Mechanics of Undulatory Swimming in a Frictional Fluid

The sandfish lizard (Scincus scincus) swims within granular media (sand) using axial body undulations to propel itself without the use of limbs. In previous work we predicted average swimming speed by developing a numerical simulation that incorporated experimentally measured biological kinematics into a multibody sandfish model. The model was coupled to an experimentally validated soft sphere discrete element method simulation of the granular medium. In this paper, we use the simulation to study the detailed mechanics of undulatory swimming in a “granular frictional fluid” and compare the predictions to our previously developed resistive force theory (RFT) which models sand-swimming using empirically determined granular drag laws. The simulation reveals that the forward speed of the center of mass (CoM) oscillates about its average speed in antiphase with head drag. The coupling between overall body motion and body deformation results in a non-trivial pattern in the magnitude of lateral displacement of the segments along the body. The actuator torque and segment power are maximal near the center of the body and decrease to zero toward the head and the tail. Approximately 30% of the net swimming power is dissipated in head drag. The power consumption is proportional to the frequency in the biologically relevant range, which confirms that frictional forces dominate during sand-swimming by the sandfish. Comparison of the segmental forces measured in simulation with the force on a laterally oscillating rod reveals that a granular hysteresis effect causes the overestimation of the body thrust forces in the RFT. Our models provide detailed testable predictions for biological locomotion in a granular environment.     

On-line Optimization of Biomimetic Undulatory Swimming by an Experiment-based Approach

An experiment-based approach is proposed to improve the performance of biomimetic undulatory locomotion through on-line optimization. The approach is implemented through two steps： （1） the generation of coordinated swimming gaits by artificial Central Pattern Generators （CPGs）; （2） an on-line searching of optimal parameter sets for the CPG model using Genetic Algorithm （GA）. The effectiveness of the approach is demonstrated in the optimization of swimming speed and energy effi- ciency for a biomimetic fin propulsor. To evaluate how well the input energy is converted into the kinetic energy of the pro- pulsor, an energy-efficiency index is presented and utilized as a feedback to regulate the on-line searching with a closed-loop swimming control. Experiments were conducted on propulsor prototypes with different fin segments and the optimal swimming patterns were found separately. Comparisons of results show that the optimal curvature of undulatory propulsor, which might have different shapes depending on the actual prototype design and control scheme. It is also found that the propulsor with six fin segments, is preferable because of hizher speed and lower energy efficiency.     

Near Surface Swimming of Salmonella Typhimurium Explains Target-Site Selection and Cooperative Invasion

Targeting of permissive entry sites is crucial for bacterial infection. The targeting mechanisms are incompletely understood. We have analyzed target-site selection by S. Typhimurium. This enteropathogenic bacterium employs adhesins (e.g. fim) and the type III secretion system 1 (TTSS-1) for host cell binding, the triggering of ruffles and invasion. Typically, S. Typhimurium invasion is focused on a subset of cells and multiple bacteria invade via the same ruffle. It has remained unclear how this is achieved. We have studied target-site selection in tissue culture by time lapse microscopy, movement pattern analysis and modeling. Flagellar motility (but not chemotaxis) was required for reaching the host cell surface in vitro. Subsequently, physical forces trapped the pathogen for ∼1.5–3 s in “near surface swimming”. This increased the local pathogen density and facilitated “scanning” of the host surface topology. We observed transient TTSS-1 and fim-independent “stopping” and irreversible TTSS-1-mediated docking, in particular at sites of prominent topology, i.e. the base of rounded-up cells and membrane ruffles. Our data indicate that target site selection and the cooperative infection of membrane ruffles are attributable to near surface swimming. This mechanism might be of general importance for understanding infection by flagellated bacteria.     

Optimal shape and motion of undulatory swimming organisms

Undulatory swimming animals exhibit diverse ranges of body shapes and motion patterns and are often considered as having superior locomotory performance. The extent to which morphological traits of swimming animals have evolved owing to primarily locomotion considerations is, however, not clear. To shed some light on that question, we present here the optimal shape and motion of undulatory swimming organisms obtained by optimizing locomotive performance measures within the framework of a combined hydrodynamical, structural and novel muscular model. We develop a muscular model for periodic muscle contraction which provides relevant kinematic and energetic quantities required to describe swimming. Using an evolutionary algorithm, we performed a multi-objective optimization for achieving maximum sustained swimming speed U and minimum cost of transport (COT)--two conflicting locomotive performance measures that have been conjectured as likely to increase fitness for survival. Starting from an initial population of random characteristics, our results show that, for a range of size scales, fish-like body shapes and motion indeed emerge when U and COT are optimized. Inherent boundary-layer-dependent allometric scaling between body mass and kinematic and energetic quantities of the optimal populations is observed. The trade-off between U and COT affects the geometry, kinematics and energetics of swimming organisms. Our results are corroborated by empirical data from swimming animals over nine orders of magnitude in size, supporting the notion that optimizing U and COT could be the driving force of evolution in many species.     

From decision to action: Detailed modelling of frog tadpoles reveals neuronal mechanisms of decision-making and reproduces unpredictable swimming movements in response to sensory signals

How does the brain process sensory stimuli, and decide whether to initiate locomotor behaviour? To investigate this question we develop two whole body computer models of a tadpole. The “Central Nervous System” (CNS) model uses evidence from whole-cell recording to define 2300 neurons in 12 classes to study how sensory signals from the skin initiate and stop swimming. In response to skin stimulation, it generates realistic sensory pathway spiking and shows how hindbrain sensory memory populations on each side can compete to initiate reticulospinal neuron firing and start swimming. The 3-D “Virtual Tadpole” (VT) biomechanical model with realistic muscle innervation, body flexion, body-water interaction, and movement is then used to evaluate if motor nerve outputs from the CNS model can produce swimming-like movements in a volume of “water”. We find that the whole tadpole VT model generates reliable and realistic swimming. Combining these two models opens new perspectives for experiments.     

Resolving Shifting Patterns of Muscle Energy Use in Swimming Fish

Muscle metabolism dominates the energy costs of locomotion. Although in vivo measures of muscle strain, activity and force can indicate mechanical function, similar muscle-level measures of energy use are challenging to obtain. Without this information locomotor systems are essentially a black box in terms of the distribution of metabolic energy. Although in situ measurements of muscle metabolism are not practical in multiple muscles, the rate of blood flow to skeletal muscle tissue can be used as a proxy for aerobic metabolism, allowing the cost of particular muscle functions to be estimated. Axial, undulatory swimming is one of the most common modes of vertebrate locomotion. In fish, segmented myotomal muscles are the primary power source, driving undulations of the body axis that transfer momentum to the water. Multiple fins and the associated fin muscles also contribute to thrust production, and stabilization and control of the swimming trajectory. We have used blood flow tracers in swimming rainbow trout (Oncorhynchus mykiss) to estimate the regional distribution of energy use across the myotomal and fin muscle groups to reveal the functional distribution of metabolic energy use within a swimming animal for the first time. Energy use by the myotomal muscle increased with speed to meet thrust requirements, particularly in posterior myotomes where muscle power outputs are greatest. At low speeds, there was high fin muscle energy use, consistent with active stability control. As speed increased, and fins were adducted, overall fin muscle energy use declined, except in the caudal fin muscles where active fin stiffening is required to maintain power transfer to the wake. The present data were obtained under steady-state conditions which rarely apply in natural, physical environments. This approach also has potential to reveal the mechanical factors that underlie changes in locomotor cost associated with movement through unsteady flow regimes.     

Myotonia Congenita-Associated Mutations in Chloride Channel-1 Affect Zebrafish Body Wave Swimming Kinematics

Myotonia congenita is a human muscle disorder caused by mutations in CLCN1, which encodes human chloride channel 1 (CLCN1). Zebrafish is becoming an increasingly useful model for human diseases, including muscle disorders. In this study, we generated transgenic zebrafish expressing, under the control of a muscle specific promoter, human CLCN1 carrying mutations that have been identified in human patients suffering from myotonia congenita. We developed video analytic tools that are able to provide precise quantitative measurements of movement abnormalities in order to analyse the effect of these CLCN1 mutations on adult transgenic zebrafish swimming. Two new parameters for body-wave kinematics of swimming reveal changes in body curvature and tail offset in transgenic zebrafish expressing the disease-associated CLCN1 mutants, presumably due to their effect on muscle function. The capability of the developed video analytic tool to distinguish wild-type from transgenic zebrafish could provide a useful asset to screen for compounds that reverse the disease phenotype, and may be applicable to other movement disorders besides myotonia congenita.     

Muscle Dynamics in Fish During Steady Swimming

SYNOPSIS. Recent research in fish locomotion has been dominatedby an interest in the dynamic mechanical properties of the swimmingmusculature. Prior observations have indicated that waves ofmuscle activation travel along the body of an undulating fishfaster than the resulting waves of muscular contraction, suggestingthat the phase relation between the muscle strain cycle andits activation must vary along the body. Since this phase relationis critical in determining how the muscle performs in cycliccontractions, the possibility has emerged that dynamic musclefunction may change with axial position in swimming fish. Quantificationof muscle contractile properties in cyclic contractions relieson in vitro experiments using strain and activation data collectedin vivo. In this paper we discuss the relation between theseparameters and body kinematics. Using videoradiographic datafrom swimming mackerel we demonstrate that red muscle straincan be accurately predicted from midline curvature but not fromlateral displacement. Electromyographic recordings show neuronalactivation patterns that are consistent with red muscle performingnet positive work at all axial positions. The relatively constantcross-section of red muscle along much of the body suggeststhat positive power for swimming is generated fairly uniformlyalong the length of the fish.     

The Roles of Pink and Red Muscle in Powering Steady Swimming in Scup, Stenotomus chrysops

Fishes power steady, undulatory swimming using both red andpink muscle. In this study we examined the roles of the twofiber types in generating power for swimming by using two-steptechnique. First, in vivo data is collected from swimming fish,and second, the electrical activity and muscle length changeconditions recorded in vivo are recreated in vitro with isolatedmuscle bundles. Force production and power generation by muscleduring swimming can then be estimated. In scup, both red andpink muscle are recruited to power swimming at the maximum sustainedswimming speed. For both fiber types, the duration of electricalactivity decreases from anterior to posterior. However, theamplitude of muscle length change increases anterior to posterior.Mass-specific power production increases posteriorly for bothmuscle types. The faster contraction kinetics of pink muscletranslate to higher power production pink muscle relative tored muscle for all longitudinal positions of the fish. Determinationof absolute power production, based on mass-specific power andmuscle mass, shows that the posterior regions of the fish generatethe most power for swimming. At 20°C, red muscle generatesmore absolute power than pink due to its higher muscle mass.However, at 10°C, pink muscle generates more absolute powerthan red, because red muscle produces little or no positivepower for all longitudinal positions.     

Swimming patterns of the quadriflagellate Tetraflagellochloris mauritanica (Chlamydomonadales,Chlorophyceae)

Chlamydomonadales are elective subjects for the investigation of the problems related to locomotion and transport in biological fluid dynamics, whose resolution could enhance searching efficiency and assist in the avoidance of dangerous environments. In this paper, we elucidate the swimming behavior of Tetraflagellochloris mauritanica, a unicellular–multicellular alga belonging to the order Chlamydomonadales. This quadriflagellate alga has a complex swimming motion consisting of alternating swimming phases connected by in‐place random reorientations and resting phases. It is capable of both forward and backward swimming, both being normal modes of swimming. The complex swimming behavior resembles the run‐and‐tumble motion of peritrichous bacteria, with in‐place reorientation taking the place of tumbles. In the forward swimming, T. mauritanica shows a very efficient flagellar beat, with undulatory retrograde waves that run along the flagella to their tip. In the backward swimming, the flagella show a nonstereotypical synchronization mode, with a pattern that does not fit any of the modes present in the other Chlamydomonadales so far investigated.     

Mechanical properties of a bio-inspired robotic knifefish with an undulatory propulsor

South American electric knifefish are a leading model system within neurobiology. Recent efforts have focused on understanding their biomechanics and relating this to their neural processing strategies. Knifefish swim by means of an undulatory fin that runs most of the length of their body, affixed to the belly. Propelling themselves with this fin enables them to keep their body relatively straight while swimming, enabling straightforward robotic implementation with a rigid hull. In this study, we examined the basic properties of undulatory swimming through use of a robot that was similar in some key respects to the knifefish. As we varied critical fin kinematic variables such as frequency, amplitude, and wavelength of sinusoidal traveling waves, we measured the force generated by the robot when it swam against a stationary sensor, and its velocity while swimming freely within a flow tunnel system. Our results show that there is an optimal operational region in the fin's kinematic parameter space. The optimal actuation parameters found for the robotic knifefish are similar to previously observed parameters for the black ghost knifefish, Apteronotus albifrons. Finally, we used our experimental results to show how the force generated by the robotic fin can be decomposed into thrust and drag terms. Our findings are useful for future bio-inspired underwater vehicles as well as for understanding the mechanics of knifefish swimming.     

Evolution of root nodule symbiosis: Focusing on the transcriptional regulation from the genomic point of view

Since molecular phylogenetics recognized root nodule symbiosis (RNS) of all lineages as potentially homologous, scientists have tried to understand the “when” and the “how” of RNS evolution. Initial progress was made on understanding the timing of RNS evolution, facilitating our progress on understanding the underlying genomic changes leading to RNS. Here, we will first cover the different hypotheses on the timings of gains/losses of RNS and show how this has helped us understand how RNS has evolved. Finally, we will discuss how our improved understanding of the genetic changes that led to RNS is now helping us refine our understanding on when RNS has evolved.     

Direct Mapping from Intracellular Chemotaxis Signaling to Single-Cell Swimming Behavior

Bacterial chemotaxis allows bacteria to sense the chemical environment and modulate their swimming behavior accordingly. Although the intracellular chemotaxis signaling pathway has been studied extensively, experimental studies are still lacking that could provide direct link from the pathway output (the intracellular concentration of the phosphorylated form of the response regulator phosphorylated CheY (CheY-P)) to single-cell swimming behavior. Here, we measured the swimming behavior of individual Escherichia coli cells while simultaneously detecting the intracellular CheY-P concentration, thereby providing a direct relationship between the intracellular CheY-P concentration and the single-cell run-and-tumble behavior. The measured relationship is consistent with the ultrasensitivity of the motor switch and a “veto model” that describes the interaction among individual flagella, although contribution from the voting mechanism could not be ruled out.     

The Effect of Drag and Attachment Site of External Tags on Swimming Eels: Experimental Quantification and Evaluation Tool

Telemetry studies on aquatic animals often use external tags to monitor migration patterns and help to inform conservation effort. However, external tags are known to impair swimming energetics dramatically in a variety of species, including the endangered European eel. Due to their high swimming efficiency, anguilliform swimmers are very susceptibility for added drag. Using an integration of swimming physiology, behaviour and kinematics, we investigated the effect of additional drag and site of externally attached tags on swimming mode and costs. The results show a significant effect of a) attachment site and b) drag on multiple energetic parameters, such as Cost Of Transport (COT), critical swimming speed (U_crit) and optimal swimming speed (U_opt), possibly due to changes in swimming kinematics. Attachment at 0.125 bl from the tip of the snout is a better choice than at the Centre Of Mass (0.35 bl), as it is the case in current telemetry studies. Quantification of added drag effect on COT and U_crit show a (limited) correlation, suggesting that the U_crit test can be used for evaluating external tags for telemetry studies until a certain threshold value. U_opt is not affected by added drag, validating previous findings of telemetry studies. The integrative methodology and the evaluation tool presented here can be used for the design of new studies using external telemetry tags, and the (re-) evaluation of relevant studies on anguilliform swimmers.     

Swimming speed, respiration rate, and estimated cost of transport in adult killer whales

The physiology of free-ranging cetaceans is difficult to study and as a consequence, data on the energetics of these animals are limited. To better understand the energetic cost of swimming in killer whales, total cost of transport ( COT ) was estimated from swimming speeds and respiration rates from wild adult northern resident killer whales ( Orcinus orca ) and reported values of oxygen consumption in captive whales. Respiration rate (breaths per minute) was positively correlated with swimming speed (meters per second), while mass-specific COT (Joules per kilogram per meter) decreased with speed. Lack of data on very fast-swimming animals hindered assessment of the exact speed at which COT was minimal. However, minimum mass-specific COT for killer whales in the present study approached those predicted by a previously published allometric equation for marine mammals, and corresponded to "optimal" swimming speeds of 2.6–3 m/s. Interestingly, the observed average swimming speed (1.6 m/s) was lower than predicted optimal swimming speed. Finally, females with dependent calves had higher respiration rates than females without calves. These findings could be due to synchronous breathing with calves or could result from increased costs of lactation and swimming with a calf in echelon formation. Consequently, females with calves may have much greater COT at optimal swimming speeds than females without calves.     

Lungfish Axial Muscle Function and the Vertebrate Water to Land Transition

The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates. The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics. Lungfish are an ideal group to study the role of axial function in terrestrial locomotion as they are the sister taxon to tetrapods and regularly move on land. Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty. We compared terrestrial lungfish data to data from lungfish swimming in different viscosities as well as to salamander locomotion. The terrestrial locomotion of lungfish involved substantial activity in the trunk muscles but almost no tail activity. Unlike other elongate vertebrates, lungfish moved on land with a standing wave pattern of axial muscle activity that closely resembled the pattern observed in terrestrially locomoting salamanders. The similarity in axial motor pattern in salamanders and lungfish suggests that some aspects of neuromuscular control for the axial movements involved in terrestrial locomotion were present before derived appendicular structures.     

Locomotion of Gymnarchus Niloticus： Experiment and Kinematics

In addition to forward undulatory swimming, Gymnarchus niloticus can swim via undulations of the dorsal fin while the body axis remains straight; furthermore, it swims forward and backward in a similar way, which indicates that the undulation of the dorsal fin can simultaneously provide bidirectional propulsive and maneuvering forces with the help of the tail fin. A high-resolution Charge-Coupled Device （CCD） imaging camera system is used to record kinematics of steady swimming as well as maneuvering in G. niloticus. Based on experimental data, this paper discusses the kinematics （cruising speed, wave speed, cycle frequency, amplitude, lateral displacement） of forward as well as backward swimming and maneuvering. During forward swimming, the propulsive force is generated mainly by undulations of the dorsal fin while the body axis remains straight. The kinematic parameters （wave speed, wavelength, cycle frequency, amplitude） have statistically significant correlations with cruising speed. In addition, the yaw at the head is minimal during steady swimming. From experimental data, the maximal lateral displacement of head is not more than 1% of the body length, while the maximal lateral displacement of the whole body is not more than 5% of the body length. Another important feature is that G. niloticus swims backwards using an undulatory mechanism that resembles the forward undulatory swimming mechanism. In backward swimming, the increase of lateral displacement of the head is comparatively significant; the amplitude profiles of the propulsive wave along the dorsal fin are significantly different from those in forward swimming. When G. niloticus does fast maneuvering, its body is first bent into either a C shape or an S shape, then it is rapidly unwound in a travelling wave fashion. It rarely maneuvers without the help of the tail fin and body bending.     

Fibrous Flagellar Hairs of Chlamydomonas reinhardtii Do Not Enhance Swimming

The flagella of Chlamydomonas reinhardtii possess fibrous ultrastructures of a nanometer-scale thickness known as mastigonemes. These structures have been widely hypothesized to enhance flagellar thrust; however, detailed hydrodynamic analysis supporting this claim is lacking. In this study, we present a comprehensive investigation into the hydrodynamic effects of mastigonemes using a genetically modified mutant lacking the fibrous structures. Through high-speed observations of freely swimming cells, we found the average and maximum swimming speeds to be unaffected by the presence of mastigonemes. In addition to swimming speeds, no significant difference was found for flagellar gait kinematics. After our observations of swimming kinematics, we present direct measurements of the hydrodynamic forces generated by flagella with and without mastigonemes. These measurements were conducted using optical tweezers, which enabled high temporal and spatial resolution of hydrodynamic forces. Through our measurements, we found no significant difference in propulsive flows due to the presence of mastigonemes. Direct comparison between measurements and fluid mechanical modeling revealed that swimming hydrodynamics were accurately captured without including mastigonemes on the modeled swimmer’s flagella. Therefore, mastigonemes do not appear to increase the flagella’s effective area while swimming, as previously thought. Our results refute the longstanding claim that mastigonemes enhance flagellar thrust in C. reinhardtii, and so, their function still remains enigmatic.     

Center of mass motion in swimming fish: effects of speed and locomotor mode during undulatory propulsion

Studies of center of mass (COM) motion are fundamental to understanding the dynamics of animal movement, and have been carried out extensively for terrestrial and aerial locomotion. But despite a large amount of literature describing different body movement patterns in fishes, analyses of how the center of mass moves during undulatory propulsion are not available. These data would be valuable for understanding the dynamics of different body movement patterns and the effect of differing body shapes on locomotor force production. In the present study, we analyzed the magnitude and frequency components of COM motion in three dimensions (x: surge, y: sway, z: heave) in three fish species (eel, bluegill sunfish, and clown knifefish) swimming with four locomotor modes at three speeds using high-speed video, and used an image cross-correlation technique to estimate COM motion, thus enabling untethered and unrestrained locomotion. Anguilliform swimming by eels shows reduced COM surge oscillation magnitude relative to carangiform swimming, but not compared to knifefish using a gymnotiform locomotor style. Labriform swimming (bluegill at 0.5 body lengths/s) displays reduced COM sway oscillation relative to swimming in a carangiform style at higher speeds. Oscillation frequency of the COM in the surge direction occurs at twice the tail beat frequency for carangiform and anguilliform swimming, but at the same frequency as the tail beat for gymnotiform locomotion in clown knifefish. Scaling analysis of COM heave oscillation for terrestrial locomotion suggests that COM heave motion scales with positive allometry, and that fish have relatively low COM oscillations for their body size.     

Roles of leader and follower cells in collective cell migration

Collective cell migration is a widely observed phenomenon during animal development, tissue repair, and cancer metastasis. Considering its broad involvement in biological processes, it is essential to understand the basics behind the collective movement. Based on the topology of migrating populations, tissue-scale kinetics, called the “leader–follower” model, has been proposed for persistent directional collective movement. Extensive in vivo and in vitro studies reveal the characteristics of leader cells, as well as the special mechanisms leader cells employ for maintaining their positions in collective migration. However, follower cells have attracted increasing attention recently due to their important contributions to collective movement. In this Perspective, the current understanding of the molecular mechanisms behind the “leader–follower” model is reviewed with a special focus on the force transmission and diverse roles of leaders and followers during collective cell movement.