Giovanni Polverino

Closed-loop control of zebrafish response using a bioinspired robotic-fish in a preference test

In this paper, we study the response of zebrafish to a robotic-fish whose morphology and colour pattern are inspired by zebrafish. Experiments are conducted in a three-chambered instrumented water tank where a robotic-fish is juxtaposed with an empty compartment, and the preference of live subjects is scored as the mean time spent in the vicinity of the tanks two lateral sides. The tail-beating of the robotic-fish is controlled in real-time based on feedback from fish motion to explore a spectrum of closed-loop systems, including proportional and integral controllers. Closed-loop control systems are complemented by open-loop strategies, wherein the tail-beat of the robotic-fish is independent of the fish motion. The preference space and the locomotory patterns of fish for each experimental condition are analysed and compared to understand the influence of real-time closed-loop control on zebrafish response. The results of this study show that zebrafish respond differently to the pattern of tail-beating motion executed by the robotic-fish. Specifically, the preference and behaviour of zebrafish depend on whether the robotic-fish tail-beating frequency is controlled as a function of fish motion and how such closed-loop control is implemented.

Zebrafish response to robotic fish: preference experiments on isolated individuals and small shoals

Recently developed bioinspired robots imitate their live counterparts in both aspect and functionality. Nevertheless, whether these devices can be integrated within the ecological niche inspiring their design is seldom tested experimentally. An elemental research question concerns the feasibility of modulating spontaneous behaviour of animal systems through bioinspired robotics. The following study explores the possibility of engineering a robotic fish capable of influencing the behaviour of live zebrafish (Danio rerio) in a dichotomous preference test. While we observe that the preference for the robotic fish never exceeds the preference for a conspecific, our data show that the robot is successful in attracting both isolated individuals and small shoals and that such capability is influenced by its bioinspired features. In particular, we find that the robots undulations enhance its degree of attractiveness, despite the noise inherent in the actuation system. This is the first experimental evidence that live zebrafish behaviour can be influenced by engineered robots. Such robotic platforms may constitute a valuable tool to investigate the bases of social behaviour and uncover the fundamental determinants of animal functions and dysfunctions.

Fish and robots swimming together in a water tunnel: robot color and tail-beat frequency influence fish behavior.

The possibility of integrating bioinspired robots in groups of live social animals may constitute a valuable tool to study the basis of social behavior and uncover the fundamental determinants of animal functions and dysfunctions. In this study, we investigate the interactions between individual golden shiners (Notemigonus crysoleucas) and robotic fish swimming together in a water tunnel at constant flow velocity. The robotic fish is designed to mimic its live counterpart in the aspect ratio, body shape, dimension, and locomotory pattern. Fish positional preference with respect to the robot is experimentally analyzed as the robots color pattern and tail-beat frequency are varied. Behavioral observations are corroborated by particle image velocimetry studies aimed at investigating the flow structure behind the robotic fish. Experimental results show that the time spent by golden shiners in the vicinity of the bioinspired robotic fish is the highest when the robot mimics their natural color pattern and beats its tail at the same frequency. In these conditions, fish tend to swim at the same depth of the robotic fish, where the wake from the robotic fish is stronger and hydrodynamic return is most likely to be effective.

Fish and robot dancing together: bluefin killifish females respond differently to the courtship of a robot with varying color morphs

The experimental integration of bioinspired robots in groups of social animals has become a valuable tool to understand the basis of social behavior and uncover the fundamental determinants of animal communication. In this study, we measured the preference of fertile female bluefin killifish (Lucania goodei) for robotic replicas whose aspect ratio, body size, motion pattern, and color morph were inspired by adult male killifish. The motion of the fish replica was controlled via a robotic platform, which simulated the typical courtship behavior observed in killifish males. The positional preferences of females were measured for three different color morphs (red, yellow, and blue). While variation in preference was high among females, females tend to spend more time in the vicinity of the yellow painted robot replicas. This preference may have emerged because the yellow robot replicas were very bright, particularly in the longer wavelengths (550–700 nm) compared to the red and blue replicas. These findings are in agreement with previous observations in mosquitofish and zebrafish on fish preference for artificially enhanced yellow pigmentation.

Zebrafish (Danio rerio) behavioural response to bioinspired robotic fish and mosquitofish (Gambusia affinis)

The field of ethorobotics holds promise in aiding fundamental research in animal behaviour, whereby it affords fully controllable and easily reproducible experimental tools. Most of the current ethorobotics studies are focused on the behavioural response of a selected target species as it interacts with a biologically-inspired robot in controlled laboratory conditions. In this work, we first explore the interactions between two social fish species and a robotic fish, whose design is inspired by salient visual features of one of the species. Specifically, this study investigates the behavioural response of small shoals of zebrafish interacting with a zebrafish-inspired robotic fish and small shoals of mosquitofish in a basic ecological context. Our results demonstrate that the robotic fish differentially influences the behaviour of the two species by consistently attracting zebrafish, while repelling mosquitofish. This selective behavioural control is successful in spatially isolating the two species, which would otherwise exhibit prey-predator interactions, with mosquitofish attacking zebrafish.

Mosquitofish (Gambusia affinis) responds differentially to a robotic fish of varying swimming depth and aspect ratio

In this study, we explore the feasibility of using bioinspired robotics to influence the behaviour of mosquitofish (Gambusia affinis), a social freshwater fish species that is extensively studied for the ecological issues associated with its diffusion in non-native environments. Specifically, in a dichotomous choice test, we investigate the behavioural response of small shoals of mosquitofish to a robotic fish inspired by mosquitofish in its colouration, shape, aspect ratio, and locomotion. Our results indicate that the swimming depth and the aspect ratio of the robotic fish are both determinants of mosquitofish preference. In particular, we find that mosquitofish are never attracted by a robotic fish whose colouration and shape are inspired by live subjects and that the degree of repulsion varies as a function of the swimming depth and the aspect ratio.

Collective behaviour across animal species

We posit a new geometric perspective to define, detect, and classify inherent patterns of collective behaviour across a variety of animal species. We show that machine learning techniques, and specifically the isometric mapping algorithm, allow the identification and interpretation of different types of collective behaviour in five social animal species. These results offer a first glimpse at the transformative potential of machine learning for ethology, similar to its impact on robotics, where it enabled robots to recognize objects and navigate the environment.

Influence of robotic shoal size, configuration, and activity on zebrafish behavior in a free-swimming environment.

In animal studies, robots have been recently used as a valid tool for testing a wide spectrum of hypotheses. These robots often exploit visual or auditory cues to modulate animal behavior. The propensity of zebrafish, a model organism in biological studies, toward fish with similar color patterns and shape has been leveraged to design biologically inspired robots that successfully attract zebrafish in preference tests. With an aim of extending the application of such robots to field studies, here, we investigate the response of zebrafish to multiple robotic fish swimming at different speeds and in varying arrangements. A soft real-time multi-target tracking and control system remotely steers the robots in circular trajectories during the experimental trials. Our findings indicate a complex behavioral response of zebrafish to biologically inspired robots. More robots produce a significant change in salient measures of stress, with a fast robot swimming alone causing more freezing and erratic activity than two robots swimming slowly together. In addition, fish spend more time in the proximity of a robot when they swim far apart than when the robots swim close to each other. Increase in the number of robots also significantly alters the degree of alignment of fish motion with a robot. Results from this study are expected to advance our understanding of robot perception by live animals and aid in hypothesis-driven studies in unconstrained free-swimming environments.

Mosquitofish (Gambusia affinis) Preference and Behavioral Response to Animated Images of Conspecifics Altered in Their Color, Aspect Ratio, and Swimming Depth

Mosquitofish (Gambusia affinis) is an example of a freshwater fish species whose remarkable diffusion outside its native range has led to it being placed on the list of the world’s hundred worst invasive alien species (International Union for Conservation of Nature). Here, we investigate mosquitofish shoaling tendency using a dichotomous choice test in which computer-animated images of their conspecifics are altered in color, aspect ratio, and swimming level in the water column. Pairs of virtual stimuli are systematically presented to focal subjects to evaluate their attractiveness and the effect on fish behavior. Mosquitofish respond differentially to some of these stimuli showing preference for conspecifics with enhanced yellow pigmentation while exhibiting highly varying locomotory patterns. Our results suggest that computer-animated images can be used to understand the factors that regulate the social dynamics of shoals of Gambusia affinis. Such knowledge may inform the design of control plans and open new avenues in conservation and protection of endangered animal species.

How different is a 3D-printed replica from a conspecific in the eyes of a zebrafish?

Robotics is emerging as a promising tool for aiding research on animal behavior. The possibility of generating customizable, controllable, and standardized robotic stimuli has been demonstrated through a number of behavioral assays, involving vertebrates and invertebrates. However, the specific appraisal of the nature of robotic stimuli is currently lacking. Here, we attempt to evaluate this aspect in zebrafish, through a within-subject design in which experimental subjects are faced with three experimental conditions. In the first test, we investigated sociability by measuring zebrafish response to a conspecific separated by a one-way glass. In the second test, we studied zebrafish behavior in response to a 3D-printed zebrafish replica actuated along realistic trajectories through a novel four-degree-of-freedom robotic platform. Last, we investigated fear responses in a shelter-seeking test. In agreement with our expectations, zebrafish exhibited an equivalent preference for live and robotic stimuli, and the degree of preference for the robotic replica correlated negatively with the individual propensity to seek shelter. The equivalent preference for the replica and conspecific suggests that the appraisal of the target stimuli is analogous. The preliminary evidence of a correlation between behavioral responses across tests points to the readability of robotics-based approaches to investigate interindividual differences.