Animal-robot interaction-an emerging field at the intersection of biology and robotics.

The field of animal-robot and organism-robot interaction systems (ARIS, ORIS) is a currently rapidly emerging field in biorobotics. In this special issue we aim for providing a comprehensive overview of the cutting-edge advancements and pioneering breakthroughs within this scientific and engineering discipline. Therefore, we collected scientific articles that delineate and expound upon the complexity of these remarkable biohybrid systems. These configurations stand as engineered conduits, facilitating the accurate investigation and profound exploration of the multifaceted interactions between robotic devices and biological entities, including various fish species, honeybees and plants. Also the human factor plays a role in this collection, as we also include a philosophical perspective on such systems as well as an augmented reality setup that brings humans into the loop with living fish. Within our editorial purview, we categorize the scientific contributions based on their focal points, differentiating between examinations of singular agent-to-agent interactions, extensions to the social stratum, and further expansions to the intricate levels of swarm dynamics, colonies, populations, and ecosystems. Considering potential applications, we delve into the multifaceted domains wherein these biohybrid systems might be applied. This discourse culminates in a tentative glimpse into the future trajectories these technologies might traverse, elucidating their promising prospects for both scientific advancement and societal enrichment. In sum, this special issue aims at facilitating the convergence of diverse insights, at encapsulating the richness of the ARIS and ORIS domain, and at charting a course toward the untapped prospects lying at the nexus of biology and robotics.

Daphnia's phototaxis as an indicator in ecotoxicological studies: A review.

Animal-based sensors have been increasingly applied to many water monitoring systems and ecological studies. One of the staple organisms used as living sensors for such systems is Daphnia. This organism has been extensively studied and, with time, used in many toxicological and pharmaceutical bioassays, often used for exploring the ecology of freshwater communities. One of its behaviours used for evaluating the state of the aquatic environment is phototaxis. A disruption in the predicted behaviour is interpreted as a sign of stress and forms the basis for further investigation. However, phototaxis is a result of complex processes counteracting and interacting with each other. Predator presence, food quality, body pigmentation and other factors can greatly affect the predicted phototactic response, hampering its reliability as a bioindicator. Therefore, a holistic approach and meticulous documentation of the methods are needed for the correct interpretation of this behavioural indicator. In this review, we present the current methods used for studying phototaxis, the factors affecting it and proposed ways to optimise the reliability of the results.

Organisms as sensors in biohybrid entities as a novel tool for in-field aquatic monitoring.

Rapidly intensifying global warming and water pollution calls for more efficient and continuous environmental monitoring methods. Biohybrid systems connect mechatronic components to living organisms and this approach can be used to extract data from the organisms. Compared to conventional monitoring methods, they allow for a broader data collection over long periods, minimizing the need for sampling processes and human labour. We aim to develop a methodology for creating various bioinspired entities, here referred to as 'biohybrids', designed for long-term aquatic monitoring. Here, we test several aspects of the development of the biohybrid entity: autonomous power source, lifeform integration and partial biodegradability. An autonomous power source was supplied by microbial fuel cells which exploit electron flows from microbial metabolic processes in the sediments. Here, we show that by stacking multiple cells, sufficient power can be supplied. We integrated lifeforms into the developed bioinspired entity which includes organisms such as the zebra musselDreissena polymorphaand water fleaDaphniaspp. The setups developed allowed for observing their stress behaviours. Through this, we can monitor changes in the environment in a continuous manner. The further development of this approach will allow for extensive, long-term aquatic data collection and create an early-warning monitoring system.

Self-complexification through integral feedback in eusocial paper wasps of various levels of sociality.

We investigate how simple physical interactions can generate remarkable diversity in the life history of social agents using data of social wasps, yielding complex scalable task partitioning. We built and analyzed a computational model to investigate how diverse task allocation patterns found in nature can emerge from the same behavioral blueprint. Self-organizing mechanisms of interwoven behavioral feedback loops, task-dependent time delays and simple material flows between interacting individuals yield an emergent homeostatic self-regulation while keeping the global colony performance scalable. Task allocation mechanisms based on implicitly honest signaling via material flows are not only very robust but are also highly evolvable due to their simplicity and reliability. We find that task partitioning has evolved to be scalable and adaptable to life history traits, such as expected colony size or temporal bottlenecks in the available workforce or materials. By tuning solely the total number of agents and a social connectivity-related parameter in the model, our simulations yield the whole range of emergent patterns in task allocation and task fidelity akin to observed field data. Our model suggests that the material exchange ("common stomach mechanism") found in many paper wasps provides a common functional "core" across these genera, which not only provides self-regulation of the colony, but also provides a scalable mechanism allowing natural selection to yield complex social integration in larger colonies over the course of their evolutionary trajectory.

Will biomimetic robots be able to change a hivemind to guide honeybees' ecosystem services?

We study whether or not a group of biomimetic waggle dancing robots is able to significantly influence the swarm-intelligent decision making of a honeybee colony, e.g. to avoid foraging at dangerous food patches using a mathematical model. Our model was successfully validated against data from two empirical experiments: one examined the selection of foraging targets and the other cross inhibition between foraging targets. We found that such biomimetic robots have a significant effect on a honeybee colony's foraging decision. This effect correlates with the number of applied robots up to several dozens of robots and then saturates quickly with higher robot numbers. These robots can reallocate the bees' pollination service in a directed way towards desired locations or boost it at specific locations, without having a significant negative effect on the colony's nectar economy. Additionally, we found that such robots may be able to lower the influx of toxic substances from potentially harmful foraging sites by guiding the bees to alternative places. These effects also depend on the saturation level of the colony's nectar stores. The more nectar is already stored in the colony, the easier the bees are guided by the robots to alternative foraging targets. Our study shows that biomimetic and socially immersive biomimetic robots are a relevant future research target in order to support (a) the bees by guiding them to safe (pesticide free) places, (b) the ecosystem via boosted and directed pollination services and (c) human society by supporting agricultural crop pollination, thus increasing our food security this way.

A robotic honeycomb for interaction with a honeybee colony.

Robotic technologies have shown the capability to interact with living organisms and even to form integrated mixed societies composed of living and artificial agents. Biocompatible robots, incorporating sensing and actuation capable of generating and responding to relevant stimuli, can be a tool to study collective behaviors previously unattainable with traditional techniques. To investigate collective behaviors of the western honeybee (Apis mellifera), we designed a robotic system capable of observing and modulating the bee cluster using an array of thermal sensors and actuators. We initially integrated the system into a beehive populated with about 4000 bees for several months. The robotic system was able to observe the colony by continuously collecting spatiotemporal thermal profiles of the winter cluster. Furthermore, we found that our robotic device reliably modulated the superorganism's response to dynamic thermal stimulation, influencing its spatiotemporal reorganization. In addition, after identifying the thermal collapse of a colony, we used the robotic system in a "life-support" mode via its thermal actuators. Ultimately, we demonstrated a robotic device capable of autonomous closed-loop interaction with a cluster comprising thousands of individual bees. Such biohybrid societies open the door to investigation of collective behaviors that necessitate observing and interacting with the animals within a complete social context, as well as for potential applications in augmenting the survivability of these pollinators crucial to our ecosystems and our food supply.

Improving the Accuracy of a Biohybrid for Environmental Monitoring.

Environmental monitoring should be minimally disruptive to the ecosystems that it is embedded in. Therefore, the project Robocoenosis suggests using biohybrids that blend into ecosystems and use life forms as sensors. However, such a biohybrid has limitations regarding memory-as well as power-capacities, and can only sample a limited number of organisms. We model the biohybrid and study the degree of accuracy that can be achieved by using a limited sample. Importantly, we consider potential misclassification errors (false positives and false negatives) that lower accuracy. We suggest the method of using two algorithms and pooling their estimations as a possible way of increasing the accuracy of the biohybrid. We show in simulation that a biohybrid could improve the accuracy of its diagnosis by doing so. The model suggests that for the estimation of the population rate of spinning Daphnia, two suboptimal algorithms for spinning detection outperform one qualitatively better algorithm. Further, the method of combining two estimations reduces the number of false negatives reported by the biohybrid, which we consider important in the context of detecting environmental catastrophes. Our method could improve environmental modeling in and outside of projects such as Robocoenosis and may find use in other fields.

Mycelial Beehives of HIVEOPOLIS: Designing and Building Therapeutic Inner Nest Environments for Honeybees.

The perceptions and definitions of healthy indoor environments have changed significantly throughout architectural history. Today, molecular biology teaches us that microbes play important roles in human health, and that isolation from them puts not only us but also other inhabitants of urban landscapes, at risk. In order to provide an environment that makes honeybees more resilient to environmental changes, we aim for combining the thermal insulation functionality of mycelium materials with bioactive therapeutic properties within beehive constructions. By identifying mycelial fungi's interactions with nest-related materials, using digital methods to design a hive structure, and engaging in additive manufacturing, we were able to develop a set of methods for designing and fabricating a fully grown hive. We propose two digital methods for modelling 3D scaffolds for micro-super organism co-occupation scenarios: "variable-offset" and "iterative-subtraction", followed by two inoculation methods for the biofabrication of scaffolded fungal composites. The HIVEOPOLIS project aims to diversify and complexify urban ecological niches to make them more resilient to future game changers such as climate change. The combined functions of mycelium materials have the potential to provide a therapeutic environment for honeybees and, potentially, humans in the future.

A Minimally Invasive Approach Towards "Ecosystem Hacking" With Honeybees.

Honey bees live in colonies of thousands of individuals, that not only need to collaborate with each other but also to interact intensively with their ecosystem. A small group of robots operating in a honey bee colony and interacting with the queen bee, a central colony element, has the potential to change the collective behavior of the entire colony and thus also improve its interaction with the surrounding ecosystem. Such a system can be used to study and understand many elements of bee behavior within hives that have not been adequately researched. We discuss here the applicability of this technology for ecosystem protection: A novel paradigm of a minimally invasive form of conservation through "Ecosystem Hacking". We discuss the necessary requirements for such technology and show experimental data on the dynamics of the natural queen's court, initial designs of biomimetic robotic surrogates of court bees, and a multi-agent model of the queen bee court system. Our model is intended to serve as an AI-enhanceable coordination software for future robotic court bee surrogates and as a hardware controller for generating nature-like behavior patterns for such a robotic ensemble. It is the first step towards a team of robots working in a bio-compatible way to study honey bees and to increase their pollination performance, thus achieving a stabilizing effect at the ecosystem level.

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".

Social Integrating Robots Suggest Mitigation Strategies for Ecosystem Decay.

We develop here a novel hypothesis that may generate a general research framework of how autonomous robots may act as a future contingency to counteract the ongoing ecological mass extinction process. We showcase several research projects that have undertaken first steps to generate the required prerequisites for such a technology-based conservation biology approach. Our main idea is to stabilise and support broken ecosystems by introducing artificial members, robots, that are able to blend into the ecosystem's regulatory feedback loops and can modulate natural organisms' local densities through participation in those feedback loops. These robots are able to inject information that can be gathered using technology and to help the system in processing available information with technology. In order to understand the key principles of how these robots are capable of modulating the behaviour of large populations of living organisms based on interacting with just a few individuals, we develop novel mathematical models that focus on important behavioural feedback loops. These loops produce relevant group-level effects, allowing for robotic modulation of collective decision making in social organisms. A general understanding of such systems through mathematical models is necessary for designing future organism-interacting robots in an informed and structured way, which maximises the desired output from a minimum of intervention. Such models also help to unveil the commonalities and specificities of the individual implementations and allow predicting the outcomes of microscopic behavioural mechanisms on the ultimate macroscopic-level effects. We found that very similar models of interaction can be successfully used in multiple very different organism groups and behaviour types (honeybee aggregation, fish shoaling, and plant growth). Here we also report experimental data from biohybrid systems of robots and living organisms. Our mathematical models serve as building blocks for a deep understanding of these biohybrid systems. Only if the effects of autonomous robots onto the environment can be sufficiently well predicted can such robotic systems leave the safe space of the lab and can be applied in the wild to be able to unfold their ecosystem-stabilising potential.

A swarm design paradigm unifying swarm behaviors using minimalistic communication.

Numerous nature inspired algorithms have been suggested to enable robotic swarms, mobile sensor networks and other multi-agent systems to exhibit various self-organized behaviors. Swarm intelligence and swarm robotics research have been underway for a few decades and have produced many such algorithms based on natural self-organizing systems. While a large body of research exists for variations and modifications in swarm intelligence algorithms, there have been few attempts to unify the underlying agent level design of these widely varying behaviors. In this work, a design paradigm for a swarm of agents is presented which can exhibit a wide range of collective behaviors at swarm level while using minimalistic single-bit communication at the agent level. The communication in the proposed paradigm is based on waves of 'ping'-signals inspired by strategies for communication and self organization of slime mold (Dictyostelium discoideum) and fireflies (lampyridae). The unification of common collective behaviors through this Wave Oriented Swarm Paradigm (WOSP) enables the control of swarms with minimalistic communication and yet allowing the emergence of diverse complex behaviors. It is demonstrated both in simulation and using real robotic experiments that even a single-bit communication channel between agents suffices for the design of a substantial set of behaviors. Ultimately, the reader will be enabled to combine different behaviours based on the paradigm to develop a control scheme for individual swarms.

Constructing living buildings: a review of relevant technologies for a novel application of biohybrid robotics.

Biohybrid robotics takes an engineering approach to the expansion and exploitation of biological behaviours for application to automated tasks. Here, we identify the construction of living buildings and infrastructure as a high-potential application domain for biohybrid robotics, and review technological advances relevant to its future development. Construction, civil infrastructure maintenance and building occupancy in the last decades have comprised a major portion of economic production, energy consumption and carbon emissions. Integrating biological organisms into automated construction tasks and permanent building components therefore has high potential for impact. Live materials can provide several advantages over standard synthetic construction materials, including self-repair of damage, increase rather than degradation of structural performance over time, resilience to corrosive environments, support of biodiversity, and mitigation of urban heat islands. Here, we review relevant technologies, which are currently disparate. They span robotics, self-organizing systems, artificial life, construction automation, structural engineering, architecture, bioengineering, biomaterials, and molecular and cellular biology. In these disciplines, developments relevant to biohybrid construction and living buildings are in the early stages, and typically are not exchanged between disciplines. We, therefore, consider this review useful to the future development of biohybrid engineering for this highly interdisciplinary application.

Robotic Sensing and Stimuli Provision for Guided Plant Growth.

Robot systems are actively researched for manipulation of natural plants, typically restricted to agricultural automation activities such as harvest, irrigation, and mechanical weed control. Extending this research, we introduce here a novel methodology to manipulate the directional growth of plants via their natural mechanisms for signaling and hormone distribution. An effective methodology of robotic stimuli provision can open up possibilities for new experimentation with later developmental phases in plants, or for new biotechnology applications such as shaping plants for green walls. Interaction with plants presents several robotic challenges, including short-range sensing of small and variable plant organs, and the controlled actuation of plant responses that are impacted by the environment in addition to the provided stimuli. In order to steer plant growth, we develop a group of immobile robots with sensors to detect the proximity of growing tips, and with diodes to provide light stimuli that actuate phototropism. The robots are tested with the climbing common bean, Phaseolus vulgaris, in experiments having durations up to five weeks in a controlled environment. With robots sequentially emitting blue light-peak emission at wavelength 465 nm-plant growth is successfully steered through successive binary decisions along mechanical supports to reach target positions. Growth patterns are tested in a setup up to 180 cm in height, with plant stems grown up to roughly 250 cm in cumulative length over a period of approximately seven weeks. The robots coordinate themselves and operate fully autonomously. They detect approaching plant tips by infrared proximity sensors and communicate via radio to switch between blue light stimuli and dormant status, as required. Overall, the obtained results support the effectiveness of combining robot and plant experiment methodologies, for the study of potentially complex interactions between natural and engineered autonomous systems.

Collective Motion as an Ultimate Effect in Crowded Selfish Herds.

The selfish herd hypothesis explains how social prey can assemble cohesive groups for maximising individual fitness. However, previous models often abstracted away the physical manifestation of the focal animals such that the influence of getting stuck in a crowded herd on individual adaptation was less intensively investigated. Here, we propose an evolutionary model to simulate the adaptation of egoistic social prey to predation given that individual mobility is strictly restrained by the presence of other conspecifics. In our simulated evolutionary races, agents were set to either be confined by neighbours or move to empty cells on the lattice, and the behavioural traits of those less exposed were selected and inherited. Our analyses show that under this crowded environment, cohesive and steady herds were consistently replaced by morphing and moving aggregates via the attempt of border agents to share predation risk with the inner members. This kind of collective motion emerges purely from the competition among selfish individuals regardless of any group benefit. Our findings reveal that including the crowding effect with the selfish herd scenario permits additional diversity in the predicted outcomes and imply that a wider set of collective animal behaviours are explainable purely by individual-level selection.

Correction: Resilience of honeybee colonies via common stomach: A model of self-regulation of foraging.

[This corrects the article DOI: 10.1371/journal.pone.0188004.].

Robots mediating interactions between animals for interspecies collective behaviors.

Self-organized collective behavior has been analyzed in diverse types of gregarious animals. Such collective intelligence emerges from the synergy between individuals, which behave at their own time and spatial scales and without global rules. Recently, robots have been developed to collaborate with animal groups in the pursuit of better understanding their decision-making processes. These biohybrid systems make cooperative relationships between artificial systems and animals possible, which can yield new capabilities in the resulting mixed group. However, robots are currently tailor-made to successfully engage with one animal species at a time. This limits the possibilities of introducing distinct species-dependent perceptual capabilities and types of behaviors in the same system. Here, we show that robots socially integrated into animal groups of honeybees and zebrafish, each one located in a different city, allowing these two species to interact. This interspecific information transfer is demonstrated by collective decisions that emerge between the two autonomous robotic systems and the two animal groups. The robots enable this biohybrid system to function at any distance and operates in water and air with multiple sensorimotor properties across species barriers and ecosystems. These results demonstrate the feasibility of generating and controlling behavioral patterns in biohybrid groups of multiple species. Such interspecies connections between diverse robotic systems and animal species may open the door for new forms of artificial collective intelligence, where the unrivaled perceptual capabilities of the animals and their brains can be used to enhance autonomous decision-making, which could find applications in selective "rewiring" of ecosystems.

Integral feedback control is at the core of task allocation and resilience of insect societies.

Homeostatic self-regulation is a fundamental aspect of open dissipative systems. Integral feedback has been found to be important for homeostatic control on both the cellular and molecular levels of biological organization and in engineered systems. Analyzing the task allocation mechanisms of three insect societies, we identified a model of integral control residing at colony level. We characterized a general functional core mechanism, called the "common stomach," where a crucial shared substance for colony function self-regulates its own quantity via reallocating the colony's workforce, which collects and uses this substance. The central component in a redundant feedback network is the saturation level of this substance in the colony. An interaction network of positive and negative feedback loops ensures the homeostatic state of this substance and the workforce involved in processing this substance. Extensive sensitivity and stability analyses of the core model revealed that the system is very resilient against perturbations and compensates for specific types of stress that real colonies face in their ecosystems. The core regulation system is highly scalable, and due to its buffer function, it can filter noise and find a new equilibrium quickly after environmental (supply) or colony-state (demand) changes. The common stomach regulation system is an example of convergent evolution among the three different societies, and we predict that similar integral control regulation mechanisms have evolved frequently within natural complex systems.

Autonomously shaping natural climbing plants: a bio-hybrid approach.

Plant growth is a self-organized process incorporating distributed sensing, internal communication and morphology dynamics. We develop a distributed mechatronic system that autonomously interacts with natural climbing plants, steering their behaviours to grow user-defined shapes and patterns. Investigating this bio-hybrid system paves the way towards the development of living adaptive structures and grown building components. In this new application domain, challenges include sensing, actuation and the combination of engineering methods and natural plants in the experimental set-up. By triggering behavioural responses in the plants through light spectra stimuli, we use static mechatronic nodes to grow climbing plants in a user-defined pattern at a two-dimensional plane. The experiments show successful growth over periods up to eight weeks. Results of the stimuli-guided experiments are substantially different from the control experiments. Key limitations are the number of repetitions performed and the scale of the systems tested. Recommended future research would investigate the use of similar bio-hybrids to connect construction elements and grow shapes of larger size.

Resilience of honeybee colonies via common stomach: A model of self-regulation of foraging.

We propose a new regulation mechanism based on the idea of the "common stomach" to explain several aspects of the resilience and homeostatic regulation of honeybee colonies. This mechanism exploits shared pools of substances (pollen, nectar, workers, brood) that modulate recruitment, abandonment and allocation patterns at the colony-level and enable bees to perform several survival strategies to cope with difficult circumstances: Lack of proteins leads to reduced feeding of young brood, to early capping of old brood and to regaining of already spent proteins through brood cannibalism. We modeled this system by linear interaction terms and mass-action law. To test the predictive power of the model of this regulatory mechanism we compared our model predictions to experimental data of several studies. These comparisons show that the proposed regulation mechanism can explain a variety of colony level behaviors. Detailed analysis of the model revealed that these mechanisms could explain the resilience, stability and self-regulation observed in honeybee colonies. We found that manipulation of material flow and applying sudden perturbations to colony stocks are quickly compensated by a resulting counter-acting shift in task selection. Selective analysis of feedback loops allowed us to discriminate the importance of different feedback loops in self-regulation of honeybee colonies. We stress that a network of simple proximate mechanisms can explain significant colony-level abilities that can also be seen as ultimate reasoning of the evolutionary trajectory of honeybees.