The Bayesian superorganism: externalized memories facilitate distributed sampling.

A key challenge for any animal (or sampling technique) is to avoid wasting time by searching for resources (information) in places already found to be unprofitable. In biology, this challenge is particularly strong when the organism is a central place forager-returning to a nest between foraging bouts-because it is destined repeatedly to cover much the same ground. This problem will be particularly acute if many individuals forage from the same central place, as in social insects such as the ants. Foraging (sampling) performance may be greatly enhanced by coordinating movement trajectories such that each ant (walker) visits separate parts of the surrounding (unknown) space. We find experimental evidence for an externalized spatial memory in Temnothorax albipennis ants: chemical markers (either pheromones or cues such as cuticular hydrocarbon footprints) that are used by nest-mates to mark explored space. We show these markers could be used by the ants to scout the space surrounding their nest more efficiently through indirect coordination. We also develop a simple model of this marking behaviour that can be applied in the context of Markov chain Monte Carlo methods (Baddeley et al. 2019 J. R. Soc. Interface16, 20190162 (doi:10.1098/rsif.2019.0162)). This substantially enhances the performance of standard methods like the Metropolis-Hastings algorithm in sampling from sparse probability distributions (such as those confronted by the ants) with only a little additional computational cost. Our Bayesian framework for superorganismal behaviour motivates the evolution of exploratory mechanisms such as trail marking in terms of enhanced collective information processing.

Phenotypic Plasticity Provides a Bioinspiration Framework for Minimal Field Swarm Robotics.

The real world is highly variable and unpredictable, and so fine-tuned robot controllers that successfully result in group-level "emergence" of swarm capabilities indoors may quickly become inadequate outside. One response to unpredictability could be greater robot complexity and cost, but this seems counter to the "swarm philosophy" of deploying (very) large numbers of simple agents. Instead, here I argue that bioinspiration in swarm robotics has considerable untapped potential in relation to the phenomenon of phenotypic plasticity: when a genotype can produce a range of distinctive changes in organismal behavior, physiology and morphology in response to different environments. This commonly arises following a natural history of variable conditions; implying the need for more diverse and hazardous simulated environments in offline, pre-deployment optimization of swarms. This will generate-indicate the need for-plasticity. Biological plasticity is sometimes irreversible; yet this characteristic remains relevant in the context of minimal swarms, where robots may become mass-producible. Plasticity can be introduced through the greater use of adaptive threshold-based behaviors; more fundamentally, it can link to emerging technologies such as smart materials, which can adapt form and function to environmental conditions. Moreover, in social animals, individual heterogeneity is increasingly recognized as functional for the group. Phenotypic plasticity can provide meaningful diversity "for free" based on early, local sensory experience, contributing toward better collective decision-making and resistance against adversarial agents, for example. Nature has already solved the challenge of resilient self-organisation in the physical realm through phenotypic plasticity: swarm engineers can follow this lead.

Testing the limits of pheromone stigmergy in high-density robot swarms.

Area coverage and collective exploration are key challenges for swarm robotics. Previous research in this field has drawn inspiration from ant colonies, with real, or more commonly virtual, pheromones deposited into a shared environment to coordinate behaviour through stigmergy. Repellent pheromones can facilitate rapid dispersal of robotic agents, yet this has been demonstrated only for relatively small swarm sizes (N < 30). Here, we report findings from swarms of real robots (Kilobots) an order of magnitude larger (N > 300) and from realistic simulation experiments up to N = 400. We identify limitations to stigmergy in a spatially constrained, high-density environment-a free but bounded two-dimensional workspace-using repellent binary pheromone. At larger N and higher densities, a simple stigmergic avoidance algorithm becomes first no better, then inferior to, the area coverage of non-interacting random walkers. Thus, the assumption of robustness and scalability for such approaches may need to be re-examined when they are working at a high density caused by ever-increasing swarm sizes. Instead, subcellular biology, and diffusive processes, may prove a better source of inspiration at large N in high agent density environments.

Optimal foraging and the information theory of gambling.

At a macroscopic level, part of the ant colony life cycle is simple: a colony collects resources; these resources are converted into more ants, and these ants in turn collect more resources. Because more ants collect more resources, this is a multiplicative process, and the expected logarithm of the amount of resources determines how successful the colony will be in the long run. Over 60 years ago, Kelly showed, using information theoretic techniques, that the rate of growth of resources for such a situation is optimized by a strategy of betting in proportion to the probability of pay-off. Thus, in the case of ants, the fraction of the colony foraging at a given location should be proportional to the probability that resources will be found there, a result widely applied in the mathematics of gambling. This theoretical optimum leads to predictions as to which collective ant movement strategies might have evolved. Here, we show how colony-level optimal foraging behaviour can be achieved by mapping movement to Markov chain Monte Carlo (MCMC) methods, specifically Hamiltonian Monte Carlo (HMC). This can be done by the ants following a (noisy) local measurement of the (logarithm of) resource probability gradient (possibly supplemented with momentum, i.e. a propensity to move in the same direction). This maps the problem of foraging (via the information theory of gambling, stochastic dynamics and techniques employed within Bayesian statistics to efficiently sample from probability distributions) to simple models of ant foraging behaviour. This identification has broad applicability, facilitates the application of information theory approaches to understand movement ecology and unifies insights from existing biomechanical, cognitive, random and optimality movement paradigms. At the cost of requiring ants to obtain (noisy) resource gradient information, we show that this model is both efficient and matches a number of characteristics of real ant exploration.

Resting networks and personality predict attack speed in social spiders.

Groups of social predators capture large prey items collectively, and their social interaction patterns may impact how quickly they can respond to time-sensitive predation opportunities. We investigated whether various organizational levels of resting interactions (individual, sub-group, group), observed at different intervals leading up to a collective prey attack, impacted the predation speed of colonies of the social spider Stegodyphus dumicola. We found that in adult spiders, overall group connectivity (average degree) increased group attack speed. However, this effect was detected only immediately before the predation event; connectivity between 2 and 4 days before prey capture had little impact on the collective dynamics. Significantly, lower social proximity of the group's boldest individual to other group members (closeness centrality) immediately prior and 2 days before prey capture was associated with faster attack speeds. These results suggest that for adult spiders, the long-lasting effects of the boldest individual on the group's attack dynamics are mediated by its role in the social network, and not only by its boldness. This suggests that behavioural traits and social network relationships should be considered together when defining keystone individuals in some contexts. By contrast, for subadult spiders, while the group maximum boldness was negatively correlated with latency to attack, no significant resting network predictors of latency to attack were found. Thus, separate behavioural mechanisms might play distinctive roles in determining collective outcomes at different developmental stages, timescales, and levels of social organization.

Social interactions shape individual and collective personality in social spiders.

The behavioural composition of a group and the dynamics of social interactions can both influence how social animals work collectively. For example, individuals exhibiting certain behavioural tendencies may have a disproportionately large impact on the group, and so are referred to as keystone individuals, while interactions between individuals can facilitate information transmission about resources. Despite the potential impact of both behavioural composition and interactions on collective behaviour, the relationship between consistent behaviours (also known as personalities) and social interactions remains poorly understood. Here, we use stochastic actor-oriented models to uncover the interdependencies between boldness and social interactions in the social spider Stegodyphus dumicola We find that boldness has no effect on the likelihood of forming social interactions, but interactions do affect boldness, and lead to an increase in the boldness of the shyer individual. Furthermore, spiders tend to interact with the same individuals as their neighbours. In general, boldness decreases over time, but once an individual's boldness begins to increase, this increase accelerates, suggesting a positive feedback mechanism. These dynamics of interactions and boldness result in skewed boldness distributions of a few bold individuals and many shy individuals, as observed in nature. This group behavioural composition facilitates efficient collective behaviours, such as rapid collective prey attack. Thus, by examining the relationship between behaviour and interactions, we reveal the mechanisms that underlie the emergence of adaptive group composition and collective behaviour.

Asymmetric ommatidia count and behavioural lateralization in the ant Temnothorax albipennis.

Workers of the house-hunting ant Temnothorax albipennis rely on visual edge following and landmark recognition to navigate their rocky environment, and they also exhibit a leftward turning bias when exploring unknown nest sites. We used electron microscopy to count the number of ommatidia composing the compound eyes of workers, males and queens, to make an approximate assessment of their relative sampling resolution; and to establish whether there is an asymmetry in the number of ommatidia composing the workers' eyes, which might provide an observable, mechanistic explanation for the turning bias. We hypothesise that even small asymmetries in relative visual acuity between left and right eyes could be magnified by developmental experience into a symmetry-breaking turning preference that results in the inferior eye pointing toward the wall. Fifty-six workers were examined: 45% had more ommatidia in the right eye, 36% more in the left, and 20% an equal number. A tentative connection between relative ommatidia count for each eye and turning behaviour was identified, with a stronger assessment of behavioural lateralization before imaging and a larger sample suggested for further work. There was a clear sexual dimorphism in ommatidia counts between queens and males.

Complementary landmarks facilitate ant navigation.

Visual landmarks are important navigational aids to many animals, and when more than one is available their juxtaposition can convey valuable new information to a navigator about progress toward a goal, depending on the landmarks' comparative distinctiveness. We investigated the effect of presenting rock ant colonies (Temnothorax albipennis) with identical horizontal landmarks either side of their route, versus one horizontal landmark paired with a sloping landmark, as they navigated to a new nest site. Our findings suggest that ants can obtain more navigational information from a combination of dissimilar landmarks: the average tortuosity of the route taken between old and new nests was significantly lower when a horizontal landmark was paired with a monotonically downward sloping landmark (the paths were more direct). The impact on available navigational information from the similarity or dissimilarity of nearby landmarks is likely made through more distinctive visual panoramas, and could be an influential factor in individual and collective animal decision-making about which routes are followed. Furthermore, the effect of landmark complementarity may be relevant to a wide range of species, including other insects or birds, and highlights the possibility that there is an intrinsic difference in the informational content of natural vs. artificial environments.

Deconstructing Superorganisms and Societies to Address Big Questions in Biology.

Social insect societies are long-standing models for understanding social behaviour and evolution. Unlike other advanced biological societies (such as the multicellular body), the component parts of social insect societies can be easily deconstructed and manipulated. Recent methodological and theoretical innovations have exploited this trait to address an expanded range of biological questions. We illustrate the broadening range of biological insight coming from social insect biology with four examples. These new frontiers promote open-minded, interdisciplinary exploration of one of the richest and most complex of biological phenomena: sociality.

Ants determine their next move at rest: motor planning and causality in complex systems.

To find useful work to do for their colony, individual eusocial animals have to move, somehow staying attentive to relevant social information. Recent research on individual Temnothorax albipennis ants moving inside their colony's nest found a power-law relationship between a movement's duration and its average speed; and a universal speed profile for movements showing that they mostly fluctuate around a constant average speed. From this predictability it was inferred that movement durations are somehow determined before the movement itself. Here, we find similar results in lone T. albipennis ants exploring a large arena outside the nest, both when the arena is clean and when it contains chemical information left by previous nest-mates. This implies that these movement characteristics originate from the same individual neural and/or physiological mechanism(s), operating without immediate regard to social influences. However, the presence of pheromones and/or other cues was found to affect the inter-event speed correlations. Hence we suggest that ants' motor planning results in intermittent response to the social environment: movement duration is adjusted in response to social information only between movements, not during them. This environmentally flexible, intermittently responsive movement behaviour points towards a spatially allocated division of labour in this species. It also prompts more general questions on collective animal movement and the role of intermittent causation from higher to lower organizational levels in the stability of complex systems.

Ants show a leftward turning bias when exploring unknown nest sites.

Behavioural lateralization in invertebrates is an important field of study because it may provide insights into the early origins of lateralization seen in a diversity of organisms. Here, we present evidence for a leftward turning bias in Temnothorax albipennis ants exploring nest cavities and in branching mazes, where the bias is initially obscured by thigmotaxis (wall-following) behaviour. Forward travel with a consistent turning bias in either direction is an effective nest exploration method, and a simple decision-making heuristic to employ when faced with multiple directional choices. Replication of the same bias at the colony level would also reduce individual predation risk through aggregation effects, and may lead to a faster attainment of a quorum threshold for nest migration. We suggest the turning bias may be the result of an evolutionary interplay between vision, exploration and migration factors, promoted by the ants' eusociality.

Static electric fields modify the locomotory behaviour of cockroaches.

Static electric fields are found throughout the environment and there is growing interest in how electric fields influence insect behaviour. Here we have analysed the locomotory behaviour of cockroaches (Periplaneta americana) in response to static electric fields at levels equal to and above those found in the natural environment. Walking behaviour (including velocity, distance moved, turn angle and time spent walking) were analysed as cockroaches approached an electric field boundary in an open arena, and also when continuously exposed to an electric field. On approaching an electric field boundary, the greater the electric field strength the more likely a cockroach would be to turn away from, or be repulsed by, the electric field. Cockroaches completely exposed to electric fields showed significant changes in locomotion by covering less distance, walking slowly and turning more often. This study highlights the importance of electric fields on the normal locomotory behaviour of insects.

Static electric field detection and behavioural avoidance in cockroaches.

Electric fields are pervasively present in the environment and occur both as a result of man-made activities and through natural occurrence. We have analysed the behaviour of cockroaches to static electric fields and determined the physiological mechanisms that underlie their behavioural responses. The behaviour of animals in response to electric fields was tested using a Y-choice chamber with an electric field generated in one arm of the chamber. Locomotory behaviour and avoidance were affected by the magnitude of the electric fields with up to 85% of individuals avoiding the charged arm when the static electric field at the entrance to the arm was above 8-10 kV m(-1). Electric fields were found to cause a deflection of the antennae but when the antennae were surgically ablated, the ability of cockroaches to avoid electric fields was abolished. Fixation of various joints of the antennae indicated that hair plate sensory receptors at the base of the scape were primarily responsible for the detection of electric fields, and when antennal movements about the head-scape joint were prevented cockroaches failed to avoid electric fields. To overcome the technical problem of not being able to carry out electrophysiological analysis in the presence of electric fields, we developed a procedure using magnetic fields combined with the application of iron particles to the antennae to deflect the antennae and analyse the role of thoracic interneurones in signalling this deflection. The avoidance of electric fields in the context of high voltage power lines is discussed.