Synchronized locomotion can improve spatial accessibility inside ant colonies.

Synchronization is a conspicuous form of collective behaviour that is of crucial importance in numerous biological systems. Ant colonies from the genera Leptothorax and Temnothorax form small colonies, typically made up of only a few hundred workers, and exhibit a form of synchronized behaviour where workers inside colonies' nests become active together in rhythmic cycles that have a period of approximately 20-200 min. However, it is not currently known if these synchronized rhythms of locomotion confer any functional benefit to colonies. By using a combination of multiple image analysis techniques, we show that inactive Leptothorax ants can act as immobile obstacles to moving ants, and that synchronized activity has the potential to reduce the likelihood that individual ants will encounter regions of immobile obstacles that impede access to portions of the nest. We demonstrate qualitatively similar findings using a computational model of confined active particles with oscillating activity.

Environmental habituation and sexual composition affect juveniles' shoaling activity in a cichlid fish (Pelvicachromis taeniatus).

Group living is widespread in animals, and many fishes form shoals. Examining within-group interactions in fishes may contribute to the general understanding of dynamic social structures in animals. The sex ratio of a group has been shown to influence grouping decisions of fishes and can be expected to affect behaviour at group level. Behavioural experiments usually involve relatively short acclimatisation times, although the establishment of environmental habituation in fishes is understudied. This study tests whether the sex ratio and long-term habituation to experimental conditions influence general shoal performance (activity parameters, density) and responses of shoals to an acoustic-mechanical disturbance cue in juveniles of the cichlid fish Pelvicachromis taeniatus via individual tracking. The disturbance consisted of a defined hit against the experimental tank, which caused sudden noise and water movement. We found that a higher proportion of females increases shoal activity (swimming speed and distance covered), suggesting that female P. taeniatus are more active than males. Furthermore, shoal activity declined when shoals habituated to the experimental settings and with the time that the shoals were grouped together, which may reflect intensified group member familiarity. Moreover, behavioural changes after disturbance were weaker when individuals were kept with their group longer and more familiar to the experimental conditions. For prey species, lower activity might be beneficial under natural conditions due to lower conspicuousness of the group. We did not find any significant effects of the investigated factors on shoal density (mean interindividual distance) and speed synchronisation. The results indicate that sexual composition, familiarity between shoal members and habituation to the experimental environment affect shoal performance in a cichlid fish.

Diurnal variation in the production of vocal information about food supports a model of social adjustment in wild songbirds.

Wintering songbirds have been widely shown to make economic foraging decisions to manage the changing balance of risks from predation and starvation over the course of the day. In this study, we ask whether the communication and use of information about food availability differ throughout the day. First, we assessed temporal variation in food-related vocal information produced in foraging flocks of tits ( Paridae) using audio recordings at radio-frequency identification-equipped feeding stations. Vocal activity was highest in the morning and decreased into the afternoon. This pattern was not explained by there being fewer birds present, as we found that group sizes increased over the course of the day. Next, we experimentally tested the underlying causes for this diurnal calling pattern. We set up bird feeders with or without playback of calls from tits, either in the morning or in the afternoon, and compared latency to feeder discovery, accumulation of flock members, and total number of birds visiting the feeder. Irrespective of time of day, playbacks had a strong effect on all three response measures when compared to silent control trials, demonstrating that tits will readily use vocal information to improve food detection throughout the day. Thus, the diurnal pattern of foraging behaviour did not appear to affect use and production of food-related vocalizations. Instead, we suggest that, as the day progresses and foraging group sizes increase, the costs of producing calls at the food source (e.g. competition and attraction of predators) outweigh the benefits of recruiting group members (i.e. adding individuals to large groups only marginally increases safety in numbers), causing the observed decrease in vocal activity into the afternoon. Our findings imply that individuals make economic social adjustments based on conditions of their social environment when deciding to vocally recruit group members.

Social conformity and propagation of information in collective U-turns of fish schools.

Moving animal groups such as schools of fishes or flocks of birds often undergo sudden collective changes of their travelling direction as a consequence of stochastic fluctuations in heading of the individuals. However, the mechanisms by which these behavioural fluctuations arise at the individual level and propagate within a group are still unclear. In this study, we combine an experimental and theoretical approach to investigate spontaneous collective U-turns in groups of rummy-nose tetra (Hemigrammus rhodostomus) swimming in a ring-shaped tank. U-turns imply that fish switch their heading between the clockwise and anticlockwise direction. We reconstruct trajectories of individuals moving alone and in groups of different sizes. We show that the group decreases its swimming speed before a collective U-turn. This is in agreement with previous theoretical predictions showing that speed decrease facilitates an amplification of fluctuations in heading in the group, which can trigger U-turns. These collective U-turns are mostly initiated by individuals at the front of the group. Once an individual has initiated a U-turn, the new direction propagates through the group from front to back without amplification or dampening, resembling the dynamics of falling dominoes. The mean time between collective U-turns sharply increases as the size of the group increases. We develop an Ising spin model integrating anisotropic and asymmetrical interactions between fish and their tendency to follow the majority of their neighbours nonlinearly (social conformity). The model quantitatively reproduces key features of the dynamics and the frequency of collective U-turns observed in experiments.

Individual variation in local interaction rules can explain emergent patterns of spatial organization in wild baboons.

Researchers have long noted that individuals occupy consistent spatial positions within animal groups. However, an individual's position depends not only on its own behaviour, but also on the behaviour of others. Theoretical models of collective motion suggest that global patterns of spatial assortment can arise from individual variation in local interaction rules. However, this prediction remains untested. Using high-resolution GPS tracking of members of a wild baboon troop, we identify consistent inter-individual differences in within-group spatial positioning. We then apply an algorithm that identifies what number of conspecific group members best predicts the future location of each individual (we call this the individual's neighbourhood size) while the troop is moving. We find clear variation in the most predictive neighbourhood size, and this variation relates to individuals' propensity to be found near the centre of their group. Using simulations, we show that having different neighbourhood sizes is a simple candidate mechanism capable of linking variation in local individual interaction rules-in this case how many conspecifics an individual interacts with-to global patterns of spatial organization, consistent with the patterns we observe in wild primates and a range of other organisms.

When social behaviour is moulded in clay: on growth and form of social insect nests.

The nests built by social insects are among the most complex structures produced by animal groups. They reveal the social behaviour of a colony and as such they potentially allow comparative studies. However, for a long time, research on nest architecture was hindered by the lack of technical tools allowing the visualisation of their complex 3D structures and the quantification of their properties. Several techniques, developed over the years, now make it possible to study the organisation of these nests and how they are built. Here, we review present knowledge of the mechanisms of nest construction, and how nest structure affects the behaviour of individual insects and the organisation of activities within a colony.

Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions.

Over recent years, modelling approaches from nutritional ecology (known as Nutritional Geometry) have been increasingly used to describe how animals and some other organisms select foods and eat them in appropriate amounts in order to maintain a balanced nutritional state maximising fitness. These nutritional strategies profoundly affect the physiology, behaviour and performance of individuals, which in turn impact their social interactions within groups and societies. Here, we present a conceptual framework to study the role of nutrition as a major ecological factor influencing the development and maintenance of social life. We first illustrate some of the mechanisms by which nutritional differences among individuals mediate social interactions in a broad range of species and ecological contexts. We then explain how studying individual- and collective-level nutrition in a common conceptual framework derived from Nutritional Geometry can bring new fundamental insights into the mechanisms and evolution of social interactions, using a combination of simulation models and manipulative experiments.

Dynamics of collective motion across time and species.

Most studies of collective animal behaviour rely on short-term observations, and comparisons of collective behaviour across different species and contexts are rare. We therefore have a limited understanding of intra- and interspecific variation in collective behaviour over time, which is crucial if we are to understand the ecological and evolutionary processes that shape collective behaviour. Here, we study the collective motion of four species: shoals of stickleback fish (Gasterosteus aculeatus), flocks of homing pigeons (Columba livia), a herd of goats (Capra aegagrus hircus) and a troop of chacma baboons (Papio ursinus). First, we describe how local patterns (inter-neighbour distances and positions), and group patterns (group shape, speed and polarization) during collective motion differ across each system. Based on these, we place data from each species within a 'swarm space', affording comparisons and generating predictions about the collective motion across species and contexts. We encourage researchers to add their own data to update the 'swarm space' for future comparative work. Second, we investigate intraspecific variation in collective motion over time and provide guidance for researchers on when observations made over different time scales can result in confident inferences regarding species collective motion. This article is part of a discussion meeting issue 'Collective behaviour through time'.

A data-driven method for reconstructing and modelling social interactions in moving animal groups.

Group-living organisms that collectively migrate range from cells and bacteria to human crowds, and include swarms of insects, schools of fish, and flocks of birds or ungulates. Unveiling the behavioural and cognitive mechanisms by which these groups coordinate their movements is a challenging task. These mechanisms take place at the individual scale and can be described as a combination of interactions between individuals and interactions between these individuals and the physical obstacles in the environment. Thanks to the development of novel tracking techniques that provide large and accurate datasets, the main characteristics of individual and collective behavioural patterns can be quantified with an unprecedented level of precision. However, in a large number of studies, social interactions are usually described by force map methods that only have a limited capacity of explanation and prediction, being rarely suitable for a direct implementation in a concise and explicit mathematical model. Here, we present a general method to extract the interactions between individuals that are involved in the coordination of collective movements in groups of organisms. We then apply this method to characterize social interactions in two species of shoaling fish, the rummy-nose tetra (Hemigrammus rhodostomus) and the zebrafish (Danio rerio), which both present a burst-and-coast motion. From the detailed quantitative description of individual-level interactions, it is thus possible to develop a quantitative model of the emergent dynamics observed at the group level, whose predictions can be checked against experimental results. This method can be applied to a wide range of biological and social systems. This article is part of the theme issue 'Multi-scale analysis and modelling of collective migration in biological systems'.

Weber's Law-based perception and the stability of animal groups.

Group living animals form aggregations and flocks that remain cohesive in spite of internal movements of individuals. This is possible because individual group members repeatedly adjust their position and motion in response to the position and motion of other group members. Here, we develop a theoretical approach to address the question, what general features-if any-underlie the interaction rules that mediate group stability in animals of all species? We do so by considering how the spatial organization of a group would change in the complete absence of interactions. Without interactions, a group would disperse in a way that can be easily characterized in terms of Fick's diffusion equations. We can hence address the inverse theoretical problem of finding the individual-level interaction responses that are required to counterbalance diffusion and to preserve group stability. We show that an individual-level response to neighbour densities in the form of Weber's Law (a 'universal' law describing the functioning of the sensory systems of animals of all species) results in an 'anti-diffusion' term at the group level. On short timescales, this anti-diffusion restores the initial group configuration in a way that is reminiscent of methods for image deblurring in image processing. We also show that any non-homogeneous, spatial density distribution can be preserved over time if individual movement patterns have the form of a Weber's Law response. Weber's Law describes the fundamental functioning of perceptual systems. Our study indicates that it is also a necessary-but not sufficient-feature of collective interactions in stable animal groups.

Friendship across species borders: factors that facilitate and constrain heterospecific sociality.

Our understanding of animal sociality is based almost entirely on single-species sociality. Heterospecific sociality, although documented in numerous taxa and contexts, remains at the margins of sociality research and is rarely investigated in conjunction with single-species sociality. This could be because heterospecific and single-species sociality are thought to be based on fundamentally different mechanisms. However, our literature survey shows that heterospecific sociality based on mechanisms similar to single-species sociality is reported from many taxa, contexts and for various benefits. Therefore, we propose a conceptual framework to understand conspecific versus heterospecific social partner choice. Previous attempts, which are all in the context of social information, model partner choice as a trade-off between information benefit and competition cost, along a single phenotypic distance axis. Our framework of partner choice considers both direct grouping benefits and information benefits, allows heterospecific and conspecific partners to differ in degree and qualitatively, and uses a multi-dimensional trait space analysis of costs (competition and activity matching) and benefits (relevance of partner and quality of partner). We conclude that social partner choice is best-viewed as a continuum: some social benefits are obtainable only from conspecifics, some only from dissimilar heterospecifics, while many are potentially obtainable from conspecifics and heterospecifics.This article is part of the theme issue 'Collective movement ecology'.

Collective behaviour in vertebrates: a sensory perspective.

Collective behaviour models can predict behaviours of schools, flocks, and herds. However, in many cases, these models make biologically unrealistic assumptions in terms of the sensory capabilities of the organism, which are applied across different species. We explored how sensitive collective behaviour models are to these sensory assumptions. Specifically, we used parameters reflecting the visual coverage and visual acuity that determine the spatial range over which an individual can detect and interact with conspecifics. Using metric and topological collective behaviour models, we compared the classic sensory parameters, typically used to model birds and fish, with a set of realistic sensory parameters obtained through physiological measurements. Compared with the classic sensory assumptions, the realistic assumptions increased perceptual ranges, which led to fewer groups and larger group sizes in all species, and higher polarity values and slightly shorter neighbour distances in the fish species. Overall, classic visual sensory assumptions are not representative of many species showing collective behaviour and constrain unrealistically their perceptual ranges. More importantly, caution must be exercised when empirically testing the predictions of these models in terms of choosing the model species, making realistic predictions, and interpreting the results.

Initiation and spread of escape waves within animal groups.

The exceptional reactivity of animal collectives to predatory attacks is thought to be owing to rapid, but local, transfer of information between group members. These groups turn together in unison and produce escape waves. However, it is not clear how escape waves are created from local interactions, nor is it understood how these patterns are shaped by natural selection. By startling schools of fish with a simulated attack in an experimental arena, we demonstrate that changes in the direction and speed by a small percentage of individuals that detect the danger initiate an escape wave. This escape wave consists of a densely packed band of individuals that causes other school members to change direction. In the majority of cases, this wave passes through the entire group. We use a simulation model to demonstrate that this mechanism can, through local interactions alone, produce arbitrarily large escape waves. In the model, when we set the group density to that seen in real fish schools, we find that the risk to the members at the edge of the group is roughly equal to the risk of those within the group. Our experiments and modelling results provide a plausible explanation for how escape waves propagate in nature without centralized control.

Determining asymptotically large population sizes in insect swarms.

Social animals commonly form aggregates that exhibit emergent collective behaviour, with group dynamics that are distinct from the behaviour of individuals. Simple models can qualitatively reproduce such behaviour, but only with large numbers of individuals. But how rapidly do the collective properties of animal aggregations in nature emerge with group size? Here, we study swarms of Chironomus riparius midges and measure how their statistical properties change as a function of the number of participating individuals. Once the swarms contain order 10 individuals, we find that all statistics saturate and the swarms enter an asymptotic regime. The influence of environmental cues on the swarm morphology decays on a similar scale. Our results provide a strong constraint on how rapidly swarm models must produce collective states. But our findings support the feasibility of using swarms as a design template for multi-agent systems, because self-organized states are possible even with few agents.

Animal transportation networks.

Many group-living animals construct transportation networks of trails, galleries and burrows by modifying the environment to facilitate faster, safer or more efficient movement. Animal transportation networks can have direct influences on the fitness of individuals, whereas the shape and structure of transportation networks can influence community dynamics by facilitating contacts between different individuals and species. In this review, we discuss three key areas in the study of animal transportation networks: the topological properties of networks, network morphogenesis and growth, and the behaviour of network users. We present a brief primer on elements of network theory, and then discuss the different ways in which animal groups deal with the fundamental trade-off between the competing network properties of travel efficiency, robustness and infrastructure cost. We consider how the behaviour of network users can impact network efficiency, and call for studies that integrate both network topology and user behaviour. We finish with a prospectus for future research.

Interaction rules underlying group decisions in homing pigeons.

Travelling in groups gives animals opportunities to share route information by following cues from each other's movement. The outcome of group navigation will depend on how individuals respond to each other within a flock, school, swarm or herd. Despite the abundance of modelling studies, only recently have researchers developed techniques to determine the interaction rules among real animals. Here, we use high-resolution GPS (global positioning system) tracking to study these interactions in pairs of pigeons flying home from a familiar site. Momentary changes in velocity indicate alignment with the neighbour's direction, as well as attraction or avoidance depending on distance. Responses were stronger when the neighbour was in front. From the flocking behaviour, we develop a model to predict features of group navigation. Specifically, we show that the interactions between pigeons stabilize a side-by-side configuration, promoting bidirectional information transfer and reducing the risk of separation. However, if one bird gets in front it will lead directional choices. Our model further predicts, and observations confirm, that a faster bird (as measured from solo flights) will fly slightly in front and thus dominate the choice of homing route. Our results explain how group decisions emerge from individual differences in homing flight behaviour.

The modelling cycle for collective animal behaviour.

Collective animal behaviour is the study of how interactions between individuals produce group level patterns, and why these interactions have evolved. This study has proved itself uniquely interdisciplinary, involving physicists, mathematicians, engineers as well as biologists. Almost all experimental work in this area is related directly or indirectly to mathematical models, with regular movement back and forth between models, experimental data and statistical fitting. In this paper, we describe how the modelling cycle works in the study of collective animal behaviour. We classify studies as addressing questions at different levels or linking different levels, i.e. as local, local to global, global to local or global. We also describe three distinct approaches-theory-driven, data-driven and model selection-to these questions. We show, with reference to our own research on species across different taxa, how we move between these different levels of description and how these various approaches can be applied to link levels together.