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Inferring the structure and dynamics of interactions in schooling fish
Open accessAbstract
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.
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“This knowledge can then be used to infer individual decision rules in collective motion (Katz, Tunstrom, Ioannou, Huepe, & Couzin, 2011;Nagy, Kos, Biro, & Vicsek, 2010) and to compute activity budgets for individuals without the need for continuous human observation or time-consuming video analysis.”
From Applications of machine learning in animal behaviour studies (2017) · cites this paper as Katz et al., 2011
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“The latter has typically been estimated from experiments or derived from heuristic observations [5, 8, 37].”
Emergent Properties of a Fish School
Kasumyan, A. O., & Pavlov, D. S. (2023) · Journal of Ichthyology · doi:10.1134/s0032945223070160 · Cited by 1
“…leader in a school and the rapid rotation of the leading fish has been confirmed by the example of many schooling fish (Bowen, 1931; Steven, 1959; Kühlmann and Karst, 1967; Krause et al., 2000; Reebs, 2001; Leblond and Reebs, 2006; Katz et al., 2011; Burns et al., 2012; Quera et al., 2023).”
Brief Announcement: On the Limits of Information Spread by Memory-less Agents
d'Archivio, N., & Vacus, R. (2024) · ACM Symposium on Principles of Distributed Computing (PODC) · doi:10.1145/3662158.3662813 · Cited by 1
Long-term co-occurrence and gregariousness in the migratory common stingray using network analysis
Kraft, S., Winkler, A. C., Abecasis, D., & Mourier, J. (2024) · Marine Biology · doi:10.1007/s00227-024-04498-z · Cited by 1
“Most works have been conducted on collective behaviour and structure and the mechanisms driving such individual interactions (Katz et al. 2011).”
Impact of Individual Defection on Collective Motion
Agrawal, S., Jhawar, J., Reina, A., Baliyarasimhuni, S. P., Hamann, H., & Li, L. (2024) · Lecture notes in computer science · doi:10.1007/978-3-031-70932-6_10 · Cited by 1
Familiarity dampens the effect of boldness on coordination in three-spined sticklebacks
Riley, R. J., Kwon, Y. M., Manica, A., & Savage, J. L. (2025) · Behaviour · doi:10.1163/1568539x-bja10300 · Cited by 1
Estimating social network metrics from single-file movements in Barbary macaques, Macaca sylvanus
Murphy, D., & Fischer, J. (2025) · Animal Behaviour · doi:10.1016/j.anbehav.2025.123146 · Cited by 1
Pausing Makes Perfect: Intermittent Pauses for Resilient Swarming
Shefi, P., Ayali, A., & Kaminka, G. A. (2025) · Springer proceedings in advanced robotics · doi:10.1007/978-3-032-04584-3_16 · Cited by 1
Investigating Coupling Strength in Multi-agent System
Liu, M., Yang, P., & Lei, X. (2016) · International Journal of Control and Automation · doi:10.14257/ijca.2016.9.10.21 · Cited by 1
“T (0) [20,10] m n p is the initial position of the virtual leader which updates according to (1).”
BackgroundCollective behaviors of self-propelled rods under semi-flexible elastic confinement
Zhong, Y., & Shi, X.-Q. (2020) · Acta Physica Sinica · doi:10.7498/aps.69.20200561 · Cited by 1
Processes affecting size of fish schools in agent‐based model
Kiriyama, K., & Iwasa, Y. (2021) · Population Ecology · doi:10.1002/1438-390x.12081 · Cited by 1
Ishibashi, K., & Sakaguchi, H. (2022) · Journal of the Physical Society of Japan · doi:10.7566/jpsj.91.034003 · Cited by 1
The HoneyComb Paradigm for Research on Collective Human Behavior
Boos, M., Pritz, J., & Belz, M. (2019) · Journal of Visualized Experiments · doi:10.3791/58719-v · Cited by 1
Forming, Confining, and Observing Microtubule-Based Active Nematics
Memarian, F. L., Khaladj, D. A., Hammar, D., & Hirst, L. S. (2023) · Journal of Visualized Experiments · doi:10.3791/64287-v · Cited by 1
Quera, V., Beltran, F. S., Gimeno, E., & Dolado, R. (2023) · Journal of Fish Biology · doi:10.1111/jfb.15315 · Cited by 1
An efficient method for sorting and selecting for social behaviourPreprint
Szorkovszky, A., Kotrschal, A., Herbert‐Read, J. E., Sumpter, D. J. T., Kolm, N., & Kristiaan Pelckmans, A. (2016) · arXiv (Cornell University) · doi:10.48550/arxiv.1602.05833 · Cited by 1
“Precise observations are increasingly available [11, 12], but detailed knowledge of how individuals respond to each other is more difficult to infer from this data [13].”
BackgroundNew Classification of Collective Animal Behaviour as an Autonomous SystemPreprint
Niizato, T., Sakamoto, K., Mototake, Y.-I., Murakami, H., Tomaru, T., Hoshika, T., & Fukushima, T. (2019) · Preprints.org · doi:10.20944/preprints201902.0269.v1 · Cited by 1
“How? The information transfer in the group, for instance, assumes the individual’s collective behaviour as one collection [38,42].”
BackgroundThe visual coupling between neighbors explains ‘flocking’ in human crowdsPreprint
Dachner, G. C., Wirth, T. D., Richmond, E., & Warren, W. H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.04.459001 · Cited by 1
“…approach that deploys experimental studies of behavioral interactions to infer the local rules (Calovi et al., 2018; Gautrais et al., 2012; Katz, Tunstrøm, Ioannou, Huepe, & Couzin, 2011; Moussaid et al., 2009; Sumpter, Mann, & Perna, 2012; Warren & Fajen, 2008; Zienkiewicz, Barton,…”
BackgroundMann, R. P., Perna, A., Strömbom, D., Garnett, R., Herbert‐Read, J. E., Sumpter, D. J. T., & Ward, A. J. W. (2012) · PLoS Computational Biology · doi:10.1371/annotation/f490031b-2e94-42c8-8c10-4e316a7435be · Cited by 1
New Classification of Collective Animal Behaviour as an Autonomous SystemPreprint
Niizato, T., Sakamoto, K., Mototake, Y.-I., Murakami, H., Tomaru, T., Hoshika, T., & Fukushima, T. (2020) · Preprints.org · doi:10.20944/preprints202003.0282.v1
Investigating manta ray collective movements via drone surveysPreprint
Perryman, R. J. Y., Brown, C., Pasian, N., Ward, A. J. W., & Kent, M. I. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.29.501955 · Cited by 1
“Various mechanisms and functions of collective behaviours are well understood in captive fish under experimental conditions (e.g. Katz et al. 2011; Ward et al. 2011; Tunstrøm et al. 2013; Schaerf et al. 2017; Herbert-Read et al. 2017; Ioannou et al. 2017b; Kent 2019).”
BackgroundModelling collective behavior in groups of mice housed under semi-naturalistic conditionsPreprint
Chen, X., Winiarski, M. J., Puścian, A., Knapska, E., Mora, T., & Walczak, A. M. (2024) · eLife · doi:10.7554/elife.94999.1 · Cited by 1
Metadata
- Authors
- Katz, Y., Tunstrøm, K., Ioannou, C. C., Huepe, C., & Couzin, I. D.
- Affiliations
- Princeton University (US)
- 614 North Paulina Street, Chicago, IL 60622
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-07-27
- Volume
- 108
- Issue
- 46
- Pages
- 18720-18725
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3219116
- OpenAlex
- W2002266200
- Cited by
- 927
- References
- 54
- Citations by year
- 2026: 50 · 2025: 69 · 2024: 76 · 2023: 80 · 2022: 72 · 2021: 73 · 2020: 76 · 2019: 58 · 2018: 69 · 2017: 57 · 2016: 53 · 2015: 54 · 2014: 46 · 2013: 46 · 2012: 40
- FWCI
- 58.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (publishedVersion)
- KOPS (University of Konstanz) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- National Science Foundation (0848755, 0905970, N00014-09-1-1074)
- Princeton University
- Norges Forskningsråd
- Advanced Research Projects Agency
- Office of Naval Research (N00014-09-1-1074, N00014)
- Topics
- Physical Sciences › Engineering › Control and Systems Engineering › Distributed Control Multi-Agent Systems
- Social Sciences › Safety Research › Evacuation and Crowd Dynamics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- fish schooling, collective behavior, golden shiner, Notemigonus crysoleucas, fish shoals, effective force, speed regulation, alignment, attraction and repulsion, three-body interactions, pairwise interactions, trajectory analysis, social information, group cohesion
- MeSH terms
- Animals, Behavior, Animal, Cyprinidae, Fishes, Models, Biological, Movement, Social Behavior, Software, Swimming, Time Factors
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