Determining individual-level interactions that govern highly coordinated motion in animal groups or cellular aggregates has been a long-standing challenge, central to understanding the mechanisms and evolution of collective behavior. Numerous models have been proposed, many of which display realistic-looking dynamics, but nonetheless rely on untested assumptions about how individuals integrate information to guide movement. Here we infer behavioral rules directly from experimental data. We begin by analyzing trajectories of golden shiners (Notemigonus crysoleucas) swimming in two-fish and three-fish shoals to map the mean effective forces as a function of fish positions and velocities. Speeding and turning responses are dynamically modulated and clearly delineated. Speed regulation is a dominant component of how fish interact, and changes in speed are transmitted to those both behind and ahead. Alignment emerges from attraction and repulsion, and fish tend to copy directional changes made by those ahead. We find no evidence for explicit matching of body orientation. By comparing data from two-fish and three-fish shoals, we challenge the standard assumption, ubiquitous in physics-inspired models of collective behavior, that individual motion results from averaging responses to each neighbor considered separately; three-body interactions make a substantial contribution to fish dynamics. However, pairwise interactions qualitatively capture the correct spatial interaction structure in small groups, and this structure persists in larger groups of 10 and 30 fish. The interactions revealed here may help account for the rapid changes in speed and direction that enable real animal groups to stay cohesive and amplify important social information.A fundamental problem in a wide range of biological disciplines is understanding how functional complexity at a macroscopic scale (such as the functioning of a biological tissue) results from the actions and interactions among the individual components (such as the cells forming the tissue). Animal groups such as bird flocks, fish schools, and insect swarms frequently exhibit complex and coordinated collective behaviors and present unrivaled opportunities to link the behavior of individuals with dynamic group-level properties. With the advent of tracking technologies such as computer vision and global positioning systems, group behavior can be reduced to a set of trajectories in space and time. Consequently, in principle, it is possible to deduce the individual interaction rules starting from the observed kinematics. However, calculating interindividual interactions from trajectories means solving a fundamental inverse problem that appears universally in many-body systems. In general, such problems are very hard to solve and, even if they can be solved, their solution is often not unique.To avoid solving these inverse problems (and because detailed kinematic data were not available until recently), many attempts have been made to replicate the patterns observed in animal groups by...
The capacity for groups to exhibit collective intelligence is an often-cited advantage of group living. Previous studies have shown that social organisms frequently benefit from pooling imperfect individual estimates. However, in principle, collective intelligence may also emerge from interactions between individuals, rather than from the enhancement of personal estimates. Here, we reveal that this emergent problem solving is the predominant mechanism by which a mobile animal group responds to complex environmental gradients. Robust collective sensing arises at the group level from individuals modulating their speed in response to local, scalar, measurements of light and through social interaction with others. This distributed sensing requires only rudimentary cognition and thus could be widespread across biological taxa, in addition to being appropriate and cost-effective for robotic agents.
The spontaneous emergence of pattern formation is ubiquitous in nature, often arising as a collective phenomenon from interactions among a large number of individual constituents or sub-systems. Understanding, and controlling, collective behavior is dependent on determining the low-level dynamical principles from which spatial and temporal patterns emerge; a key question is whether different group-level patterns result from all components of a system responding to the same external factor, individual components changing behavior but in a distributed self-organized way, or whether multiple collective states co-exist for the same individual behaviors. Using schooling fish (golden shiners, in groups of 30 to 300 fish) as a model system, we demonstrate that collective motion can be effectively mapped onto a set of order parameters describing the macroscopic group structure, revealing the existence of at least three dynamically-stable collective states; swarm, milling and polarized groups. Swarms are characterized by slow individual motion and a relatively dense, disordered structure. Increasing swim speed is associated with a transition to one of two locally-ordered states, milling or highly-mobile polarized groups. The stability of the discrete collective behaviors exhibited by a group depends on the number of group members. Transitions between states are influenced by both external (boundary-driven) and internal (changing motion of group members) factors. Whereas transitions between locally-disordered and locally-ordered group states are speed dependent, analysis of local and global properties of groups suggests that, congruent with theory, milling and polarized states co-exist in a bistable regime with transitions largely driven by perturbations. Our study allows us to relate theoretical and empirical understanding of animal group behavior and emphasizes dynamic changes in the structure of such groups.
Conflicting interests among group members are common when making collective decisions, yet failure to achieve consensus can be costly. Under these circumstances individuals may be susceptible to manipulation by a strongly opinionated, or extremist, minority. It has previously been argued, for humans and animals, that social groups containing individuals who are uninformed, or exhibit weak preferences, are particularly vulnerable to such manipulative agents. Here, we use theory and experiment to demonstrate that, for a wide range of conditions, a strongly opinionated minority can dictate group choice, but the presence of uninformed individuals spontaneously inhibits this process, returning control to the numerical majority. Our results emphasize the role of uninformed individuals in achieving democratic consensus amid internal group conflict and informational constraints. S ocial organisms must often achieve a consensus to obtain the benefits of group living and to avoid the costs of indecision (1 12). In some societies, notably those of eu social insects, making consensus decisions is often a unitary, conflict free process because the close relatedness among individuals means that they typically share preferences (11). However, in other social animals, such as schooling fub, flocking birds, herding ungulates, and humans, individual groop members may be oflow relatedness; thus, self interest can play an important role in group decisions. Reaching a consensus decision, there fore, frequently depends on individuals resolving complex conilicts of interest (1 11, 13, 14).There are several means of achieving groop consensus. In some cases, decisions made by one or only a small proportion of the group dictate the behavior of the entire group ( 4 6, 13, 14). There fore, a minority, or even a single individual, has the potential to control or exploit the majority, achieving substantial gains at the expense of other group members (1 6,9,10,14). In contrast, consensus can also be reached throogh demo cratic means, with fuir representation and an out come determined by a plurality. Democratic decisions tend to be more moderate, rninimiz ing group consensus costs, particularly in large animal groops (3). However, in the absence of established procedures such as voting ( 8), it is IDlclear how equal representation is enforced Consequently, for both human socwtJes (1,2,6,9,10,14) and group living animals ( 6, 13), it has been afb'lted that group decisions can be subject to manipulation by a self interested and opinionated minority. In particular, previoos work suggests that groups containing individu als who are uninformed, or naive, about the de cision being made are particularly vulnerable to such manipulation (2,9,10,13). Under this view, IDlinformed individuals destabilize the capacity for collective intelligence in groups (J 0, 14), with poorly informed individuals potentially facilitat ing the establishment of extremist opinions in populations (9,14).Here, we address the question of whether and, if so, under which condit...
Movement in animal groups is highly varied and ranges from seemingly disordered motion in swarms to coordinated aligned motion in flocks and schools. These social interactions are often thought to reduce risk from predators, despite a lack of direct evidence. We investigated risk-related selection for collective motion by allowing real predators (bluegill sunfish) to hunt mobile virtual prey. By fusing simulated and real animal behavior, we isolated predator effects while controlling for confounding factors. Prey with a tendency to be attracted toward, and to align direction of travel with, near neighbors tended to form mobile coordinated groups and were rarely attacked. These results demonstrate that collective motion could evolve as a response to predation, without prey being able to detect and respond to predators.
Predator-prey interactions are vital to the stability of many ecosystems. Yet, few studies have considered how they are mediated due to substantial challenges in quantifying behavior over appropriate temporal and spatial scales. Here, we employ high-resolution sonar imaging to track the motion and interactions among predatory fish and their schooling prey in a natural environment. In particular, we address the relationship between predator attack behavior and the capacity for prey to respond both directly and through collective propagation of changes in velocity by group members. To do so, we investigated a large number of attacks and estimated per capita risk during attack and its relation to the size, shape, and internal structure of prey groups. Predators were found to frequently form coordinated hunting groups, with up to five individuals attacking in line formation. Attacks were associated with increased fragmentation and irregularities in the spatial structure of prey groups, features that inhibit collective information transfer among prey. Prey group fragmentation, likely facilitated by predator line formation, increased (estimated) per capita risk of prey, provided prey schools were maintained below a threshold size of approximately 2 m(2). Our results highlight the importance of collective behavior to the strategies employed by both predators and prey under conditions of considerable informational constraints.
Predation is thought to shape the macroscopic properties of animal groups, making moving groups more cohesive and coordinated. Precisely how predation has shaped individuals' fine-scale social interactions in natural populations, however, is unknown. Using high-resolution tracking data of shoaling fish (Poecilia reticulata) from populations differing in natural predation pressure, we show how predation adapts individuals' social interaction rules. Fish originating from high predation environments formed larger, more cohesive, but not more polarized groups than fish from low predation environments. Using a new approach to detect the discrete points in time when individuals decide to update their movements based on the available social cues, we determine how these collective properties emerge from individuals' microscopic social interactions. We first confirm predictions that predation shapes the attraction–repulsion dynamic of these fish, reducing the critical distance at which neighbours move apart, or come back together. While we find strong evidence that fish align with their near neighbours, we do not find that predation shapes the strength or likelihood of these alignment tendencies. We also find that predation sharpens individuals' acceleration and deceleration responses, implying key perceptual and energetic differences associated with how individuals move in different predation regimes. Our results reveal how predation can shape the social interactions of individuals in groups, ultimately driving differences in groups' collective behaviour.
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