Quantifying the biomimicry gap in biohybrid robot-fish pairs.

Biohybrid systems in which robotic lures interact with animals have become compelling tools for probing and identifying the mechanisms underlying collective animal behavior. One key challenge lies in the transfer of social interaction models from simulations to reality, using robotics to validate the modeling hypotheses. This challenge arises in bridging what we term the 'biomimicry gap', which is caused by imperfect robotic replicas, communication cues and physics constraints not incorporated in the simulations, that may elicit unrealistic behavioral responses in animals. In this work, we used a biomimetic lure of a rummy-nose tetra fish (Hemigrammus rhodostomus) and a neural network (NN) model for generating biomimetic social interactions. Through experiments with a biohybrid pair comprising a fish and the robotic lure, a pair of real fish, and simulations of pairs of fish, we demonstrate that our biohybrid system generates social interactions mirroring those of genuine fish pairs. Our analyses highlight that: 1) the lure and NN maintain minimal deviation in real-world interactions compared to simulations and fish-only experiments, 2) our NN controls the robot efficiently in real-time, and 3) a comprehensive validation is crucial to bridge the biomimicry gap, ensuring realistic biohybrid systems.

How aggressive interactions with biomimetic agents optimize reproductive performances in mass-reared males of the Mediterranean fruit fly.

Mass-rearing procedures of insect species, often used in biological control and Sterile Insect Technique, can reduce the insects competitiveness in foraging, dispersal, and mating. The evocation of certain behaviours responsible to induce specific neuroendocrine products may restore or improve the competitiveness of mass-reared individuals. Herein, we used a mass-reared strain of Ceratitis capitata as model organism. C. capitata is a polyphagous pest exhibiting territorial displays that are closely related to its reproductive performance. We tested if the behaviour of C. capitata males could be altered by hybrid aggressive interactions with a conspecific-mimicking robotic fly, leading to more competitive individuals in subsequent mating events. Aggressive interactions with the robotic fly had a notable effect on subsequent courtship and mating sequences of males that performed longer courtship displays compared to naïve individuals. Furthermore, previous interactions with the robotic fly produced a higher mating success of males. Reproductive performances of C. capitata males may be improved by specific octopaminergic neurones activated during previous aggressive interactions with the robotic fly. This study adds fundamental knowledge on the potential role of specific neuro-behavioural processes in the ecology of tephritid species and paves the way to innovative biotechnological control methods based on robotics and bionics.

[Simulation design and experimental study of magnetic stimulation coil for robot pigeon].

To explore the feasibility of applying magnetic stimulation technology to the movement control of animal robots, the influence of coil radius, number of turns and other factors on the intensity, depth and focus of magnetic stimulation was simulated and analyzed for robot pigeons. The coil design scheme was proposed. The coil was placed on the head and one of the legs of the pigeon, and the leg electromyography (EMG) was recorded when magnetic stimulation was performed. Results showed that the EMG was significantly strengthened during magnetic stimulation. With the reduction of the output frequency of the magnetic stimulation system, the output current was increased and the EMG was enhanced accordingly. Compared with the brain magnetic stimulation, sciatic nerve stimulation produced a more significant EMG enhancement response. This indicated that the magnetic stimulation system could effectively modulate the functions of brain and peripheral nerves by driving the coil. This study provides theoretical and experimental guidance for the subsequent optimization and improvement of practical coils, and lays a preliminary theoretical and experimental foundation for the implementation of magnetic stimulation motion control of animal robots.

Simulation design and experimental study of magnetic stimulation coil for robot pigeon / 生物医学工程学杂志

To explore the feasibility of applying magnetic stimulation technology to the movement control of animal robots, the influence of coil radius, number of turns and other factors on the intensity, depth and focus of magnetic stimulation was simulated and analyzed for robot pigeons. The coil design scheme was proposed. The coil was placed on the head and one of the legs of the pigeon, and the leg electromyography (EMG) was recorded when magnetic stimulation was performed. Results showed that the EMG was significantly strengthened during magnetic stimulation. With the reduction of the output frequency of the magnetic stimulation system, the output current was increased and the EMG was enhanced accordingly. Compared with the brain magnetic stimulation, sciatic nerve stimulation produced a more significant EMG enhancement response. This indicated that the magnetic stimulation system could effectively modulate the functions of brain and peripheral nerves by driving the coil. This study provides theoretical and experimental guidance for the subsequent optimization and improvement of practical coils, and lays a preliminary theoretical and experimental foundation for the implementation of magnetic stimulation motion control of animal robots.

[Design and preliminary application of outdoor flying pigeon-robot].

Control at beyond-visual ranges is of great significance to animal-robots with wide range motion capability. For pigeon-robots, such control can be done by the way of onboard preprogram, but not constitute a closed-loop yet. This study designed a new control system for pigeon-robots, which integrated the function of trajectory monitoring to that of brain stimulation. It achieved the closed-loop control in turning or circling by estimating pigeons' flight state instantaneously and the corresponding logical regulation. The stimulation targets located at the formation reticularis medialis mesencephali (FRM) in the left and right brain, for the purposes of left- and right-turn control, respectively. The stimulus was characterized by the waveform mimicking the nerve cell membrane potential, and was activated intermittently. The wearable control unit weighted 11.8 g totally. The results showed a 90% success rate by the closed-loop control in pigeon-robots. It was convenient to obtain the wing shape during flight maneuver, by equipping a pigeon-robot with a vivo camera. It was also feasible to regulate the evolution of pigeon flocks by the pigeon-robots at different hierarchical level. All of these lay the groundwork for the application of pigeon-robots in scientific researches.

[Research and application of photovoltaic cell online monitoring system for animal robot stimulator].

Power supply plays a key role in ensuring animal robots to obtain effective stimulation. To extending the stimulating time, there is a need to apply photovoltaic cells and monitor their parameter variations, which can help operators to obtain the optimal stimulation strategy. In this paper, an online monitoring system of photovoltaic cells for animal robot stimulators was presented. It was composed of battery information sampling circuit, multi-channel neural signal generator, power module and human-computer interaction interface. When the signal generator was working, remote navigation control of animal robot could be achieved, and the battery voltage, current, temperature and electricity information was collected through the battery information sampling circuit and displayed on the human-computer interaction system in real time. If there was any abnormal status, alarm would be activated. The battery parameters were obtained by charging and discharging test. The battery life under different light intensity and the stimulation effect of neural signal generator were tested. Results showed that the sampling errors of battery voltage, current and electric quantity were less than 15 mV, 5 mA and 6 mAh, respectively. Compared with the system without photovoltaic cells, the battery life was extended by 148% at the light intensity of 78 320 lx, solving the battery life problem to some extent. When animal robot was stimulated with this system, left and right turns could be controlled to complete with the success rate more than 80%. It will help researchers to optimize animal robot control strategies through the parameters obtained in this system.

Exploring the advantages of using artificial agents to investigate animacy perception in cats and dogs.

Self-propelled motion cues elicit the perception of inanimate objects as animate. Studies usually rely on the looking behaviour of subjects towards stimuli displayed on a screen, but utilizing artificial unidentified moving objects (UMOs) provides a more natural, interactive context. Here, we investigated whether cats and dogs discriminate between UMOs showing animate vs inanimate motion, and how they react to the UMOs' interactive behaviour. Subjects first observed, in turn, the motion of an animate and an inanimate UMO, and then they could move freely for 2 min while both UMOs were present (two-way choice phase). In the following specific motion phase, the animate UMO showed one of three interactive behaviours: pushing a ball, a luring motion, or moving towards the subject (between-subject design). Then, subjects could move freely for 2 min again while the UMO was motionless. At the end, subjects were free to move in the room while the UMO was moving semi-randomly in the room. We found that dogs approached and touched the UMO(s) sooner and more frequently than cats, regardless of the context. In the two-way choice phase, dogs looked at the animate UMO more often, and both species touched the animate UMO more frequently. However, whether the UMO showed playing, luring or assertive behaviour did not influence subjects' behaviour. In summary, both species displayed distinctive behaviour towards the animate UMO, but in dogs, in addition to the physical contact this was also reflected by the looking behaviour. Overall, dogs were more keen to explore and interact with the UMO than cats, which might be due to the general increased stress of cats in novel environments. The findings indicate the importance of measuring multiple behaviours when assessing responses to animacy. The live demonstration using artificial agents provides a unique opportunity to study social perception in nonhuman species.

Robotic communication with ants.

We used a robotic gantry to test the hypothesis that tandem running in the ant Temnothorax albipennis can be successful in the absence of trail laying by the leader. Pheromone glands were placed on a pin attached to a gantry. This set-up substituted for the leader of a tandem run. Neither the pin nor the glands touched the substrate and thus the ant following the robot was tracking a plume of airborne pheromones. The robot led individual workers from their current nest to a potential new one. The robotic gantry was programmed to allow for human intervention along its path to permit the following ant to stop and survey its surroundings and then catch up with its mechanical leader. The gantry then automatically tracked the precise route taken by each ant from the new nest back to the old one. Ants led by the robot were significantly more successful at finding their way home than those we carried to the new nest that had no opportunity to learn landmarks. The robot was programmed to take either a straight or a sinusoidal path to the new nest. However, we found no significant difference in the abilities of ants that had been led on such direct or sinuous paths to find their way home. Here, the robot laid no trail but our findings suggest that, under such circumstances, the following ant may lay a trail to substitute for the missing one.

Individual recognition and long-term memory of inanimate interactive agents and humans in dogs.

Investigation of individual recognition (IR) is difficult due to the lack of proper control of cues and previous experiences of subjects. Utilization of artificial agents (Unidentified Moving Objects: UMOs) may offer a better approach than using conspecifics or humans as partners. In Experiment 1, we investigated whether dogs are able to develop IR of UMOs (that is stable for at least 24 h) or that they only retain a more generalised memory about them. The UMO helped dogs to obtain an unreachable ball and played with them. One day, one week or one month later, we tested whether dogs display specific behaviour toward the familiar UMO over unfamiliar ones (four-way choice test). Dogs were also re-tested in the same helping context and playing interaction. Subjects did not approach the familiar UMO sooner than the others; however, they gazed at the familiar UMO earlier during re-testing of the problem solving task, irrespectively of the delay. In Experiment 2, we repeated the same procedure with human partners, applying a two-way choice test after a week delay, to study whether lack of IR was specific to the UMO. Dogs did not approach the familiar human sooner than the unfamiliar, but they gazed at the familiar partner earlier during re-testing. Thus, dogs do not seem to recognise an individual UMO or human after a short experience, but they remember the interaction with the novel partner in general, even after a long delay. We suggest that dogs need more experience with a specific social partner for the development of long-term memory.

Any colour you like: fish interacting with bioinspired robots unravel mechanisms promoting mixed phenotype aggregations.

Collective behaviours in homogeneous shoals provide several benefits to conspecifics, although mixed-species aggregations have been reported to often occur. Mixed aggregations may confer several beneficial effects such as antipredator and foraging advantages. However, the mechanisms promoting phenotypically heterogeneous fish aggregations have been poorly explored so far. Herein, the neon tetraParacheirodon innesiwas selected as the ideal model organism to test the role of visible phenotypic traits in promoting fish shoaling. Robotic fish replicas of different colours, but with a morphology inspired byP. innesi, were developed to test the affiliation behaviour of neon tetra individuals towards fish replicas with different phenotypic traits.P. innesiindividuals showed a decreasing preference in shoaling with the biomimetic, the blue, the red, and the grey replicas. This could be due to the greater visibility of the blue colour even in dark conditions. Furthermore, an increased reddening of the livery is often caused by physiological processes related to a nonoptimal behavioural status. The time spent in shoaling with each fish replica was strongly influenced by different ecological contexts. The longest shoaling duration was observed when a biomimetic predator was present, while the shortest shoaling duration was recorded in the presence of food. This confirms the hypothesis that heterogeneous shoals are promoted by the antipredator benefits, and reduced by competition. This study allowed us to understand basic features of the behavioural ecology favouring heterogeneous aggregations in shoaling fish, and provided a novel paradigm for biohybrid robotics.

Design and preliminary application of outdoor flying pigeon-robot / 生物医学工程学杂志

Control at beyond-visual ranges is of great significance to animal-robots with wide range motion capability. For pigeon-robots, such control can be done by the way of onboard preprogram, but not constitute a closed-loop yet. This study designed a new control system for pigeon-robots, which integrated the function of trajectory monitoring to that of brain stimulation. It achieved the closed-loop control in turning or circling by estimating pigeons' flight state instantaneously and the corresponding logical regulation. The stimulation targets located at the formation reticularis medialis mesencephali (FRM) in the left and right brain, for the purposes of left- and right-turn control, respectively. The stimulus was characterized by the waveform mimicking the nerve cell membrane potential, and was activated intermittently. The wearable control unit weighted 11.8 g totally. The results showed a 90% success rate by the closed-loop control in pigeon-robots. It was convenient to obtain the wing shape during flight maneuver, by equipping a pigeon-robot with a vivo camera. It was also feasible to regulate the evolution of pigeon flocks by the pigeon-robots at different hierarchical level. All of these lay the groundwork for the application of pigeon-robots in scientific researches.

Freshwater organisms potentially useful as biosensors and power-generation mediators in biohybrid robotics.

Facing the threat of rapidly worsening water quality, there is an urgent need to develop novel approaches of monitoring its global supplies and early detection of environmental fluctuations. Global warming, urban growth and other factors have threatened not only the freshwater supply but also the well-being of many species inhabiting it. Traditionally, laboratory-based studies can be both time and money consuming and so, the development of a real-time, continuous monitoring method has proven necessary. The use of autonomous, self-actualizing entities became an efficient way of monitoring the environment. The Microbial Fuel Cells (MFC) will be investigated as an alternative energy source to allow for these entities to self-actualize. This concept has been improved with the use of various lifeforms in the role of biosensors in a structure called "biohybrid" which we aim to develop further within the framework of project Robocoenosis relying on animal-robot interaction. We introduce a novel concept of a fully autonomous biohybrid agent with various lifeforms in the role of biosensors. Herein, we identify most promising organisms in the context of underwater robotics, among others Dreissena polymorpha, Anodonta cygnaea, Daphnia sp. and various algae. Special focus is placed on the "ecosystem hacking" based on their interaction with the electronic parts. This project uses Austrian lakes of various trophic levels (Millstättersee, Hallstättersee and Neusiedlersee) as case studies and as a "proof of concept".

Electric signal synchronization as a behavioural strategy to generate social attention in small groups of mormyrid weakly electric fish and a mobile fish robot.

African weakly electric fish communicate at night by constantly emitting and perceiving brief electrical signals (electric organ discharges, EOD) at variable inter-discharge intervals (IDI). While the waveform of single EODs contains information about the sender's identity, the variable IDI patterns convey information about its current motivational and behavioural state. Pairs of fish can synchronize their EODs to each other via echo responses, and we have previously formulated a 'social attention hypothesis' stating that fish use echo responses to address specific individuals and establish brief dyadic communication frameworks within a group. Here, we employed a mobile fish robot to investigate the behaviour of small groups of up to four Mormyrus rume and characterized the social situations during which synchronizations occurred. An EOD-emitting robot reliably evoked social following behaviour, which was strongest in smaller groups and declined with increasing group size. We did not find significant differences in motor behaviour of M. rume with either an interactive playback (echo response) or a random control playback by the robot. Still, the robot reliably elicited mutual synchronizations with other fish. Synchronizations mostly occurred during relatively close social interactions, usually when the fish that initiated synchronization approached either the robot or another fish from a distance. The results support our social attention hypothesis and suggest that electric signal synchronization might facilitate the exchange of social information during a wide range of social behaviours from aggressive territorial displays to shoaling and even cooperative hunting in some mormyrids.

Archerfish respond to a hunting robotic conspecific.

While the unique hunting behavior of archerfish has received considerable scientific attention, the specific social cues that govern behaviors like intraspecific kleptoparasitism in the species are less understood. This paper asks whether the use of a robotic facsimile representing an archerfish can elicit a social response if it approximates an archerfish's appearance, along with key features of its hunting behavior. We found that the fish respond to the robot when it hunted, as indicated by decreasing distances between the robot and fish (and among the fish) during the robot's hunting behavior sequence, as well as higher net transfer entropy when the robot was hunting. These effects were present even when the robot's "hunt" was unproductive and did not result in food. The temporal pattern of fish approach to the robot and each other indicated that the segment of robot hunting behavior proximal to the robotic facsimile shot elicited fish behavior initially. However, earlier cues in the robot's hunting sequence became important following more experience with a food contingency. This indicates that further studies could use a robotic facsimile to conduct a detailed stimulus analysis, changing aspects of the robot's appearance and behavior to uncover the basic mechanisms of information transfer among individuals in a social hunting scenario.

Absence of "selfish herd" dynamics in bird flocks under threat.

The "selfish herd" hypothesis1 provides a potential mechanism to explain a ubiquitous phenomenon in nature: that of non-kin aggregations. Individuals in selfish herds are thought to benefit by reducing their own risk at the expense of conspecifics by attracting toward their neighbors' positions1,2 or central locations in the aggregation.3-5 Alternatively, increased alignment with their neighbors' orientation could reduce the chance of predation through information sharing6-8 or collective escape.6 Using both small and large flocks of homing pigeons (Columba livia; n = 8-10 or n = 27-34 individuals) tagged with 5-Hz GPS loggers and a GPS-tagged, remote-controlled model peregrine falcon (Falco peregrinus), we tested whether individuals increase their use of attraction over alignment when under perceived threat. We conducted n = 27 flights in treatment conditions, chased by the robotic "predator," and n = 16 flights in control conditions (not chased). Despite responding strongly to the RobotFalcon-by turning away from its flight direction-individuals in treatment flocks demonstrated no increased attraction compared with control flocks, and this result held across both flock sizes. We suggest that mutualistic alignment is more advantageous than selfish attraction in groups with a high coincidence of individual and collective interests (adaptive hypothesis). However, we also explore alternative explanations, such as high cognitive demand under threat and collision avoidance (mechanistic hypotheses). We conclude that selfish herd may not be an appropriate paradigm for understanding the function of highly synchronous collective motion, as observed in bird flocks and perhaps also fish shoals and highly aligned mammal aggregations, such as moving herds.

Unveiling social distancing mechanisms via a fish-robot hybrid interaction.

Pathogen transmission is a major limit of social species. Social distancing, a behavioural-based response to diseases, has been regularly reported in nature. However, the identification of distinctive stimuli associated with an infectious disease represents a challenging task for host species, whose cognitive mechanisms are still poorly understood. Herein, the social fish Paracheirodon innesi, was selected as model organism to investigate animal abilities in exploiting visual information to identify and promote social distancing towards potentially infected conspecifics. To address this, a robotic fish replica mimicking a healthy P. innesi subject, and another mimicking P. innesi with morphological and/or locomotion anomalies were developed. P. innesi individuals were attracted by the healthy fish replica, while they avoided the fish replica with morphological abnormalities, as well as the fish replica with an intact appearance, but performing locomotion anomalies (both symptoms associated with a microsporidian parasite infesting P. innesi and other fish). Furthermore, the fish replica presenting both morphology and locomotion anomalies in conjunction, triggered a significantly stronger social distancing response. This confirms the hypothesis that group living animals overgeneralize cues that can be related with a disease to minimize transmission, and highlights the important role of visual cues in infection risk contexts. This study prompts more attention on the role of behavioural-based strategies to avoid pathogen/parasite diffusion, and can be used to optimize computational approaches to model disease dynamics.

Opposite valence social information provided by bio-robotic demonstrators shapes selection processes in the green bottle fly.

Social learning represents a high-level complex process to acquire information about the environment, which is increasingly reported in invertebrates. The animal-robot interaction paradigm turned out to be an encouraging strategy to unveil social learning in vertebrates, but it has not been fully exploited in invertebrates. In this study, Lucilia sericata adults were induced to observe bio-robotic conspecific and predator demonstrators to reproduce different flower foraging choices. Can a fly manage two flows of social information with opposite valence? Herein, we attempt a reply. The selection process of L. sericata was affected by social information provided through different bio-robotic demonstrators, by avoiding coloured discs previously visited by a bio-robotic predator and preferring coloured discs previously visited by a bio-robotic conspecific. When both bio-robotic demonstrators visited the same disc, the latency duration increased and the flies significantly tended to avoid this disc. This indicates the complex risk-benefit evaluation process carried out by L. sericata during the acquisition of such social information. Overall, this article provides a unique perspective on the behavioural ecology of social learning in non-social insects; it also highlights the high potential of the animal-robot interaction approach for unveiling the full spectrum of invertebrates' abilities in using social information.

Bio-robotic cues show how the Trinidadian guppy male recognises the morphological features of receptive females.

Sensory fusion is used by the males of several animal species to discriminate the mating status of females by evaluating their phenotypic traits. The predominant trait used is olfactory cues, and the role of visual cues is not yet fully understood. The ability of Poecilia reticulata males to evaluate females' receptivity based on visual cues was investigated. Guppy males adopt two different mating strategies, courtship displays and forced copulation, towards receptive and pregnant females, respectively. Robotic counterparts mimicking receptive and pregnant females were developed to test whether males relied only on visual information to determine a females' mating status. Exposure to the robotic receptive females evoked courtship behaviours, while forced copulation attempts were more frequent towards the robotic pregnant females. When the robotic fish were simultaneously exposed, regardless of the presence or absence of receptive-female olfactory cues, males expressed their preference for the receptive female. Visual processing showed that fish social interactions played a strategic role in their collection of information, especially when other stimuli were not available. The proposed ethorobotic approach allowed for assessing the role of visual cues in the mating choice of P. reticulata males and highlighting the information processing methods and cognition in aquatic animals.

Beetle-robot hybrid interaction: sex, lateralization and mating experience modulate behavioural responses to robotic cues in the larger grain borer Prostephanus truncatus (Horn).

Ethorobotics, a new fascinating field of biorobotics, proposes the use of robotic replicas as an advanced method for investigating animal behaviour. This novel research approach can also encourage the development of advanced bioinspired robots. In the present study, we investigated the pushing behaviour, a particular display occurring in several beetle species, such as the larger grain borer, Prostephanus truncatus, during both male-female and male-male contexts. We developed a robotic apparatus actuating female and male-mimicking dummies to study if sex, mating experience and asymmetries of robotic cues can modulate the escalation of pushing behaviour. Results showed that the time needed by P. truncatus to react to female-smelling biomimetic dummies was chiefly affected by their mating experience and the dummy odour. This was likely due to reduce waste of costly sperm in mated males during the subsequent sexual interactions. The pushing behaviour was performed longer and with a higher number of acts when virgin females were approached from their right side. More and longer pushing acts were noted when virgin males were approached from their left side. Dedicated neural circuits would likely act in opposite direction in females and males producing population-level lateralized sensory-motor displays, which may be evolved to promote male approaches from the left side of females, thus improving short-distance sex recognition. Overall, this study provides new insights on the behavioural ecology of stored-product beetles, as well as on self-organization and decentralized decision making that can be exploited to develop bioinspired algorithms for task optimization, involving real-world scenarios.

A novel rat robot controlled by electrical stimulation of the nigrostriatal pathway.

OBJECTIVE: Artificial manipulation of animal movement could offer interesting advantages and potential applications using the animal's inherited superior sensation and mobility. Although several behavior control models have been introduced, they generally epitomize virtual reward-based training models. In this model, rats are trained multiple times so they can recall the relationship between cues and rewards. It is well known that activation of one side of the nigrostriatal pathway (NSP) in the rat induces immediate turning toward the contralateral side. However, this NSP stimulation-induced directional movement has not been used for the purpose of animal-robot navigation. In this study, the authors aimed to electrically stimulate the NSP of conscious rats to build a command-prompt rat robot. METHODS: Repetitive NSP stimulation at 1-second intervals was applied via implanted electrodes to induce immediate contraversive turning movements in 7 rats in open field tests in the absence of any sensory cues or rewards. The rats were manipulated to navigate from the start arm to a target zone in either the left or right arm of a T-maze. A leftward trial was followed by a rightward trial, and each rat completed a total of 10 trials. In the control group, 7 rats were tested in the same way without NSP stimulation. The time taken to navigate the maze was compared between experimental and control groups. RESULTS: All rats in the experimental group successfully reached the target area for all 70 trials in a short period of time with a short interstimulus interval (< 0.7 seconds), but only 41% of rats in the control group reached the target area and required a longer period of time to do so. The experimental group made correct directional turning movements at the intersection zone of the T-maze, taking significantly less time than the control group. No significant difference in navigation duration for the forward movements on the start and goal arms was observed between the two groups. However, the experimental group showed quick and accurate movement at the intersection zone, which made the difference in the success rate and elapsed time of tasks. CONCLUSIONS: The results of this study clearly indicate that a rat-robot model based on NSP stimulation can be a practical alternative to previously reported models controlled by virtual sensory cues and rewards.