft tissues of the disc, such as the soft lip surrounding the bony disc and the muscles that control the bony lamellae, have been largely ignored. To understand the sealing mechanism of the disc, it is imperative to understand the tissue morphology and material properties of the soft lip. Here, we show that the soft lip surrounding the remora disc is comprised of discrete multilayered collagen, fat, and elastic tissues which we hypothesize to have specific roles in the viscoelastic sealing mechanism of the remora disc. The central, heavily vascularized fat and collagen layer are infiltrated by strands of elastic tissue and surrounded by crossed-fiber collagen. A newly described jubilee muscle underneath the adhesive disc provides a mechanism for stopping venous return from the disc lip, thereby allowing it to become engorged and create a pressurized fit to the attachment substrate. Thus, the remora lip acts as a vascular hydrostat.

Morphology, performance and fluid dynamics of the crayfish escape response.

Sexual selection can result in an exaggerated morphology that constrains locomotor performance. We studied the relationship between morphology and the tail-flip escape response in male and female rusty crayfish (Faxonius rusticus), a species in which males have enlarged claws (chelae). We found that females had wider abdomens and longer uropods (terminal appendage of the tail fan) than males, while males possessed deeper abdomens and larger chelae, relative to total length. Chelae size was negatively associated with escape velocity, whereas longer abdomens and uropods were positively associated with escape velocity. We found no sex-specific differences in maximum force generated during the tail flip, but uropod length was strongly, positively correlated with tail-flip force in males. Particle image velocimetry (PIV) revealed that the formation of a vortex, rather than the expulsion of fluid between two closing body surfaces, generates propulsion in rusty crayfish. PIV also revealed that the pleopods (ventral abdominal appendages) contribute to the momentum generated by the tail. To our knowledge, this is the first confirmation of vortex formation in a decapod crustacean.

Knowing when to stick: touch receptors found in the remora adhesive disc.

Remoras are fishes that piggyback onto larger marine fauna via an adhesive disc to increase locomotor efficiency, likelihood of finding mates and access to prey. Attaching rapidly to a large, fast-moving host is no easy task, and while research to date has focused on how the disc supports adhesion, no attention has been paid to how or if remoras are able to sense attachment. We identified push-rod-like mechanoreceptor complexes embedded in the soft lip of the remora adhesive disc that are known in other organisms to respond to touch and shear forces. This is, to our knowledge, the first time such mechanoreceptor complexes are described in fishes as they were only known previously in monotremes. The presence of push-rod-like mechanoreceptor complexes suggests not only that fishes may be able to sense their environment in ways not heretofore described but that specialized tactile mechanoreceptor complexes may be a more basal vertebrate feature than previously thought.

Bioinspired remora adhesive disc offers insight into evolution.

Remoras are a family of fishes that can attach to other swimming organisms via an adhesive disc evolved from dorsal fin elements. However, the factors driving the evolution of remora disc morphology are poorly understood. It is not possible to link selective pressure for attachment to a specific host surface because all known hosts evolved before remoras themselves. Fortunately, the fundamental physics of suction and friction are mechanically conserved. Therefore, a morphologically relevant bioinspired model can be used to examine performance of hypothetical evolutionary intermediates. Using a bioinspired remora disc, we experimentally investigated the performance of increased lamellar number on shear adhesion. Herein, we translated fundamental biological principles into engineering design rules and show that a passive model system can autonomously achieve adhesive forces measured in live remoras in any environment. Our experimental results show that an increase in lamellar number resulted in an increase in shear adhesive performance, supporting the phylogenetic trend observed in extant remoras. The greatest pull-off forces measured for our model were on surface roughness on the order of shark skin and exceeded those measured for live remoras attached to shark skin by almost 60%. Overall, relative to fossil remoras and their closest ancestor, extant remoras exhibit a morphology indicative of selection for enhanced shear adhesive performance.

Channeling vorticity: modeling the filter-feeding mechanism in silver carp using µCT and 3D PIV.

Invasive silver carp are thriving within eutrophic environments in the United States, in part because of their highly efficient filter-feeding mechanism. Silver carp utilize modified gill rakers to capture a specific range of food; however, their greatly modified filtering morphology allows them to feed on phytoplankton and zooplankton ranging in size from 4 to 85 µm. The filtering apparatus of silver carp comprises rigid filtering plates where the outer anatomy of these plates is characterized by long parallel channels that change in orientation along the length of the plate. Here, we investigate the underlying morphology and concomitant hydrodynamics that support the filtration mechanisms of silver and bighead carp. Bighead carp are also invasive filter feeders, but their filtering apparatus is morphologically distinct from that of silver carp. Using 3D particle image velocimetry, we determined how particles and fluid interact with the surface of the gill rakers/plates. Filtering plates in silver carp induce strong directed vortical flow, whereas the filtering apparatus of bighead carp resulted in a type of haphazard cross-flow filtration. The organized vortical flow established by silver carp likely increased the number of interactions that the particle-filled water had with the filtering membrane. This strong vortical organization is maintained only at 0.75 body lengths s-1, and vortical flow is poorly developed and maintained at slower and faster speeds. Moreover, we found that absolute vorticity magnitude in silver carp is an order of magnitude greater than in bighead carp.

Author Correction: Remora cranial vein morphology and its functional implications for attachment.

A correction to this article has been published and is linked from the HTML version of this paper. The error has been fixed in the paper.

Remora cranial vein morphology and its functional implications for attachment.

Remora fishes adhere to, and maintain long-term, reversible attachment with, surfaces of varying roughness and compliance under wetted high-shear conditions using an adhesive disc that evolved from the dorsal fin spines typical of other fishes. Evolution of this complex hierarchical structure required extensive reorganization of the skull and fin spines, but the functional role of the soft tissues of the disc are poorly understood. Here I show that remora cranial veins are highly-modified in comparison to those of other vertebrates; they are transposed anteriorly and enlarged, and lie directly ventral to the disc on the dorsum of the cranium. Ancestrally, these veins lie inside the neurocranium, in the dura ventral to the brain, and return blood from the eyes, nares, and brain to the heart. Repositioning of these vessels to lie in contact with the ventral surface of the disc lamellae implies functional importance associated with the adhesive mechanism. The position of the anterior cardinal sinus suggests that it may aid in pressurization equilibrium during attachment by acting as a hydraulic differential.

Development of a vortex generator to perturb fish locomotion.

Knowledge about the stiffness of fish fins, and whether stiffness is modulated during swimming, is important for understanding the mechanics of a fin's force production. However, the mechanical properties of fins have not been studied during natural swimming, in part because of a lack of instrumentation. To remedy this, a vortex generator was developed that produces traveling vortices of adjustable strength which can be used to perturb the fins of swimming fish. Experiments were conducted to understand how the generator's settings affected the resulting vortex rings. A variety of vortices (14-32 mm diameter traveling at 371-2155 mm s-1) were produced that elicited adequate responses from the fish fins to help us to understand the fin's mechanical properties at various swimming speeds (0-350 mm s-1).

Theoretical and computational fluid dynamics of an attached remora (Echeneis naucrates).

Remora fishes have a unique dorsal suction pad that allows them to form robust, reliable, and reversible attachment to a wide variety of host organisms and marine vessels. Although investigations of the suction pad have been performed, the primary force that remoras must resist, namely fluid drag, has received little attention. This work provides a theoretical estimate of the drag experienced by an attached remora using computational fluid dynamics informed by geometry obtained from micro-computed tomography. Here, simulated flows are compared to measured flow fields of a euthanized specimen in a flow tank. Additionally, the influence of the host's boundary layer is investigated, and scaling relationships between remora features are inferred from the digitized geometry. The results suggest the drag on an attached remora is similar to that of a streamlined body, and is minimally influenced by the host's viscous boundary layer. Consequently, this evidence does not support the hypothesis that remoras discriminate between attachment locations based on hydrodynamic considerations. Comparison of the simulated drag with experimental friction tests show that even at elevated swimming speeds it is unlikely that remoras are dislodged by drag alone, and furthermore that larger remoras may be more difficult to dislodge than smaller remoras indicating that they become more suited to attachment as they mature.

Functional morphology and hydrodynamics of backward swimming in bluegill sunfish, Lepomis macrochirus.

Most teleost fishes, like the bluegill sunfish Lepomis macrochirus, have multiple flexible fins that are used as modifiable control surfaces. This helps to make fish highly maneuverable, permitting behaviors like reversing direction of motion and swimming backwards without having to rotate body position. To answer the question of how fish swim backwards we used high-speed videography and electromyography to determine the kinematics and muscle activity necessary to produce reverse-direction propulsion in four bluegill sunfish. We found that, in contrast to slow forward swimming, low-speed backward swimming is a multi-fin behavior, utilizing the pectoral, dorsal, anal, and caudal fins. The pectoral fins alternate beats, each fin broadly flaring on the outstroke and feathered on the instroke. The dorsal fin and dorsal portion of the caudal fin move out of phase as do the anal fin and ventral portion of the caudal fin. Electromyography of muscles in the pectoral, dorsal, anal, and caudal fins demonstrated bilateral activation when these fins changed direction, suggesting that fins are stiffened at this time. In addition to backward propulsion by the pectoral fins, particle image velocimetry revealed that the dorsal and anal fins are capable of producing reverse momentum jets to propel the fish backward. Because teleost fishes are statically unstable, locomotion at slow speeds requires precise fin control to adequately balance torques produced about the center of mass. Therefore, the kinematics of backward swimming may be the result of compensation for rolling, pitching, and yawning instability. We suggest that asymmetric pectoral fin activity with feathering during adduction balances rolling instability. The ventral to dorsal undulatory wave on the caudal fin controls pitch instability and yaw instability encountered from pectoral-driven backward locomotion. Thrust generation from the dorsal and anal fins decreases the destabilizing effect of the long moment arm of the tail in backward swimming. Thus, backward locomotion at slow speed is not simply the reverse of slow forward swimming.

Tetrapod-like pelvic girdle in a walking cavefish.

Fishes have adapted a number of different behaviors to move out of the water, but none have been described as being able to walk on land with a tetrapod-like gait. Here we show that the blind cavefish Cryptotora thamicola walks and climbs waterfalls with a salamander-like diagonal-couplets lateral sequence gait and has evolved a robust pelvic girdle that shares morphological features associated with terrestrial vertebrates. In all other fishes, the pelvic bones are suspended in a muscular sling or loosely attached to the pectoral girdle anteriorly. In contrast, the pelvic girdle of Cryptotora is a large, broad puboischiadic plate that is joined to the iliac process of a hypertrophied sacral rib; fusion of these bones in tetrapods creates an acetabulum. The vertebral column in the sacral area has large anterior and posterior zygapophyses, transverse processes, and broad neural spines, all of which are associated with terrestrial organisms. The diagonal-couplet lateral sequence gait was accomplished by rotation of the pectoral and pelvic girdles creating a standing wave of the axial body. These findings are significant because they represent the first example of behavioural and morphological adaptation in an extant fish that converges on the tetrapodal walking behaviour and morphology.

Remora fish suction pad attachment is enhanced by spinule friction.

The remora fishes are capable of adhering to a wide variety of natural and artificial marine substrates using a dorsal suction pad. The pad is made of serial parallel pectinated lamellae, which are homologous to the dorsal fin elements of other fishes. Small tooth-like projections of mineralized tissue from the dorsal pad lamella, known as spinules, are thought to increase the remora's resistance to slippage and thereby enhance friction to maintain attachment to a moving host. In this work, the geometry of the spinules and host topology as determined by micro-computed tomography and confocal microscope data, respectively, are combined in a friction model to estimate the spinule contribution to shear resistance. Model results are validated with natural and artificially created spinules and compared with previous remora pull-off experiments. It was found that spinule geometry plays an essential role in friction enhancement, especially at short spatial wavelengths in the host surface, and that spinule tip geometry is not correlated with lamellar position. Furthermore, comparisons with pull-off experiments suggest that spinules are primarily responsible for friction enhancement on rough host topologies such as shark skin.

Locomotion of free-swimming ghost knifefish: anal fin kinematics during four behaviors.

The maneuverability demonstrated by the weakly electric ghost knifefish (Apteronotus albifrons) is a result of its highly flexible ribbon-like anal fin, which extends nearly three-quarters the length of its body and is composed of approximately 150 individual fin rays. To understand how movement of the anal fin controls locomotion we examined kinematics of the whole fin, as well as selected individual fin rays, during four locomotor behaviors executed by free-swimming ghost knifefish: forward swimming, backward swimming, heave (vertical) motion, and hovering. We used high-speed video (1000 fps) to examine the motion of the entire anal fin and we measured the three-dimensional curvature of four adjacent fin rays in the middle of the fin during each behavior to determine how individual fin rays bend along their length during swimming. Canonical discriminant analysis separated all four behaviors on anal fin kinematic variables and showed that forward and backward swimming behaviors contrasted the most: forward behaviors exhibited a large anterior wavelength and posterior amplitude while during backward locomotion the anal fin exhibited both a large posterior wavelength and anterior amplitude. Heave and hover behaviors were defined by similar kinematic variables; however, for each variable, the mean values for heave motions were generally greater than for hovering. Individual fin rays in the middle of the anal fin curved substantially along their length during swimming, and the magnitude of this curvature was nearly twice the previously measured maximum curvature for ray-finned fish fin rays during locomotion. Fin rays were often curved into the direction of motion, indicating active control of fin ray curvature, and not just passive bending in response to fluid loading.

Pectoral fins aid in navigation of a complex environment by bluegill sunfish under sensory deprivation conditions.

Complex structured environments offer fish advantages as places of refuge and areas of greater potential prey densities, but maneuvering through these environments is a navigational challenge. To successfully navigate complex habitats, fish must have sensory input relaying information about the proximity and size of obstacles. We investigated the role of the pectoral fins as mechanosensors in bluegill sunfish swimming through obstacle courses under different sensory deprivation and flow speed conditions. Sensory deprivation was accomplished by filming in the dark to remove visual input and/or temporarily blocking lateral line input via immersion in cobalt chloride. Fish used their pectoral fins to touch obstacles as they swam slowly past them under all conditions. Loss of visual and/or lateral line sensory input resulted in an increased number of fin taps and shorter tap durations while traversing the course. Propulsive pectoral fin strokes were made in open areas between obstacle posts and fish did not use the pectoral fins to push off or change heading. Bending of the flexible pectoral fin rays may initiate an afferent sensory input, which could be an important part of the proprioceptive feedback system needed to navigate complex environments. This behavioral evidence suggests that it is possible for unspecialized pectoral fins to act in both a sensory and a propulsive capacity.