TY - JOUR
T1 - Individual and collective encoding of risk in animal groups
AU - Sosna, Matthew M.G.
AU - Twomey, Colin R.
AU - Bak-Coleman, Joseph
AU - Poel, Winnie
AU - Daniels, Bryan C.
AU - Romanczuk, Pawel
AU - Couzin, Iain D.
N1 - Funding Information:
We thank the Couzin Laboratory for helpful discussions. This work was funded by an NSF Graduate Research Fellowship (to M.M.G.S.). C.R.T. was supported by a MindCORE (Center for Outreach, Research, and Education) Postdoctoral Fellowship. P.R. and W.P. were funded by the Deutsche Forschungsgemeinschaft (DFG) (German Research Foundation), Grant RO47766/2-1. P.R. acknowledges funding by the DFG under Germany?s Excellence Strategy?EXC 2002/1 ?Science of Intelligence??Project 390523135. I.D.C. acknowledges support from the NSF (IOS-1355061), the Office of Naval Research (N00014-09-1-1074 and N00014-14-1-0635), the Army Research Office (W911NG-11-1-0385 and W911NF14-1-0431), the Struktur- und Innovationsfunds f?r die Forschung of the State of Baden-W?rttemberg, the Max Planck Society, and the DFG Center of Excellence 2117 ?Center for the Advanced Study of Collective Behavior? (ID: 422037984).
Funding Information:
ACKNOWLEDGMENTS. We thank the Couzin Laboratory for helpful discussions. This work was funded by an NSF Graduate Research Fellowship (to M.M.G.S.). C.R.T. was supported by a MindCORE (Center for Outreach, Research, and Education) Postdoctoral Fellowship. P.R. and W.P. were funded by the Deutsche Forschungsgemeinschaft (DFG) (German Research Foundation), Grant RO47766/2-1. P.R. acknowledges funding by the DFG under Germany’s Excellence Strategy–EXC 2002/1 “Science of Intelligence”–Project 390523135. I.D.C. acknowledges support from the NSF (IOS-1355061), the Office of Naval Research (N00014-09-1-1074 and N00014-14-1-0635), the Army Research Office (W911NG-11-1-0385 and W911NF14-1-0431), the Struktur-und Innovationsfunds für die Forschung of the State of Baden-Württemberg, the Max Planck Society, and the DFG Center of Excellence 2117 “Center for the Advanced Study of Collective Behavior” (ID: 422037984).
Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019/10/8
Y1 - 2019/10/8
N2 - The need to make fast decisions under risky and uncertain conditions is a widespread problem in the natural world. While there has been extensive work on how individual organisms dynamically modify their behavior to respond appropriately to changing environmental conditions (and how this is encoded in the brain), we know remarkably little about the corresponding aspects of collective information processing in animal groups. For example, many groups appear to show increased “sensitivity” in the presence of perceived threat, as evidenced by the increased frequency and magnitude of repeated cascading waves of behavioral change often observed in fish schools and bird flocks under such circumstances. How such context-dependent changes in collective sensitivity are mediated, however, is unknown. Here we address this question using schooling fish as a model system, focusing on 2 nonexclusive hypotheses: 1) that changes in collective responsiveness result from changes in how individuals respond to social cues (i.e., changes to the properties of the “nodes” in the social network), and 2) that they result from changes made to the structural connectivity of the network itself (i.e., the computation is encoded in the “edges” of the network). We find that despite the fact that perceived risk increases the probability for individuals to initiate an alarm, the context-dependent change in collective sensitivity predominantly results not from changes in how individuals respond to social cues, but instead from how individuals modify the spatial structure, and correspondingly the topology of the network of interactions, within the group. Risk is thus encoded as a collective property, emphasizing that in group-living species individual fitness can depend strongly on coupling between scales of behavioral organization.
AB - The need to make fast decisions under risky and uncertain conditions is a widespread problem in the natural world. While there has been extensive work on how individual organisms dynamically modify their behavior to respond appropriately to changing environmental conditions (and how this is encoded in the brain), we know remarkably little about the corresponding aspects of collective information processing in animal groups. For example, many groups appear to show increased “sensitivity” in the presence of perceived threat, as evidenced by the increased frequency and magnitude of repeated cascading waves of behavioral change often observed in fish schools and bird flocks under such circumstances. How such context-dependent changes in collective sensitivity are mediated, however, is unknown. Here we address this question using schooling fish as a model system, focusing on 2 nonexclusive hypotheses: 1) that changes in collective responsiveness result from changes in how individuals respond to social cues (i.e., changes to the properties of the “nodes” in the social network), and 2) that they result from changes made to the structural connectivity of the network itself (i.e., the computation is encoded in the “edges” of the network). We find that despite the fact that perceived risk increases the probability for individuals to initiate an alarm, the context-dependent change in collective sensitivity predominantly results not from changes in how individuals respond to social cues, but instead from how individuals modify the spatial structure, and correspondingly the topology of the network of interactions, within the group. Risk is thus encoded as a collective property, emphasizing that in group-living species individual fitness can depend strongly on coupling between scales of behavioral organization.
KW - Antipredator behavior
KW - Group structure
KW - Social contagion
UR - http://www.scopus.com/inward/record.url?scp=85073049837&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85073049837&partnerID=8YFLogxK
U2 - 10.1073/pnas.1905585116
DO - 10.1073/pnas.1905585116
M3 - Article
C2 - 31548427
AN - SCOPUS:85073049837
VL - 116
SP - 20556
EP - 20561
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 41
ER -