Individual and collective encoding of risk in animal groups

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.