Animal-Robot Interactions: Electrocommunication, Sensory Ecology, and Group Dynamics in a Mormyrid Weakly Electric Fish

Mormyrid weakly electric fish possess a specialized electrosensory system. During the process of active electrolocation, these animals perceive self-generated electric organ dis-charges (EOD) and are thereby able to detect objects in their nearby environment. The EOD is a short, biphasic pulse, which is simultaneously used to communicate with conspe-cifics. There are two principles according to which information exchange occurs during electrocommunication. The waveform of the EOD constitutes a relatively stable identity marker that signals species, gender, and status of an individual. In contrast, the temporal sequence of inter-discharge intervals (IDI) is highly variable and encodes context-specific information. Modifications of IDI-duration not only alter the instantaneous discharge fre-quency but also enable the generation of specific signaling patterns and interactive dis-charge sequences. One such interactive discharge behavior is the so-called echo response, during which a fish responds with a constant latency of only a few milliseconds to the EOD of a conspecific. Animals can synchronize their signaling sequences by mutually generating echoes to each other's signals over a coherent period. Although active electrolocation and electrocommunication are mediated by different types of electroreceptor organs and neural pathways, an unambiguous assignment of electromotor behavior to only one of the two functions is often problematic. In this thesis, the significance of IDI-based signaling sequences during motor and electro-motor interactions of the mormyrid fish Mormyrus rume proboscirostris were investigated. To this end, different electrical playback sequences of species-specific EODs were generated via mobile fish dummies, and the motor and electromotor responses of live fish were analyzed. In Part One of this thesis, electrocommunication strategies of the fish were analyzed, and particularly the functions of double pulses, discharge regularizations, and echo responses were examined in an adaptive context. Double pulses were classified as an aggressive mo-tivation signal, whereas regularizations may have a communicative function during the early stages of the sequential assessment of a potential opponent. In this context, discharge synchronization by means of echo responses may enable a mutual assessment for the net benefit of both contestants. Because echo responses occur in various behavioral contexts, and artificial echoes of the dummy evoked increased echoing by the fish, it was hypothesized that the echo response serves a more general purpose by enabling mutual allocation of social attention between two fish. In Part Two of this thesis, a biomimetic robotic fish was designed to investigate the senso-ry basis on which fish followed the dummy. It was shown that electrical playback signals induced following-behavior in live fish, whereas biomimetic motility patterns had no ef-fect. By subsequently reducing the mobile dummy to only the electric signaling sequence from the perspective of the fish, it could be shown that passive perception of electrical communication signals is also involved in mediating the spatial coordination of social in-teractions. This passive perception is likely mediated by the same electroreceptor organs that are used during electrocommunication. The EOD can therefore be considered to be an essential social stimulus that makes it possible to integrate a dummy into a group of weak-ly electric fish as an artificial conspecific. The influence of an interactively signaling mobile dummy fish on small groups of up to four individuals was investigated in Part Three of this thesis. Typical schooling behavior was a rare occurrence in this context. However, EOD-synchronizations through mutual echo responses between two fish, or between a fish and the interactive dummy, were fre-quently observed during social interactions in small groups. Motor interactions during synchronization episodes supported the hypothesis that mormyrids may use discharge synchronizations between individuals to allocate social attention, and the echo response may thus adopt a particularly useful function during communication in groups.Schwach elektrische Fisch aus der Familie der Mormyriden verfügen über ein spezialisier-tes elektrosensorisches Sinnessystem. In einem Prozess, der als aktive Elektroortung be-zeichnet wird, sind diese Tiere in der Lage, selbstgenerierte elektrische Organentladungen (EOD) wahrzunehmen, und dadurch Objekte in ihrer unmittelbaren Nähe zu detektieren. Das EOD ist ein kurzer bipolarer Puls, der gleichzeitig auch zur Kommunikation mit Artge-nossen dient. Informationsaustausch während der Elektrokommunikation basiert auf zwei verschiedenen Prinzipien: Die Wellenform des EOD stellt einen relativ konstanten Identi-tätsmarker dar, der beispielsweise Art, Geschlecht und Status eines Individuums signali-siert. Die zeitliche Abfolge der Intervalle zwischen den EODs ist hingegen höchst variabel und kodiert kontextspezifische Information. Durch Modifikation der Intervalldauer ändert sich nicht nur die Entladungsfrequenz, sondern es können auch spezifische Signalmuster und interaktive Entladungssequenzen generiert werden. Ein interaktives Entladungsver-halten stellt beispielsweise die Echoantwort dar, bei der ein Fisch mit einer konstanten Latenz von wenigen Millisekunden auf das EOD eines Artgenossen reagiert. Zwei Tiere können ihre Entladungssequenzen synchronisieren, indem sie ihre Signale über einen kohärenten Zeitraum gegenseitig mit Echos beantworten. Obwohl aktive Elektroortung und Elektrokommunikation über unterschiedliche Rezeptororgansysteme und neuronale Pfade vermittelt werden, ist eine eindeutige Zuordnung der elektromotorischen Verhal-tensäußerungen der Fische zu nur einer der beiden Funktionen oft problematisch. In der vorliegenden Arbeit wurde die Bedeutung intervallbasierter EOD-Sequenzen für motorische und elektromotorische Interaktionen des Mormyriden Mormyrus rume proboscirostris erforscht. Hierzu wurden verschiedene elektrische Playbacksequenzen artspezifischer EODs generiert und durch mobile Fischattrappen wiedergegeben. Die mo-torischen und elektromotorischen Verhaltensreaktionen der Fische wurden analysiert. Im ersten Teil der Arbeit wurden Elektrokommunikationsstrategien der Fische analysiert und die adaptive Funktion insbesondere von Doppelpulsen, Entladungsregularisierungen und Echoantworten untersucht. Doppelpulse wurden als aggressives Motivationssignal kategorisiert, wohingegen die Kommunikationsfunktion von Regularisierungen im gegen-seitigen Einschätzen zu Beginn einer kompetitiven Begegnung zu liegen scheint. Entla-dungssynchronisation durch gegenseitige Echoantworten kann dabei eine Einschätzung des Gegenübers zum Vorteil beider Parteien erleichtern. Da Echoantworten in verschiede-nen Verhaltenssituationen auftreten und artifizielle Echoantworten der Attrappe vermehrt zu Echos vonseiten der Fische führten, wurde postuliert, dass die Echoantwort eine generellere Funktion bei der Fokussierung gegenseitiger sozialer Aufmerksamkeit über-nehmen kann. Im zweiten Teil der Arbeit wurde ein biomimetischer Fischroboter konstruiert, um zu untersuchen, auf welcher sensorischen Grundlage die Fische der Attrappe folgen. Es konnte gezeigt werden, dass elektrische Playbacksignale, nicht aber biomimetische Bewe-gungsmuster, Folgeverhalten der Fische induzieren. In einem weiteren Schritt konnte durch die Reduktion der Attrappe auf die elektrischen Signalsequenzen aus der Perspektive der Versuchsfische gezeigt werden, dass passive Wahrnehmung elektrischer Kommu-nikationssignale auch bei der räumlichen Koordination sozialer Interaktionen von Bedeu-tung ist. Dies wird mutmaßlich über die gleichen Rezeptororgane vermittelt, die auch für die Elektrokommunikation verantwortlich sind. Das EOD kann daher als ein soziales Signal betrachtet werden, das es ermöglicht, eine Attrappe als künstlichen Artgenossen in eine Gruppe schwach elektrischer Fische zu integrieren. Der Einfluss einer elektrisch interaktiven mobilen Fischattrappe auf kleine Gruppen von bis zu vier Individuen wurde im dritten Teil der Arbeit getestet. Typisches Schwarmver-halten konnte in diesem Zusammenhang nur selten beobachtet werden. In kleinen Gruppen kam es während sozialer Interaktionen jedoch häufig zu EOD-Synchronisationen durch Echoantworten zwischen zwei Fischen, oder zwischen einem Fisch und der interaktiven Attrappe. Motorische Verhaltensinteraktionen im Zeitraum dieser Synchronisationen stützen die Hypothese, dass Mormyriden durch elektrische Entladungssynchronisation soziale Aufmerksamkeit zwischen Individuen herstellen können, und die Echoantwort somit besonders in Gruppen eine nützliche Kommunikationsfunktion übernehmen kann

Multiple cues produced by a robotic fish modulate aggressive behaviour in Siamese fighting fishes

The use of robotics to establish social interactions between animals and robots, represents an elegant and innovative method to investigate animal behaviour. However, robots are still underused to investigate high complex and flexible behaviours, such as aggression. Here, Betta splendens was tested as model system to shed light on the effect of a robotic fish eliciting aggression. We evaluated how multiple signal systems, including a light stimulus, affect aggressive responses in B. splendens. Furthermore, we conducted experiments to estimate if aggressive responses were triggered by the biomimetic shape of fish replica, or whether any intruder object was effective as well. Male fishes showed longer and higher aggressive displays as puzzled stimuli from the fish replica increased. When the fish replica emitted its full sequence of cues, the intensity of aggression exceeded even that produced by real fish opponents. Fish replica shape was necessary for conspecific opponent perception, evoking significant aggressive responses. Overall, this study highlights that the efficacy of an artificial opponent eliciting aggressive behaviour in fish can be boosted by exposure to multiple signals. Optimizing the cue combination delivered by the robotic fish replica may be helpful to predict escalating levels of aggression

Follow the dummy: measuring the influence of a biomimetic robotic fish-lure on the collective decisions of a zebrafish shoal inside a circular corridor

Robotic agents that are accepted by animals as conspecifics are very powerful tools in behavioral biology because of the ways they help in studying social interactions in gregarious animals. In recent years, we have developed a biomimetic robotic fish lure for the purpose of studying the behavior of the zebrafish Danio rerio. In this paper, we present a series of experiments that were designed to assess the impact of some features of the lure regarding its acceptance among the fish. We developed an experimental setup composed of a circular corridor and a motorized rotating system able to steer the lure inside the corridor with a tunable linear speed. We used the fish swimming direction and distance between the fish and the lure as a metric to characterize the level of acceptance of the lure, depending on various parameters. The methodology presented and the experimental results are promising for the field of animal–robot interaction studies

Shoaling with fish: using miniature robotic agents to close the interaction loop with groups of zebrafish Danio rerio

Robotic animals are nowadays developed for various types of research, such as bio-inspired robotics, biomimetics and animal behavior studies. The miniaturization of technologies and the increase in performance of embedded systems allowed engineers to develop more powerful, sophisticated and miniature devices. The case of robotic fish is a typical example of such challenging design: the fish locomotion and body movements are difficult to reproduce and the device has to move autonomously underwater. More specifically, in the case of collective animal behavior research, the robotic device has to interact with animals by generating and exploiting signals relevant for social behavior. Once perceived by the animal society as conspecific, these robots can become powerful tools to study the animal behaviors, as they can at the same time monitor the changes in behavior and influence the collective choices of the animal society. In this work, we present novel robotized tools that can integrate shoals of fish in order to study their collective behaviors. This robotic platform is composed of two subsystems: a miniature wheeled mobile robot that can achieve dynamic movements and multi-robot long-duration experiments, and a robotic fish lure that is able to beat its tail to generate fish-like body movements. The two subsystems are coupled with magnets which allows the wheeled mobile robot to steer the robotic fish lure so that it reaches very high speeds and accelerations while achieving shoaling. An experimental setup to conduct studies on mixed societies of artificial and living fish was designed to facilitate the experiments for biologists. A software framework was also implemented to control the robots in a closed-loop using data extracted from visual tracking that retrieved the position of the robots and the fish. We selected the zebrafish Danio rerio as a model to perform experiments to qualify our system. We used the current state of the art on the zebrafish social behavior to define the specifications of the robots, and we performed stimuli analysis to improve their developments. Bio-inspired controllers were designed based on data extracted from experiments with zebrafish for the robots to mimic the zebrafish locomotion underwater. Experiments involving a robot with a shoal of fish in a constrained environment showed that the locomotion of the robot was one of the main factor to affect the collective behavior of zebrafish. We also shown that the body movements and the biomimetic appearance of the lure could increase its acceptance by fish. Finally, an experiment involving a mixed society of fish and robots qualified the robotic system to be integrated among a zebrafish shoal and to be able to influence the collective decisions of the fish. These results are very promising for the field of fish-robot interaction studies, as we showed the effect of the robots in long-duration experiments and repetitively, with the same order of response from the animals