Guppies Prefer to Follow Large (Robot) Leaders Irrespective of Own Size

Body size is often assumed to determine how successfully an individual can lead others with larger individuals being better leaders than smaller ones. But even if larger individuals are more readily followed, body size often correlates with specific behavioral patterns and it is thus unclear whether larger individuals are more often followed than smaller ones because of their size or because they behave in a certain way. To control for behavioral differences among differentially-sized leaders, we used biomimetic robotic fish (Robofish) of different sizes. Live guppies (Poecilia reticulata) are known to interact with Robofish in a similar way as with live conspecifics. Consequently, Robofish may serve as a conspecific-like leader that provides standardized behaviors irrespective of its size. We asked whether larger Robofish leaders are preferentially followed and whether the preferences of followers depend on own body size or risk-taking behavior (“boldness”). We found that live female guppies followed larger Robofish leaders in closer proximity than smaller ones and this pattern was independent of the followers’ own body size as well as risk-taking behavior. Our study shows a “bigger is better” pattern in leadership that is independent of behavioral differences among differentially-sized leaders, followers’ own size and risk-taking behavior.Peer Reviewe

Collecting eco-evolutionary data in the dark : Impediments to subterranean research and how to overcome them

Caves and other subterranean habitats fulfill the requirements of experimental model systems to address general questions in ecology and evolution. Yet, the harsh working conditions of these environments and the uniqueness of the subterranean organisms have challenged most attempts to pursuit standardized research. Two main obstacles have synergistically hampered previous attempts. First, there is a habitat impediment related to the objective difficulties of exploring subterranean habitats and our inability to access the network of fissures that represents the elective habitat for the so-called "cave species." Second, there is a biological impediment illustrated by the rarity of most subterranean species and their low physiological tolerance, often limiting sample size and complicating laboratory experiments. We explore the advantages and disadvantages of four general experimental setups (in situ, quasi in situ, ex situ, and in silico) in the light of habitat and biological impediments. We also discuss the potential of indirect approaches to research. Furthermore, using bibliometric data, we provide a quantitative overview of the model organisms that scientists have exploited in the study of subterranean life. Our over-arching goal is to promote caves as model systems where one can perform standardized scientific research. This is important not only to achieve an in-depth understanding of the functioning of subterranean ecosystems but also to fully exploit their long-discussed potential in addressing general scientific questions with implications beyond the boundaries of this discipline.Peer reviewe

After 150 years of watching: is there a need for synthetic ethology?

The Darwinian idea of mental continuity is about 150 years old. Although nobody has strongly denied this evolutionary link, both conceptually and practically, relative slow advance has been made by ethology and comparative psychology to quantify mental evolution. Debates on the mechanistic interpretation of cognition often struggle with the same old issues (e.g., associationism vs cognitivism), and in general, experimental methods have made also relative slow progress since the introduction of the puzzle box. In this paper, we illustrate the prevailing issues using examples on ‘mental state attribution’ and ‘perspective taking” and argue that the situation could be improved by the introduction of novel methodological inventions and insights. We suggest that focusing on problem-solving skills and constructing artificial agents that aim to correspond and interact with biological ones, may help to understand the functioning of the mind. We urge the establishment of a novel approach, synthetic ethology, in which researchers take on a practical stance and construct artificial embodied minds relying of specific computational architectures the performance of which can be compared directly to biological agents

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

Diurnal Changes in Hypoxia Shape Predator-Prey Interaction in a Bird-Fish System

Animals often face changing environments, and behavioral flexibility allows them to rapidly and adaptively respond to abiotic factors that vary more or less regularly. However, abiotic factors that affect prey species do not necessarily affect their predators. Still, the prey’s response might affect the predator indirectly, yet evidence from the wild for such a classical bottom-up effect of abiotic factors shaping several trophic levels remains sparse. In many aquatic environments, daily changes in oxygen concentrations occur frequently. When oxygen levels drop to hypoxic levels, many fishes respond with aquatic surface respiration (ASR), during which they obtain oxygen by skimming the upper, oxygenated surface layer. By increasing time at the surface, fish become more vulnerable to fish-eating birds. We explored these cascading effects in a sulfidic spring system that harbors the endemic sulphur molly (Poecilia sulphuraria) as prey species and several fish-eating bird species. Sulfide-rich springs pose harsh conditions as hydrogen sulfide (H2S) is lethal to most metazoans and reduces dissolved oxygen (DO). Field sampling during three daytimes indicated that water temperatures rose from morning to (after)noon, resulting in the already low DO levels to decrease further, while H2S levels showed no diurnal changes. The drop in DO levels was associated with a decrease in time spent diving in sulphur mollies, which corresponded with an increase in ASR. Interestingly, the laboratory-estimated threshold at which the majority of sulphur mollies initiate ASR (ASR50: <1.7 mg/L DO) was independent of temperature and this value was exceeded daily when hypoxic stress became more severe toward noon. As fish performed ASR, large aggregations built up at the water surface over the course of the day. As a possible consequence of fish spending more time at the surface, we found high activity levels of fish-eating birds at noon and in the afternoon. Our study reveals that daily fluctuations in water’s oxygen levels have the potential to alter predator-prey interactions profoundly and thus highlights the joined actions of abiotic and biotic factors shaping the evolution of a prey species.Peer Reviewe

Zebrafish Adjust Their Behavior in Response to an Interactive Robotic Predator

Zebrafish (Danio rerio) constitutes a valuable experimental species for the study of the biological determinants of emotional responses, such as fear and anxiety. Fear-related test paradigms traditionally entail the interaction between focal subjects and live predators, which may show inconsistent behavior throughout the experiment. To address this technical challenge, robotic stimuli are now frequently integrated in behavioral studies, yielding repeatable, customizable, and controllable experimental conditions. While most of the research has focused on open-loop control where robotic stimuli are preprogrammed to execute a priori known actions, recent work has explored the possibility of two-way interactions between robotic stimuli and live subjects. Here, we demonstrate a “closed-loop control” system to investigate fear response of zebrafish in which the response of the robotic stimulus is determined in real-time through a finite-state Markov chain constructed from independent observations on the interactions between zebrafish and their predator. Specifically, we designed a 3D-printed robotic replica of the zebrafish allopatric predator red tiger Oscar fish (Astronotus ocellatus), instrumented to interact in real-time with live subjects. We investigated the role of closed-loop control in modulating fear response in zebrafish through the analysis of the focal fish ethogram and the information-theoretic quantification of the interaction between the subject and the replica. Our results indicate that closed-loop control elicits consistent fear response in zebrafish and that zebrafish quickly adjust their behavior to avoid the predator's attacks. The augmented degree of interactivity afforded by the Markov-chain-dependent actuation of the replica constitutes a fundamental advancement in the study of animal-robot interactions and offers a new means for the development of experimental paradigms to study fear

Zebrafish Adjust Their Behavior in Response to an Interactive Robotic Predator

Zebrafish (Danio rerio) constitutes a valuable experimental species for the study of the biological determinants of emotional responses, such as fear and anxiety. Fear-related test paradigms traditionally entail the interaction between focal subjects and live predators, which may show inconsistent behavior throughout the experiment. To address this technical challenge, robotic stimuli are now frequently integrated in behavioral studies, yielding repeatable, customizable, and controllable experimental conditions. While most of the research has focused on open-loop control where robotic stimuli are preprogrammed to execute a priori known actions, recent work has explored the possibility of two-way interactions between robotic stimuli and live subjects. Here, we demonstrate a "closed-loop control" system to investigate fear response of zebrafish in which the response of the robotic stimulus is determined in real-time through a finite-state Markov chain constructed from independent observations on the interactions between zebrafish and their predator. Specifically, we designed a 3D-printed robotic replica of the zebrafish allopatric predator red tiger Oscar fish (Astronotus ocellatus), instrumented to interact in real-time with live subjects. We investigated the role of closed-loop control in modulating fear response in zebrafish through the analysis of the focal fish ethogram and the information-theoretic quantification of the interaction between the subject and the replica. Our results indicate that closed-loop control elicits consistent fear response in zebrafish and that zebrafish quickly adjust their behavior to avoid the predator's attacks. The augmented degree of interactivity afforded by the Markov-chain-dependent actuation of the replica constitutes a fundamental advancement in the study of animal-robot interactions and offers a new means for the development of experimental paradigms to study fear

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

Insights into the Social Behavior of Surface and Cave-Dwelling Fish (Poecilia mexicana) in Light and Darkness through the Use of a Biomimetic Robot

Biomimetic robots (BRs) are becoming more common in behavioral research and, if they are accepted as conspecifics, allow for new forms of experimental manipulations of social interactions. Nevertheless, it is often not clear which cues emanating from a BR are actually used as communicative signals and how species or populations with different sensory makeups react to specific types of BRs. We herein present results from experiments using two populations of livebearing fishes that differ in their sensory capabilities. In the South of Mexico, surface-dwelling mollies (Poecilia mexicana) successfully invaded caves and adapted to dark conditions. While almost without pigment, these cave mollies possess smaller but still functional eyes. Although previous studies found cave mollies to show reduced shoaling preferences with conspecifics in light compared to surface mollies, it is assumed that they possess specialized adaptations to maintain some kind of sociality also in their dark habitats. By testing surface- and cave-dwelling mollies with RoboFish, a BR made for use in laboratory experiments with guppies and sticklebacks, we asked to what extent visual and non-visual cues play a role in their social behavior. Both cave- and surface-dwelling mollies followed the BR as well as a live companion when tested in light. However, when tested in darkness, only surface-dwelling fish were attracted by a live conspecific, whereas cave-dwelling fish were not. Neither cave- nor surface-dwelling mollies were attracted to RoboFish in darkness. This is the first study to use BRs for the investigation of social behavior in mollies and to compare responses to BRs both in light and darkness. As our RoboFish is accepted as conspecific by both used populations of the Atlantic molly only under light conditions but not in darkness, we argue that our replica is providing mostly visual cues