AUTHOR=Ouellette Nicholas T. , Gordon Deborah M. TITLE=Goals and Limitations of Modeling Collective Behavior in Biological Systems JOURNAL=Frontiers in Physics VOLUME=9 YEAR=2021 URL=https://www.frontiersin.org/journals/physics/articles/10.3389/fphy.2021.687823 DOI=10.3389/fphy.2021.687823 ISSN=2296-424X ABSTRACT=

Local social interactions among individuals in animal groups generate collective behavior, allowing groups to adjust to changing conditions. Historically, scientists from different disciplines have taken different approaches to modeling collective behavior. We describe how each can contribute to the goal of understanding natural systems. Simple bottom-up models that describe individuals and their interactions directly have demonstrated that local interactions far from equilibrium can generate collective states. However, such simple models are not likely to describe accurately the actual mechanisms and interactions in play in any real biological system. Other classes of top-down models that describe group-level behavior directly have been proposed for groups where the function of the collective behavior is understood. Such models cannot necessarily explain why or how such functions emerge from first principles. Because modeling approaches have different strengths and weaknesses and no single approach will always be best, we argue that models of collective behavior that are aimed at understanding real biological systems should be formulated to address specific questions and to allow for validation. As examples, we discuss four forms of collective behavior that differ both in the interactions that produce the collective behavior and in ecological context, and thus require very different modeling frameworks. 1) Harvester ants use local interactions consisting of brief antennal contact, in which one ant assesses the cuticular hydrocarbon profile of another, to regulate foraging activity, which can be modeled as a closed-loop excitable system. 2) Arboreal turtle ants form trail networks in the canopy of the tropical forest, using trail pheromone; one ant detects the volatile chemical that another has recently deposited. The process that maintains and repairs the trail, which can be modeled as a distributed algorithm, is constrained by the physical configuration of the network of vegetation in which they travel. 3) Swarms of midges interact acoustically and non-locally, and can be well described as agents moving in an emergent potential well that is representative of the swarm as a whole rather than individuals. 4) Flocks of jackdaws change their effective interactions depending on ecological context, using topological distance when traveling but metric distance when mobbing. We discuss how different research questions about these systems have led to different modeling approaches.