How honeybees respond to heat stress from the individual to colony level.

A honey bee colony functions as an integrated collective, with individuals coordinating their behaviour to adapt and respond to unexpected disturbances. Nest homeostasis is critical for colony function; when ambient temperatures increase, individuals switch to thermoregulatory roles to cool the nest, such as fanning and water collection. While prior work has focused on bees engaged in specific behaviours, less is known about how responses are coordinated at the colony level, and how previous tasks predict behavioural changes during a heat stress. Using BeesBook automated tracking, we follow thousands of individuals during an experimentally induced heat stress, and analyse their behavioural changes from the individual to colony level. We show that heat stress causes an overall increase in activity levels and a spatial reorganization of bees away from the brood area. Using a generalized framework to analyse individual behaviour, we find that individuals differ in their response to heat stress, which depends on their prior behaviour and correlates with age. Examining the correlation of behavioural metrics over time suggests that heat stress perturbation does not have a long-lasting effect on an individual's future behaviour. These results demonstrate how thousands of individuals within a colony change their behaviour to achieve a coordinated response to an environmental disturbance.

Machine learning reveals the waggle drift's role in the honey bee dance communication system.

The honey bee waggle dance is one of the most prominent examples of abstract communication among animals: successful foragers convey new resource locations to interested followers via characteristic "dance" movements in the nest, where dances advertise different locations on different overlapping subregions of the "dance floor." To this day, this spatial separation has not been described in detail, and it remains unknown how it affects the dance communication. Here, we evaluate long-term recordings of Apis mellifera foraging at natural and artificial food sites. Using machine learning, we detect and decode waggle dances, and we individually identify and track dancers and dance followers in the hive and at artificial feeders. We record more than a hundred thousand waggle phases, and thousands of dances and dance-following interactions to quantitatively describe the spatial separation of dances on the dance floor. We find that the separation of dancers increases throughout a dance and present a motion model based on a positional drift of the dancer between subsequent waggle phases that fits our observations. We show that this separation affects follower bees as well and results in them more likely following subsequent dances to similar food source locations, constituting a positive feedback loop. Our work provides evidence that the positional drift between subsequent waggle phases modulates the information that is available to dance followers, leading to an emergent optimization of the waggle dance communication system.

Steering herds away from dangers in dynamic environments.

Shepherding, the task of guiding a herd of autonomous individuals in a desired direction, is an essential skill to herd animals, enable crowd control and rescue from danger. Equipping robots with the capability of shepherding would allow performing such tasks with increased efficiency and reduced labour costs. So far, only single-robot or centralized multi-robot solutions have been proposed. The former is unable to observe dangers at any place surrounding the herd, and the latter does not generalize to unconstrained environments. Therefore, we propose a decentralized control algorithm for multi-robot shepherding, where the robots maintain a caging pattern around the herd to detect potential nearby dangers. When danger is detected, part of the robot swarm positions itself in order to repel the herd towards a safer region. We study the performance of our algorithm for different collective motion models of the herd. We task the robots to shepherd a herd to safety in two dynamic scenarios: (i) to avoid dangerous patches appearing over time and (ii) to remain inside a safe circular enclosure. Simulations show that the robots are always successful in shepherding when the herd remains cohesive, and enough robots are deployed.

Social competence improves the performance of biomimetic robots leading live fish.

Collective motion is commonly modeled with static interaction rules between agents. Substantial empirical evidence indicates, however, that animals may adapt their interaction rules depending on a variety of factors and social contexts. Here, we hypothesized that leadership performance is linked to the leader's responsiveness to the follower's actions and we predicted that a leader is followed longer if it adapts to the follower's avoidance movements. We tested this prediction with live guppies that interacted with a biomimetic robotic fish programmed to act as a 'socially competent' leader. Fish that were avoiding the robot were approached more carefully in future approaches. In two separate experiments we then asked how the leadership performance of the socially competent robot leader differed to that of a robot leader that either approached all fish in the same, non-responsive, way or one that did change its approach behavior randomly, irrespective of the fish's actions. We found that (1) behavioral variability itself appears attractive and that socially competent robots are better leaders which (2) require fewer approach attempts to (3) elicit longer average following behavior than non-competent agents. This work provides evidence that social responsiveness to avoidance reactions plays a role in the social dynamics of guppies. We showcase how social responsiveness can be modeled and tested directly embedded in a living animal model using adaptive, interactive robots.

Live fish learn to anticipate the movement of a fish-like robot.

The ability of an individual to predict the outcome of the actions of others and to change their own behavior adaptively is called anticipation. There are many examples from mammalian species-including humans-that show anticipatory abilities in a social context, however, it is not clear to what extent fishes can anticipate the actions of their interaction partners or what the underlying mechanisms are for that anticipation. To answer these questions, we let live guppies (Poecilia reticulata) interact repeatedly with an open-loop (noninteractive) biomimetic robot that has previously been shown to be an accepted conspecific. The robot always performed the same zigzag trajectory in the experimental tank that ended in one of the corners, giving the live fish the opportunity to learn both the location of the final destination as well as the specific turning movement of the robot over three consecutive trials. The live fish's reactions were categorized into a global anticipation, which we defined as relative time to reach the robot's final corner, and a local anticipation which was the relative time and location of the live fish's turns relative to robofish turns. As a proxy for global anticipation, we found that live fish in the last trial reached the robot's destination corner significantly earlier than the robot. Overall, more than 50% of all fish arrived at the destination before the robot. This is more than a random walk model would predict and significantly more compared to all other equidistant, yet unvisited, corners. As a proxy for local anticipation, we found fish change their turning behavior in response to the robot over the course of the trials. Initially, the fish would turn after the robot, which was reversed in the end, as they began to turn slightly before the robot in the final trial. Our results indicate that live fish are able to anticipate predictably behaving social partners both in regard to final movement locations as well as movement dynamics. Given that fish have been found to exhibit consistent behavioral differences, anticipation in fish could have evolved as a mechanism to adapt to different social interaction partners.

Behavioral variation across the days and lives of honey bees.

In honey bee colonies, workers generally change tasks with age (from brood care, to nest work, to foraging). While these trends are well established, our understanding of how individuals distribute tasks during a day, and how individuals differ in their lifetime behavioral trajectories, is limited. Here, we use automated tracking to obtain long-term data on 4,100+ bees tracked continuously at 3 Hz, across an entire summer, and use behavioral metrics to compare behavior at different timescales. Considering single days, we describe how bees differ in space use, detection, and movement. Analyzing the behavior exhibited across their entire lives, we find consistent inter-individual differences in the movement characteristics of individuals. Bees also differ in how quickly they transition through behavioral space to ultimately become foragers, with fast-transitioning bees living the shortest lives. Our analysis framework provides a quantitative approach to describe individual behavioral variation within a colony from single days to entire lifetimes.

Fish waves as emergent collective antipredator behavior.

The collective behavior of animals has attracted considerable attention in recent years, with many studies exploring how local interactions between individuals can give rise to global group properties.1-3 The functional aspects of collective behavior are less well studied, especially in the field,4 and relatively few studies have investigated the adaptive benefits of collective behavior in situations where prey are attacked by predators.5,6 This paucity of studies is unsurprising because predator-prey interactions in the field are difficult to observe. Furthermore, the focus in recent studies on predator-prey interactions has been on the collective behavior of the prey7-10 rather than on the behavior of the predator (but see Ioannou et al.11 and Handegard et al.12). Here we present a field study that investigated the anti-predator benefits of waves produced by fish at the water surface when diving down collectively in response to attacks of avian predators. Fish engaged in surface waves that were highly conspicuous, repetitive, and rhythmic involving many thousands of individuals for up to 2 min. Experimentally induced fish waves doubled the time birds waited until their next attack, therefore substantially reducing attack frequency. In one avian predator, capture probability, too, decreased with wave number and birds switched perches in response to wave displays more often than in control treatments, suggesting that they directed their attacks elsewhere. Taken together, these results support an anti-predator function of fish waves. The attack delay could be a result of a confusion effect or a consequence of waves acting as a perception advertisement, which requires further exploration.

A Flying Platform to Investigate Neuronal Correlates of Navigation in the Honey Bee (Apis mellifera).

Navigating animals combine multiple perceptual faculties, learn during exploration, retrieve multi-facetted memory contents, and exhibit goal-directedness as an expression of their current needs and motivations. Navigation in insects has been linked to a variety of underlying strategies such as path integration, view familiarity, visual beaconing, and goal-directed orientation with respect to previously learned ground structures. Most works, however, study navigation either from a field perspective, analyzing purely behavioral observations, or combine computational models with neurophysiological evidence obtained from lab experiments. The honey bee (Apis mellifera) has long been a popular model in the search for neural correlates of complex behaviors and exhibits extraordinary navigational capabilities. However, the neural basis for bee navigation has not yet been explored under natural conditions. Here, we propose a novel methodology to record from the brain of a copter-mounted honey bee. This way, the animal experiences natural multimodal sensory inputs in a natural environment that is familiar to her. We have developed a miniaturized electrophysiology recording system which is able to record spikes in the presence of time-varying electric noise from the copter's motors and rotors, and devised an experimental procedure to record from mushroom body extrinsic neurons (MBENs). We analyze the resulting electrophysiological data combined with a reconstruction of the animal's visual perception and find that the neural activity of MBENs is linked to sharp turns, possibly related to the relative motion of visual features. This method is a significant technological step toward recording brain activity of navigating honey bees under natural conditions. By providing all system specifications in an online repository, we hope to close a methodological gap and stimulate further research informing future computational models of insect navigation.

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.

Social networks predict the life and death of honey bees.

In complex societies, individuals' roles are reflected by interactions with other conspecifics. Honey bees (Apis mellifera) generally change tasks as they age, but developmental trajectories of individuals can vary drastically due to physiological and environmental factors. We introduce a succinct descriptor of an individual's social network that can be obtained without interfering with the colony. This 'network age' accurately predicts task allocation, survival, activity patterns, and future behavior. We analyze developmental trajectories of multiple cohorts of individuals in a natural setting and identify distinct developmental pathways and critical life changes. Our findings suggest a high stability in task allocation on an individual level. We show that our method is versatile and can extract different properties from social networks, opening up a broad range of future studies. Our approach highlights the relationship of social interactions and individual traits, and provides a scalable technique for understanding how complex social systems function.

Group-level patterns emerge from individual speed as revealed by an extremely social robotic fish.

Understanding the emergence of collective behaviour has long been a key research focus in the natural sciences. Besides the fundamental role of social interaction rules, a combination of theoretical and empirical work indicates individual speed may be a key process that drives the collective behaviour of animal groups. Socially induced changes in speed by interacting animals make it difficult to isolate the effects of individual speed on group-level behaviours. Here, we tackled this issue by pairing guppies with a biomimetic robot. We used a closed-loop tracking and feedback system to let a robotic fish naturally interact with a live partner in real time, and programmed it to strongly copy and follow its partner's movements while lacking any preferred movement speed or directionality of its own. We show that individual differences in guppies' movement speed were highly repeatable and in turn shaped key collective patterns: a higher individual speed resulted in stronger leadership, lower cohesion, higher alignment and better temporal coordination of the pairs. By combining the strengths of individual-based models and observational work with state-of-the-art robotics, we provide novel evidence that individual speed is a key, fundamental process in the emergence of collective behaviour.

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.

Using a robotic fish to investigate individual differences in social responsiveness in the guppy.

Responding towards the actions of others is one of the most important behavioural traits whenever animals of the same species interact. Mutual influences among interacting individuals may modulate the social responsiveness seen and thus make it often difficult to study the level and individual variation in responsiveness. Here, open-loop biomimetic robots that provide standardized, non-interactive social cues can be a useful tool. These robots are not affected by the live animal's actions but are assumed to still represent valuable and biologically relevant social cues. As this assumption is crucial for the use of biomimetic robots in behavioural studies, we hypothesized (i) that meaningful social interactions can be assumed if live animals maintain individual differences in responsiveness when interacting with both a biomimetic robot and a live partner. Furthermore, to study the level of individual variation in social responsiveness, we hypothesized (ii) that individual differences should be maintained over the course of multiple tests with the robot. We investigated the response of live guppies (Poecilia reticulata) when allowed to interact either with a biomimetic open-loop-controlled fish robot-'Robofish'-or with a live companion. Furthermore, we investigated the responses of live guppies when tested three times with Robofish. We found that responses of live guppies towards Robofish were weaker compared with those of a live companion, most likely as a result of the non-interactive open-loop behaviour of Robofish. Guppies, however, were consistent in their individual responses between a live companion and Robofish, and similar individual differences in response towards Robofish were maintained over repeated testing even though habituation to the test environment was detectable. Biomimetic robots like Robofish are therefore a useful tool for the study of social responsiveness in guppies and possibly other small fish species.

Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish.

Mormyrid weakly electric fish produce electric organ discharges (EODs) for active electrolocation and electrocommunication. These pulses are emitted with variable interdischarge intervals (IDIs) resulting in temporal discharge patterns and interactive signaling episodes with nearby conspecifics. However, unequivocal assignment of interactive signaling to a specific behavioral context has proven to be challenging. Using an ethorobotical approach, we confronted single individuals of weakly electric Mormyrus rume proboscirostris with a mobile fish robot capable of interacting both physically, on arbitrary trajectories, as well as electrically, by generating echo responses through playback of species-specific EODs, thus synchronizing signals with the fish. Interactive signaling by the fish was more pronounced in response to a dynamic echo playback generated by the robot than in response to playback of static random IDI sequences. Such synchronizations were particularly strong at a distance corresponding to the outer limit of active electrolocation, and when fish oriented toward the fish replica. We therefore argue that interactive signaling through echoing of a conspecific's EODs provides a simple mechanism by which weakly electric fish can specifically address nearby individuals during electrocommunication. Echoing may thus enable mormyrids to mutually allocate social attention and constitute a foundation for complex social behavior and relatively advanced cognitive abilities in a basal vertebrate lineage.

Guidance of Navigating Honeybees by Learned Elongated Ground Structures.

Elongated landscape features like forest edges, rivers, roads or boundaries of fields are particularly salient landmarks for navigating animals. Here, we ask how honeybees learn such structures and how they are used during their homing flights after being released at an unexpected location (catch-and-release paradigm). The experiments were performed in two landscapes that differed with respect to their overall structure: a rather feature-less landscape, and one rich in close and far distant landmarks. We tested three different forms of learning: learning during orientation flights, learning during training to a feeding site, and learning during homing flights after release at an unexpected site within the explored area. We found that bees use elongated ground structures, e.g., a field boundary separating two pastures close to the hive (Experiment 1), an irrigation channel (Experiment 2), a hedgerow along which the bees were trained (Experiment 3), a gravel road close to the hive and the feeder (Experiment 4), a path along an irrigation channel with its vegetation close to the feeder (Experiment 5) and a gravel road along which bees performed their homing flights (Experiment 6). Discrimination and generalization between the learned linear landmarks and similar ones in the test area depend on their object properties (irrigation channel, gravel road, hedgerow) and their compass orientation. We conclude that elongated ground structures are embedded into multiple landscape features indicating that memory of these linear structures is one component of bee navigation. Elongated structures interact and compete with other references. Object identification is an important part of this process. The objects are characterized not only by their appearance but also by their alignment in the compass. Their salience is highest if both components are close to what had been learned. High similarity in appearance can compensate for (partial) compass misalignment, and vice versa.

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.

Tracking All Members of a Honey Bee Colony Over Their Lifetime Using Learned Models of Correspondence.

Computational approaches to the analysis of collective behavior in social insects increasingly rely on motion paths as an intermediate data layer from which one can infer individual behaviors or social interactions. Honey bees are a popular model for learning and memory. Previous experience has been shown to affect and modulate future social interactions. So far, no lifetime history observations have been reported for all bees of a colony. In a previous work we introduced a recording setup customized to track up to 4,000 marked bees over several weeks. Due to detection and decoding errors of the bee markers, linking the correct correspondences through time is non-trivial. In this contribution we present an in-depth description of the underlying multi-step algorithm which produces motion paths, and also improves the marker decoding accuracy significantly. The proposed solution employs two classifiers to predict the correspondence of two consecutive detections in the first step, and two tracklets in the second. We automatically tracked ~2,000 marked honey bees over 10 weeks with inexpensive recording hardware using markers without any error correction bits. We found that the proposed two-step tracking reduced incorrect ID decodings from initially ~13% to around 2% post-tracking. Alongside this paper, we publish the first trajectory dataset for all bees in a colony, extracted from ~3 million images covering 3 days. We invite researchers to join the collective scientific effort to investigate this intriguing animal system. All components of our system are open-source.

RenderGAN: Generating Realistic Labeled Data.

Deep Convolutional Neuronal Networks (DCNNs) are showing remarkable performance on many computer vision tasks. Due to their large parameter space, they require many labeled samples when trained in a supervised setting. The costs of annotating data manually can render the use of DCNNs infeasible. We present a novel framework called RenderGAN that can generate large amounts of realistic, labeled images by combining a 3D model and the Generative Adversarial Network framework. In our approach, image augmentations (e.g., lighting, background, and detail) are learned from unlabeled data such that the generated images are strikingly realistic while preserving the labels known from the 3D model. We apply the RenderGAN framework to generate images of barcode-like markers that are attached to honeybees. Training a DCNN on data generated by the RenderGAN yields considerably better performance than training it on various baselines.

A neural network model for familiarity and context learning during honeybee foraging flights.

How complex is the memory structure that honeybees use to navigate? Recently, an insect-inspired parsimonious spiking neural network model was proposed that enabled simulated ground-moving agents to follow learned routes. We adapted this model to flying insects and evaluate the route following performance in three different worlds with gradually decreasing object density. In addition, we propose an extension to the model to enable the model to associate sensory input with a behavioral context, such as foraging or homing. The spiking neural network model makes use of a sparse stimulus representation in the mushroom body and reward-based synaptic plasticity at its output synapses. In our experiments, simulated bees were able to navigate correctly even when panoramic cues were missing. The context extension we propose enabled agents to successfully discriminate partly overlapping routes. The structure of the visual environment, however, crucially determines the success rate. We find that the model fails more often in visually rich environments due to the overlap of features represented by the Kenyon cell layer. Reducing the landmark density improves the agents route following performance. In very sparse environments, we find that extended landmarks, such as roads or field edges, may help the agent stay on its route, but often act as strong distractors yielding poor route following performance. We conclude that the presented model is valid for simple route following tasks and may represent one component of insect navigation. Additional components might still be necessary for guidance and action selection while navigating along different memorized routes in complex natural environments.

Automatic detection and decoding of honey bee waggle dances.

The waggle dance is one of the most popular examples of animal communication. Forager bees direct their nestmates to profitable resources via a complex motor display. Essentially, the dance encodes the polar coordinates to the resource in the field. Unemployed foragers follow the dancer's movements and then search for the advertised spots in the field. Throughout the last decades, biologists have employed different techniques to measure key characteristics of the waggle dance and decode the information it conveys. Early techniques involved the use of protractors and stopwatches to measure the dance orientation and duration directly from the observation hive. Recent approaches employ digital video recordings and manual measurements on screen. However, manual approaches are very time-consuming. Most studies, therefore, regard only small numbers of animals in short periods of time. We have developed a system capable of automatically detecting, decoding and mapping communication dances in real-time. In this paper, we describe our recording setup, the image processing steps performed for dance detection and decoding and an algorithm to map dances to the field. The proposed system performs with a detection accuracy of 90.07%. The decoded waggle orientation has an average error of -2.92° (± 7.37°), well within the range of human error. To evaluate and exemplify the system's performance, a group of bees was trained to an artificial feeder, and all dances in the colony were automatically detected, decoded and mapped. The system presented here is the first of this kind made publicly available, including source code and hardware specifications. We hope this will foster quantitative analyses of the honey bee waggle dance.