Sensory collectives in natural systems.

Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a 'sensory collective'; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify 'sensescapes'. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.

Inferring social influence in animal groups across multiple timescales.

Many animal behaviours exhibit complex temporal dynamics, suggesting there are multiple timescales at which they should be studied. However, researchers often focus on behaviours that occur over relatively restricted temporal scales, typically ones that are more accessible to human observation. The situation becomes even more complex when considering multiple animals interacting, where behavioural coupling can introduce new timescales of importance. Here, we present a technique to study the time-varying nature of social influence in mobile animal groups across multiple temporal scales. As case studies, we analyse golden shiner fish and homing pigeons, which move in different media. By analysing pairwise interactions among individuals, we show that predictive power of the factors affecting social influence depends on the timescale of analysis. Over short timescales the relative position of a neighbour best predicts its influence and the distribution of influence across group members is relatively linear, with a small slope. At longer timescales, however, both relative position and kinematics are found to predict influence, and nonlinearity in the influence distribution increases, with a small number of individuals being disproportionately influential. Our results demonstrate that different interpretations of social influence arise from analysing behaviour at different timescales, highlighting the importance of considering its multiscale nature. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Disentangling influence over group speed and direction reveals multiple patterns of influence in moving meerkat groups.

Animals that travel together in groups must constantly come to consensus about both the direction and speed of movement, often simultaneously. Contributions to collective decisions may vary among group members, yet inferring who has influence over group decisions is challenging, largely due to the multifaceted nature of influence. Here we collected high-resolution GPS data from five habituated meerkat groups in their natural habitat during foraging and developed a method to quantify individual influence over both group direction and speed. We find that individual influence over direction and speed are correlated, but also exhibit substantial variation. Comparing patterns across social statuses reveals that dominant females have higher influence than other individuals over both group direction and speed. Individuals with high influence also tend to spend more time in the front of the group. We discuss our results in light of meerkat life-history and current literature on influence during group movement. Our method provides a general approach which can be applied to disentangle individual influence over group direction and speed in a wide range of species with cohesive movement, emphasizing the importance of integrating multiple lines of inquiry when inferring influence in moving animal groups.

The geometry of decision-making in individuals and collectives.

Choosing among spatially distributed options is a central challenge for animals, from deciding among alternative potential food sources or refuges to choosing with whom to associate. Using an integrated theoretical and experimental approach (employing immersive virtual reality), we consider the interplay between movement and vectorial integration during decision-making regarding two, or more, options in space. In computational models of this process, we reveal the occurrence of spontaneous and abrupt "critical" transitions (associated with specific geometrical relationships) whereby organisms spontaneously switch from averaging vectorial information among, to suddenly excluding one among, the remaining options. This bifurcation process repeats until only one option-the one ultimately selected-remains. Thus, we predict that the brain repeatedly breaks multichoice decisions into a series of binary decisions in space-time. Experiments with fruit flies, desert locusts, and larval zebrafish reveal that they exhibit these same bifurcations, demonstrating that across taxa and ecological contexts, there exist fundamental geometric principles that are essential to explain how, and why, animals move the way they do.

Collective detection based on visual information in animal groups.

We investigate key principles underlying individual, and collective, visual detection of stimuli, and how this relates to the internal structure of groups. While the individual and collective detection principles are generally applicable, we employ a model experimental system of schooling golden shiner fish (Notemigonus crysoleucas) to relate theory directly to empirical data, using computational reconstruction of the visual fields of all individuals. This reveals how the external visual information available to each group member depends on the number of individuals in the group, the position within the group, and the location of the external visually detectable stimulus. We find that in small groups, individuals have detection capability in nearly all directions, while in large groups, occlusion by neighbours causes detection capability to vary with position within the group. To understand the principles that drive detection in groups, we formulate a simple, and generally applicable, model that captures how visual detection properties emerge due to geometric scaling of the space occupied by the group and occlusion caused by neighbours. We employ these insights to discuss principles that extend beyond our specific system, such as how collective detection depends on individual body shape, and the size and structure of the group.

Consistent Individual Differences Drive Collective Behavior and Group Functioning of Schooling Fish.

The ubiquity of consistent inter-individual differences in behavior ("animal personalities") [1, 2] suggests that they might play a fundamental role in driving the movements and functioning of animal groups [3, 4], including their collective decision-making, foraging performance, and predator avoidance. Despite increasing evidence that highlights their importance [5-16], we still lack a unified mechanistic framework to explain and to predict how consistent inter-individual differences may drive collective behavior. Here we investigate how the structure, leadership, movement dynamics, and foraging performance of groups can emerge from inter-individual differences by high-resolution tracking of known behavioral types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual's propensity to stay near others, measured by a classic "sociability" assay, was negatively linked to swim speed across a range of contexts, and predicted spatial positioning and leadership within groups as well as differences in structure and movement dynamics between groups. In turn, this trait, together with individual's exploratory tendency, measured by a classic "boldness" assay, explained individual and group foraging performance. These effects of consistent individual differences on group-level states emerged naturally from a generic model of self-organizing groups composed of individuals differing in speed and goal-orientedness. Our study provides experimental and theoretical evidence for a simple mechanism to explain the emergence of collective behavior from consistent individual differences, including variation in the structure, leadership, movement dynamics, and functional capabilities of groups, across social and ecological scales. In addition, we demonstrate individual performance is conditional on group composition, indicating how social selection may drive behavioral differentiation between individuals.