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      Multi-scale Inference of Interaction Rules in Animal Groups Using Bayesian Model Selection

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          Abstract

          Inference of interaction rules of animals moving in groups usually relies on an analysis of large scale system behaviour. Models are tuned through repeated simulation until they match the observed behaviour. More recent work has used the fine scale motions of animals to validate and fit the rules of interaction of animals in groups. Here, we use a Bayesian methodology to compare a variety of models to the collective motion of glass prawns ( Paratya australiensis). We show that these exhibit a stereotypical ‘phase transition’, whereby an increase in density leads to the onset of collective motion in one direction. We fit models to this data, which range from: a mean-field model where all prawns interact globally; to a spatial Markovian model where prawns are self-propelled particles influenced only by the current positions and directions of their neighbours; up to non-Markovian models where prawns have ‘memory’ of previous interactions, integrating their experiences over time when deciding to change behaviour. We show that the mean-field model fits the large scale behaviour of the system, but does not capture the observed locality of interactions. Traditional self-propelled particle models fail to capture the fine scale dynamics of the system. The most sophisticated model, the non-Markovian model, provides a good match to the data at both the fine scale and in terms of reproducing global dynamics, while maintaining a biologically plausible perceptual range. We conclude that prawns’ movements are influenced by not just the current direction of nearby conspecifics, but also those encountered in the recent past. Given the simplicity of prawns as a study system our research suggests that self-propelled particle models of collective motion should, if they are to be realistic at multiple biological scales, include memory of previous interactions and other non-Markovian effects.

          Author Summary

          The collective movement of animals in a group is an impressive phenomenon whereby large scale spatio-temporal patterns emerge from simple interactions between individuals. Theoretically, much of our understanding of animal group motion comes from models inspired by statistical physics. In these models, animals are treated as moving (self-propelled) particles that interact with each other according to simple rules. Recently, researchers have shown greater interest in using experimental data to verify which rules are actually implemented by a particular animal species. In our study, we present a rigorous selection between alternative models inspired by the literature for a system of glass prawns. We find that the classic theoretical models do not accurately predict either the fine scale or large scale behaviour of the system. Instead, individual animals appear to be interacting even when completely separated from each other. To resolve this we introduce a new class of models wherein prawns ‘remember‚ their previous interactions, integrating their experiences over time when deciding to change behaviour. These show that the fine scale and large scale behaviour of the prawns is consistent with interactions only between individuals who are close together.

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          Most cited references18

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          Novel Type of Phase Transition in a System of Self-Driven Particles

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            Interaction Ruling Animal Collective Behaviour Depends on Topological rather than Metric Distance: Evidence from a Field Study

            Numerical models indicate that collective animal behaviour may emerge from simple local rules of interaction among the individuals. However, very little is known about the nature of such interaction, so that models and theories mostly rely on aprioristic assumptions. By reconstructing the three-dimensional position of individual birds in airborne flocks of few thousands members, we prove that the interaction does not depend on the metric distance, as most current models and theories assume, but rather on the topological distance. In fact, we discover that each bird interacts on average with a fixed number of neighbours (six-seven), rather than with all neighbours within a fixed metric distance. We argue that a topological interaction is indispensable to maintain flock's cohesion against the large density changes caused by external perturbations, typically predation. We support this hypothesis by numerical simulations, showing that a topological interaction grants significantly higher cohesion of the aggregation compared to a standard metric one.
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              Inferring individual rules from collective behavior.

              Social organisms form striking aggregation patterns, displaying cohesion, polarization, and collective intelligence. Determining how they do so in nature is challenging; a plethora of simulation studies displaying life-like swarm behavior lack rigorous comparison with actual data because collecting field data of sufficient quality has been a bottleneck. Here, we bridge this gap by gathering and analyzing a high-quality dataset of flocking surf scoters, forming well-spaced groups of hundreds of individuals on the water surface. By reconstructing each individual's position, velocity, and trajectory, we generate spatial and angular neighbor-distribution plots, revealing distinct concentric structure in positioning, a preference for neighbors directly in front, and strong alignment with neighbors on each side. We fit data to zonal interaction models and characterize which individual interaction forces suffice to explain observed spatial patterns. Results point to strong short-range repulsion, intermediate-range alignment, and longer-range attraction (with circular zones), as well as a weak but significant frontal-sector interaction with one neighbor. A best-fit model with such interactions accounts well for observed group structure, whereas absence or alteration in any one of these rules fails to do so. We find that important features of observed flocking surf scoters can be accounted for by zonal models with specific, well-defined rules of interaction.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                March 2013
                March 2013
                21 March 2013
                : 9
                : 3
                : e1002961
                Affiliations
                [1 ]Department of Mathematics, Uppsala University, Uppsala, Sweden
                [2 ]Robotics Institute, Carnegie Mellon University, Pittsburgh, Pennylvania, United States of America
                [3 ]School of Biological Sciences, University of Sydney, Sydney, New South Wales, Australia
                Indiana University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AJWW. Performed the experiments: JEHR AJWW. Analyzed the data: RPM AP DS RG DJTS AJWW. Wrote the paper: RPM AP DJTS.

                Article
                PCOMPBIOL-D-12-01357
                10.1371/journal.pcbi.1002961
                3605063
                23555206
                9b308361-1b91-48a1-b212-0b6e4a8f8940
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 23 August 2012
                : 15 January 2013
                Page count
                Pages: 13
                Funding
                This study was partly funded by an ERC grant to DJTS (ref: IDCAB - 220/104702003) and a DVC grant from the University of Sydney to AJWW. RPM was supported by the Centre for Interdisciplinary Mathematics at Uppsala University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Ecosystem Modeling
                Ecology
                Behavioral Ecology
                Freshwater Ecology
                Theoretical Ecology
                Marine Biology
                Freshwater Ecology
                Theoretical Biology
                Zoology
                Animal Behavior
                Mathematics
                Applied Mathematics
                Complex Systems
                Probability Theory
                Bayes Theorem
                Markov Model
                Probability Density
                Stochastic Processes
                Physics
                Statistical Mechanics

                Quantitative & Systems biology
                Quantitative & Systems biology

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