Caenorhabditis elegans transfers across a gap under an electric field as dispersal behavior.

Interactions between different animal species are a critical determinant of each species' evolution and range expansion. Chemical, visual, and mechanical interactions have been abundantly reported, but the importance of electric interactions is not well understood. Here, we report the discovery that the nematode Caenorhabditis elegans transfers across electric fields to achieve phoretic attachment to insects. First, we found that dauer larvae of C. elegans nictating on a substrate in a Petri dish moved directly to the lid through the air due to the electrostatic force from the lid. To more systematically investigate the transfer behavior, we constructed an assay system with well-controlled electric fields: the worms flew up regardless of whether a positive or negative electric field was applied, suggesting that an induced charge within the worm is related to this transfer. The mean take-off speed is 0.86 m/s, and the worm flies up under an electric field exceeding 200 kV/m. This worm transfer occurs even when the worms form a nictation column composed of up to 100 worms; we term this behavior "multiworm transfer." These observations led us to conclude that C. elegans can transfer and attach to the bumblebee Bombus terrestris, which was charged by rubbing with flower pollen in the lab. The charge on the bumblebee was measured with a coulomb-meter to be 806 pC, which was within the range of bumblebee charges and of the same order of flying insect charges observed in nature, suggesting that electrical interactions occur among different species.

Light-sheet microscopy reveals dorsoventral asymmetric membrane dynamics of Amoeba proteus during pressure-driven locomotion.

Amoebae are found all around the world and play an essential role in the carbon cycle in the environment. Therefore, the behavior of amoebae is a crucial factor when considering the global environment. Amoebae change their distribution through amoeboid locomotion, which are classified into several modes. In the pressure-driven mode, intracellular hydrostatic pressure generated by the contraction of cellular cortex actomyosin causes the pseudopod to extend. During amoeboid locomotion, the cellular surface exhibits dynamic deformation. Therefore, to understand the mechanism of amoeboid locomotion, it is important to characterize cellular membrane dynamics. Here, to clarify membrane dynamics during pressure-driven amoeboid locomotion, we developed a polkadot membrane staining method and performed light-sheet microscopy in Amoeba proteus, which exhibits typical pressure-driven amoeboid locomotion. It was observed that the whole cell membrane moved in the direction of movement, and the dorsal cell membrane in the posterior part of the cell moved more slowly than the other membrane. In addition, membrane complexity varied depending on the focused characteristic size of the membrane structure, and in general, the dorsal side was more complex than the ventral side. In summary, the membrane dynamics of Amoeba proteus during pressure-driven locomotion are asymmetric between the dorsal and ventral sides. This article has an associated interview with the co-first authors of the paper.

Switching of behavioral modes and their modulation by a geometrical cue in the ciliate Stentor coeruleus.

Protists ubiquitously live in nature and play key roles in the food web chain. Their habitats consist of various geometrical structures, such as porous media and rigid surfaces, affecting their motilities. A kind of protist, Stentor coeruleus, exhibits free swimming and adhering for feeding. Under environmental and culture conditions, these organisms are often found in sediments with complex geometries. The determination of anchoring location is essential for their lives. However, the factors that induce the behavioral transition from swimming to adhering are still unknown. In this study, we quantitatively characterized the behavioral transitions in S. coeruleus and observed the behavior in a chamber with dead ends made by a simple structure mimicking the environmental structures. As a result, the cell adheres and feeds in narrow spaces between the structure and the chamber wall. It may be reasonable for the organism to hide itself from predators and capture prey in these spaces. The behavioral strategy for the exploration and exploitation of spaces with a wide variety of geometries in their habitats is discussed.

A model for simulating emergent patterns of cities and roads on real-world landscapes.

Emergence of cities and road networks have characterised human activity and movement over millennia. However, this anthropogenic infrastructure does not develop in isolation, but is deeply embedded in the natural landscape, which strongly influences the resultant spatial patterns. Nevertheless, the precise impact that landscape has on the location, size and connectivity of cities is a long-standing, unresolved problem. To address this issue, we incorporate high-resolution topographic maps into a Turing-like pattern forming system, in which local reinforcement rules result in co-evolving centres of population and transport networks. Using Italy as a case study, we show that the model constrained solely by topography results in an emergent spatial pattern that is consistent with Zipf's Law and comparable to the census data. Thus, we infer the natural landscape may play a dominant role in establishing the baseline macro-scale population pattern, that is then modified by higher-level historical, socio-economic or cultural factors.

Gait switching with phase reversal of locomotory waves in the centipedeScolopocryptops rubiginosus.

Crawling using locomotory waves is a common method of locomotion for limbless and many-legged invertebrates and stimulates the biomimetic engineering of flexible locomotion. It is generally believed that the direction of locomotory waves is fixed for a given species. However, we found that a centipede,Scolopocryptops rubiginosus, flexibly generated its gait to allow for locomotory waves that varied in direction, depending on (i) locomotion speed and (ii) the physical conditions of terrain. We also found a new type of centipede's swimming gait unlike eel-like way known so far which is using posteriorly traveling waves of horizontal body undulation. The gait patterns of the centipede were examined in various conditions and analyzed how the waves switched in detailed. We showed that gait patterns were associated with control of stride length rather than stride frequency. Discussion was made on a possible scenario of the gait transition in the centipede compatible with our observations. This finding may give a hint at bio-inspired control of flexible gait switching in response to irregular terrain.

Dynamic Control of Microbial Movement by Photoswitchable ATP Antagonists.

Adenosine triphosphate (ATP) is the energy source for various biochemical processes and biomolecular motors in living things. Development of ATP antagonists and their stimuli-controlled actions offer a novel approach to regulate biological processes. Herein, we developed azobenzene-based photoswitchable ATP antagonists for controlling the activity of motor proteins; cytoplasmic and axonemal dyneins. The new ATP antagonists showed reversible photoswitching of cytoplasmic dynein activity in an in vitro dynein-microtubule system due to the trans and cis photoisomerization of their azobenzene segment. Importantly, our ATP antagonists reversibly regulated the axonemal dynein motor activity for the force generation in a demembranated model of Chlamydomonas reinhardtii. We found that the trans and cis isomers of ATP antagonists significantly differ in their affinity to the ATP binding site.

Binocular stereo-microscopy for deforming intact amoeba.

A powerful and convenient method for measuring three-dimensional (3D) deformation of moving amoeboid cells will assist the progress of environmental and cytological studies as protists amoebae play a role in the fundamental environmental ecosystem. Here we develop an inexpensive and useful method for measuring 3D deformation of single protists amoeba through binocular microscopy and a newly proposed algorithm of stereo-scopy. From the movies taken from the left and right optical tubes of the binocular microscope, we detect the 3D positions of many intrinsic intracellular vesicles and reconstruct cellular surfaces of amoeboid cells in 3D space. Some observations of sampled behaviors are shown in a single-celled organism of Amoeba proteus. The resultant surface time series is then analyzed to obtain surface velocity, curvature and volume increasing rates of pseudo-pods for characterizing the movements of amoeboid cells. The limitations and errors of this method are also discussed.

Uni-cellular integration of complex spatial information in slime moulds and ciliates.

Single-celled organisms show a fascinating faculty for integrating spatial information and adapting their behaviour accordingly. As such they are of potential interest for elucidating fundamental mechanisms of developmental biology. In this mini-review we highlight current research on two organisms, the true slime mould Physarum polycephalum and the ciliates Paramecium and Tetrahymena. For each of these, we present a case study how applying physical principles to explain behaviour can lead to the understanding of general principles possibly relevant to developmental biology.

Physarum inspires research beyond biomimetic algorithms: Reply to comments on "Does being multi-headed make you better at solving problems?"

We look at a recent expansion of Physarum research from inspiring biomimetic algorithms to serving as a model organism in the evolutionary study of perception, memory, learning, and decision making.

Does being multi-headed make you better at solving problems? A survey of Physarum-based models and computations.

Physarum polycephalum, a single-celled, multinucleate slime mould, is a seemingly simple organism, yet it exhibits quasi-intelligent behaviour during extension, foraging, and as it adapts to dynamic environments. For these reasons, Physarum is an attractive target for modelling with the underlying goal to uncover the physiological mechanisms behind the exhibited quasi-intelligence and/or to devise novel algorithms for solving complex computational problems. The recent increase in modelling studies on Physarum has prompted us to review the latest developments in this field in the context of modelling and computing alike. Specifically, we cover models based on (i) morphology, (ii) taxis, and (iii) positive feedback dynamics found in top-down and bottom-up modelling techniques. We also survey the application of each of these core features of Physarum to solving difficult computational problems with real-world applications. Finally, we highlight some open problems in the field and present directions for future research.

Current reinforcement model reproduces center-in-center vein trajectory of Physarum polycephalum.

Vein networks span the whole body of the amoeboid organism in the plasmodial slime mould Physarum polycephalum, and the network topology is rearranged within an hour in response to spatio-temporal variations of the environment. It has been reported that this tube morphogenesis is capable of solving mazes, and a mathematical model, named the 'current reinforcement rule', was proposed based on the adaptability of the veins. Although it is known that this model works well for reproducing some key characters of the organism's maze-solving behaviour, one important issue is still open: In the real organism, the thick veins tend to trace the shortest possible route by cutting the corners at the turn of corridors, following a center-in-center trajectory, but it has not yet been examined whether this feature also appears in the mathematical model, using corridors of finite width. In this report, we confirm that the mathematical model reproduces the center-in-center trajectory of veins around corners observed in the maze-solving experiment.

The role of noise in self-organized decision making by the true slime mold Physarum polycephalum.

Self-organized mechanisms are frequently encountered in nature and known to achieve flexible, adaptive control and decision-making. Noise plays a crucial role in such systems: It can enable a self-organized system to reliably adapt to short-term changes in the environment while maintaining a generally stable behavior. This is fundamental in biological systems because they must strike a delicate balance between stable and flexible behavior. In the present paper we analyse the role of noise in the decision-making of the true slime mold Physarum polycephalum, an important model species for the investigation of computational abilities in simple organisms. We propose a simple biological experiment to investigate the reaction of P. polycephalum to time-variant risk factors and present a stochastic extension of an established mathematical model for P. polycephalum to analyze this experiment. It predicts that-due to the mechanism of stochastic resonance-noise can enable P. polycephalum to correctly assess time-variant risk factors, while the corresponding noise-free system fails to do so. Beyond the study of P. polycephalum we demonstrate that the influence of noise on self-organized decision-making is not tied to a specific organism. Rather it is a general property of the underlying process dynamics, which appears to be universal across a wide range of systems. Our study thus provides further evidence that stochastic resonance is a fundamental component of the decision-making in self-organized macroscopic and microscopic groups and organisms.

A ciliate memorizes the geometry of a swimming arena.

Previous studies on adaptive behaviour in single-celled organisms have given hints to the origin of their memorizing capacity. Here we report evidence that a protozoan ciliate Tetrahymena has the capacity to learn the shape and size of its swimming space. Cells confined in a small water droplet for a short period were found to recapitulate circular swimming trajectories upon release. The diameter of the circular trajectories and their duration reflected the size of the droplet and the period of confinement. We suggest a possible mechanism for this adaptive behaviour based on a Ca(2+) channel. In our model, repeated collisions with the walls of a confining droplet result in a slow rise in intracellular calcium that leads to a long-term increase in the reversal frequency of the ciliary beat.

Allometry in Physarum plasmodium during free locomotion: size versus shape, speed and rhythm.

Physarum plasmodium is a giant unicellular organism whose length can vary by more than three orders of magnitude. Using plasmodia ranging in size from 100 µm to 10 cm, we investigated the size dependency of their thickness distributions and locomotion speeds during free locomotion. (1) In the longitudinal direction, the organism is thickest close to the front, and decreases exponentially in thickness towards the rear. The slenderness ratio varies with body size according to a power law, such that large plasmodia are long and flat, whereas small plasmodia are short and thick. (2) The mean locomotion speed is proportional to the mean maximum thickness of the frontal part. By conducting a dimensional analysis, possible physical models are discussed. (3) The intrinsic period of the thickness oscillation, which is related to shuttle streaming (period 1-2 min), increases logarithmically with body size. (4) Various characteristics exhibit size-independent, long-period (20±10 min) oscillations, including speed, shape and intrinsic thickness oscillation period. These variations are closely coupled to formation of the entire cell shape, including undulation of thickness along the longitudinal axis and timing of branching of the frontal tip. Based on these experimental results and those reported previously, we propose a simple mathematical model for cell locomotion.

Periodic traction in migrating large amoeba of Physarum polycephalum.

The slime mould Physarum polycephalum is a giant multinucleated cell exhibiting well-known Ca(2+)-dependent actomyosin contractions of its vein network driving the so-called cytoplasmic shuttle streaming. Its actomyosin network forms both a filamentous cortical layer and large fibrils. In order to understand the role of each structure in the locomotory activity, we performed birefringence observations and traction force microscopy on excised fragments of Physarum. After several hours, these microplasmodia adopt three main morphologies: flat motile amoeba, chain types with round contractile heads connected by tubes and motile hybrid types. Each type exhibits oscillations with a period of about 1.5 min of cell area, traction forces and fibril activity (retardance) when fibrils are present. The amoeboid types show only peripheral forces while the chain types present a never-reported force pattern with contractile rings far from the cell boundary under the spherical heads. Forces are mostly transmitted where the actomyosin cortical layer anchors to the substratum, but fibrils maintain highly invaginated structures and contribute to forces by increasing the length of the anchorage line. Microplasmodia are motile only when there is an asymmetry in the shape and/or the force distribution.

Attempts to retreat from a dead-ended long capillary by backward swimming in Paramecium.

We have observed how the ciliate Paramecium attempts to retreat from the dead-end of a long capillary that is too narrow for turning. After many trial-and-error episodes of short-term backward swimming (SBS), which is the conventional avoidance behavior exhibited in free swimming when an obstacle is faced, long-term backward swimming (LBS) that lasted five to ten times longer was developed. LBS may have a beneficial effect for complete withdrawal from the capillary space, although in our experiment it was impossible for the organism to do so due to the capillary length. In order to identify a physically possible mechanism for LBS, we propose model equations for the membrane potential of Hodgkin-Huxley type, which describe the control of ciliary movement. The physiological implications and physical mechanism of the development of LBS are discussed.

Common mechanics of mode switching in locomotion of limbless and legged animals.

Crawling using muscular waves is observed in many species, including planaria, leeches, nemertea, aplysia, snails, chitons, earthworms and maggots. Contraction or extension waves propagate along the antero-posterior axis of the body as the crawler pushes the ground substratum backward. However, the observation that locomotory waves can be directed forward or backward has attracted much attention over the past hundred years. Legged organisms such as centipedes and millipedes exhibit parallel phenomena; leg tips form density waves that propagate backward or forward. Mechanical considerations reveal that leg-density waves play a similar role to locomotory waves in limbless species, and that locomotory waves are used by a mechanism common to both legged and limbless species to achieve crawling. Here, we report that both mode switching of the wave direction and friction control were achieved when backward motion was induced in the laboratory. We show that the many variations of switching in different animals can essentially be classified in two types according to mechanical considerations. We propose that during their evolution, limbless crawlers first moved in a manner similar to walking before legs were obtained. Therefore, legged crawlers might have learned the mechanical mode of movement involved in walking long before obtaining legs.

Current-reinforced random walks for constructing transport networks.

Biological systems that build transport networks, such as trail-laying ants and the slime mould Physarum, can be described in terms of reinforced random walks. In a reinforced random walk, the route taken by 'walking' particles depends on the previous routes of other particles. Here, we present a novel form of random walk in which the flow of particles provides this reinforcement. Starting from an analogy between electrical networks and random walks, we show how to include current reinforcement. We demonstrate that current-reinforcement results in particles converging on the optimal solution of shortest path transport problems, and avoids the self-reinforcing loops seen in standard density-based reinforcement models. We further develop a variant of the model that is biologically realistic, in the sense that the particles can be identified as ants and their measured density corresponds to those observed in maze-solving experiments on Argentine ants. For network formation, we identify the importance of nonlinear current reinforcement in producing networks that optimize both network maintenance and travel times. Other than ant trail formation, these random walks are also closely related to other biological systems, such as blood vessels and neuronal networks, which involve the transport of materials or information. We argue that current reinforcement is likely to be a common mechanism in a range of systems where network construction is observed.

Tactic direction determined by the interaction between oscillatory chemical waves and rheological deformation in an amoeba.

The survival of an organism can depend upon the direction in which it decides to move in response to changes in external conditions. Here we propose a physicochemical mechanism of the decision process for migration direction in the case of a giant amoebalike Physarum plasmodium. The tactical movement response could be changed by reversal of the phase wave of the rhythmic contractions that occur in any part of the plasmodium body when local stimulation is applied and the frequency of the rhythmic contractions is locally modulated in the stimulated region. The proposed model describes a physicochemical mechanism of coupling between the local modulation of frequency and the global transport of protoplasmic mass. The decision process is clarified from a rheological point of view.