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Collective decision-making appears more egalitarian in populations where group fission costs are higher


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Collective decision-making is predicted to be more egalitarian in conditions where the costs of group fission are higher. Here, we ask whether Trinidadian guppies (Poecilia reticulata) living in high or low predation environments, and thereby facing differential group fission costs, make collective decisions in line with this prediction. Using a classic decision-making scenario, we found that fish from high predation environments switched their positions within groups more frequently than fish from low predation environments. Because the relative positions individuals adopt in moving groups can influence their contribution towards group decisions, increased positional switching appears to support the prediction of more evenly distributed decision-making in populations where group fission costs are higher. In an agent-based model, we further identified that more frequent, asynchronous updating of individuals' positions could explain increased positional switching, as was observed in fish from high predation environments. Our results are consistent with theoretical predictions about the structure of collective decision-making and the adaptability of social decision-rules in the face of different environmental contexts.
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Cite this article: Herbert-Read JE, Wade ASI,
Ramnarine IW, Ioannou CC. 2019 Collective
decision-making appears more egalitarian in
populations where group fission costs are
higher. Biol. Lett. 15: 20190556.
Received: 29 July 2019
Accepted: 20 November 2019
Subject Areas:
behaviour, ecology, evolution
consensus, coordination, information,
Poecilia reticulata
Author for correspondence:
J. E. Herbert-Read
Electronic supplementary material is available
online at
Animal behaviour
Collective decision-making appears more
egalitarian in populations where group
fission costs are higher
J. E. Herbert-Read1,2, A. S. I. Wade3, I. W. Ramnarine4and C. C. Ioannou3
Department of Zoology, University of Cambridge, Cambridge, UK
Department of Biology, Aquatic Ecology Unit, Lund University, Lund, Sweden
School of Biological Sciences, Bristol University, Bristol, UK
Department of Life Sciences, The University of the West Indies, St Augustine, Trinidad and Tobago
JEH-R, 0000-0003-0243-4518; CCI, 0000-0002-9739-889X
Collective decision-making is predicted to be more egalitarian in conditions
where the costs of group fission are higher. Here, we ask whether Trinida-
dian guppies (Poecilia reticulata) living in high or low predation
environments, and thereby facing differential group fission costs, make
collective decisions in line with this prediction. Using a classic decision-
making scenario, we found that fish from high predation environments
switched their positions within groups more frequently than fish from low
predation environments. Because the relative positions individuals adopt
in moving groups can influence their contribution towards group decisions,
increased positional switching appears to support the prediction of more
evenly distributed decision-making in populations where group fission
costs are higher. In an agent-based model, we further identified that more
frequent, asynchronous updating of individualspositions could explain
increased positional switching, as was observed in fish from high predation
environments. Our results are consistent with theoretical predictions about
the structure of collective decision-making and the adaptability of social
decision-rules in the face of different environmental contexts.
1. Introduction
Collective decisions involve individuals in groups combining their own imper-
fect estimates of the world around them to reach consensuses about travel
directions, activities or choices while, at the same time, remaining cohesive
[1]. In many cases, if animals are to benefit from such information sharing,
they should distribute decision-making evenly between group members [1].
However, because conflict exists in groups, where individuals have to balance
the need for social cohesion with that of their own goal-oriented behaviour
[14], some individuals may disproportionally influence the decision-making
process, through either active or passive mechanisms.
Theoretical models suggest that the degree to which decision-making is
shared between group members is influenced by both environmental and
social conditions [5,6]. In environments where the benefits of remaining with
other group members outweigh any potential consensus costs, that is, costs
of following othersdecisions, then equally shared decision-making is more
likely to evolve [7,8]. Unshared decision-making, on the other hand, is more
likely to evolve when consensus costs are relatively high compared with the
benefits of social cohesion [7,8]. Importantly, under both these scenarios, the
observed outcome of decision-making can often be the same, where groups
remain cohesive despite consensus being reached by relatively shared or
unshared decision-making processes.
© 2019 The Author(s) Published by the Royal Society. All rights reserved.
Investigating these theoretical predictions requires an
experimental system where either the consensus costs or
group cohesion costs differ between populations, and the
degree to which decisions are shared or unshared can be
approximated. The Trinidadian guppy (Poecilia reticulata)
offers one such system. Populations of guppies in the Northern
Mountain range of Trinidad have been exposed to either
relatively high or relatively low levels of predation over
both their evolutionary and ontogenetic histories [9,10].
Because group cohesion significantly reduces predation risk
[11,12], this system offers an opportunity to assess whether
group decision-making appears more or less shared between
group members in populations where the costs of group
fragmentation differ. Here, we give groups of guppies a clas-
sic decision-making paradigm [13,14], where groups choose
to swim down one of two arms of a Y-maze. We tested mul-
tiple group sizes to assess whether the patterns observed
were robust to differences in group size. Because positions
at the front of groups are more conducive of leadership,
and in many animal groups information flows from the
front to the back of groups, [1517], positional changes
within groups appear to be informative about who is dispro-
portionally influencing the decision-making process [13,18].
We therefore calculated the number of times individuals
switched positions within the group before they reached a
decision, with increased positional switching acting as a
proxy for more distributed decision-making. Furthermore,
using a simple one-dimensional model, we explored how
differences in how individuals moved might result in different
amounts of positional switching within groups.
2. Material and methods
(a) Experimental methods
Adult female guppies (P. reticulata) were caught from four
locations with high predation risk (Arima, Lower Guanapo,
Lower Lopinot and Tacarigua rivers) and four locations with
low predation risk (Paria, Upper Guanapo, Upper Lopinot and
Upper Turure rivers) in July 2013. High predation sites contain
Crenicichla frenata,Hoplias malabaricus or Aequidens pulcher
which prey on adult guppies, whereas these predators are largely
absent from low predation sites, although low predation sites do
contain Rivulus hartii which prey on juvenile guppies [9,18].
Fish were transported back to the University of the West
Indies, St Augustine Campus, where they were housed in
120 cm diameter circular holding pools (approx. 90 fish per
pool) in an outdoor enclosure that was shaded between 08.00
and 14.00 h (when trials were run). Water depth in the pools
was maintained between 10 and 13 cm, and the pools were emp-
tied, rinsed and refilled between stocking fish from different
populations. We suspended a clear polythene sheet over the
housing pools and test arena throughout the study to stop rain
falling in the pools.
For each trial, groups of two, four or eight fish with approxi-
mately the same body length were caught from the housing
pools and placed into a 15 × 15 cm transparent plastic box at
the end of the stem of a Y-maze (stem 15 cm wide, 71 cm long;
figure 1a). Following 2 min of acclimation, the box was remotely
lifted, allowing the shoals to explore the novel maze environ-
ment. Groups swam down the stem of the Y-maze before
deciding to swim into the left or right arm of the maze. Trials
were filmed with a Canon 550D DSLR camera mounted 1.25 m
above the maze at 25 fps and a resolution of 1920 × 1080 pixels.
We tested group sizes of two (n= 77), four (n= 76) or eight
(n= 77) fish, with each group size being tested once in a block
of three trials, and the order of testing randomized within each
block. Fish were never used in more than one trial. We used
automated tracking software [19] to track the positions and
orientations of fish as they made a decision. In particular, we
measured the number of times the group did not reach a consen-
sus (defined when at least two group members chose different
arms of the Y-maze to swim down), the mean speed of fish,
their cohesion (median distance of group members to the
groups centroid), the number of times they switched position
(see Results) and the number of movement decisions fish made
per second (see Results). All measures were calculated from the
time a fish entered the blue region in figure 1auntil a fish crossed
into one of the arms of the Y-maze (dashed white lines in
figure 1a). Group cohesion was only measured during times
no gravel
low predation
total number of switches
high predation
group size
Figure 1. (a) The experimental Y-maze. Tracking is superimposed on a frame for one of the trials of eight fish. The numbers next to each fish represent their
positional ranks within the group on that frame. The left arm of the Y-maze contained a gravel patch (off-screen), while the right arm contained no patch. This was
designed to create an asymmetric choice. (b) Boxplots of the total number of times individuals switched position in the group. Raw data points are shown as grey
circles. The central line on each box depicts the median, and the top and bottom edges of each box represent the 25th and 75th percentiles. Whiskers extend to
data points not considered outliers. Biol. Lett. 15: 20190556
when all group members were simultaneously tracked. All
measures were analysed using linear or generalized linear
mixed models (see electronic supplementary material for
further details). All models included predation regime (high
or low), group size and the mean body size of fish (standard
length measured from stills in the videos) in each group
as fixed effects. As expected, fish from high predation popu-
lations were significantly smaller (2.02 ± 0.48 cm, mean ± s.d.)
than fish from low predation populations (2.29 ± 0.36 cm,
mean ± s.d.; linear mixed model, likelihood ratio test (LRT):
28.97, p< 0.001), making body size an important covariate in
our models. Population was included as a random effect in
all models. The significance of each term within the models
was tested using LRTs to compare models with and without
the term of interest. All statistical analyses were carried out in
R v.3.1.2, and data are available in the electronic supplementary
3. Results
The proportion of groups that split apart during the decision-
making process did not differ between the two predation
regimes (LRT = 1.61, p= 0.20; only 33/231 groups split). Fur-
thermore, fish from the different predation regimes did not
differ in their median swim speeds as they made these
decisions (LRT = 0.42, p= 0.52). Groups of fish from high
and low predation environments, therefore, made similarly
fast and cohesive decisions.
We next investigated whether individuals within groups
from different predation regimes contributed to the consensus
decisions more or less equally. To measure this, fish were
ranked from 1 to nas they swam down the stem of the Y-
maze (shaded blue region in figure 1a), with fish at the front
of the group given a ranking of 1 and the fish at the back of
the group, n(figure 1a). We then calculated the number of
times these ranks changed in the times leading up to the final
decision (when the first fish crossed a dashed line in figure 1a).
Note that if a pair of fish switched their positions, this was
counted as two switches, and we controlled for potential differ-
ences in cohesion between the populations by including
cohesion as a covariate in the models. Fish from high predation
environments switched position more often than fish from low
predation environments (LRT = 5.12, p=0.024; figure 1b),
and as expected, larger groups also made more switches than
smaller groups (LRT = 122.8, p<0.001; figure 1b). These effects
were also observed when considering only switches that
occurred at the front position of the group (predation: LRT =
7.07, p< 0.01; group size: LRT = 20.28, p<0.001).
We then investigated the potential mechanism for how
fish from high-predation environments made more switches
in positions than fish from low predation environments. Gup-
pies, as in many other species of fish, move with intermittent
changes in speed, which can be thought of as movement
decisions [20]. We identified the number of movement
decisions that fish made per second by identifying the
times when fishs speeds were at a minimum (see grey mar-
kers in figure 2a). After controlling for the effects of median
speed (LRT = 197.6, p< 0.001) and body size (LRT = 22.1,
p< 0.001), fish from high predation environments still made
more decisions per second than fish from low predation
environments (LRT = 4.31, p= 0.038; figure 2b).
To test whether differences in the rate at which fish
updated their position could explain differential switching
behaviour between the populations, we built a simple one-
dimensional self-propelled particle model capturing the
dynamics of guppiesmovements. On each time step,
agents updated their position along an one-dimensional
world with a probability, p, that was determined by the
mean update frequency of fish in either low ( p= 0.0368) or
high ( p= 0.0463) predation environments (figure 2b). If fish
updated their position, they moved for a uniformly randomly
determined distance in the range, 0d(where d> 0). The only
social interaction we implemented was an attraction rule to
neighbours behind a focal individual, that is, if the focal indi-
vidual was in front of its closest follower by more than d,it
did not update its position. One hundred simulation runs
were performed for the same relative number of time steps
it took fish to make the decision for each experimental trial
(n= 231 × 100). This simple model captured the switching
rates observed in the experimental trials, with agents with
higher update probabilities switching position more often
than agents with low update probabilities (figure 2c).
speed (mm s–1)
decisions per second
no. switches
3.0 low predation simulated low update
simulated high update
high predation
time (s)
roup size 248
roup size
Figure 2. (a) Example speed profile of a fish as it moved through the Y-maze. Grey markers represent times when the speed profile has local minima, indicating
times immediately before the fish made a decision to move. (b) Boxplot of the number of decisions fish made per second as a function of group size and low (grey)
or high (blue) predation environments. (c) Results of the simulation where each point represents the average switches a group made out of 100 simulation runs.
Simulations were given two update frequencies: low (grey) or high (blue), respectively, matching the update frequency of fish from low or high predation environ-
ments. The central line on each box depicts the median, and the top and bottom edges of each box represent the 25th and 75th percentiles. Whiskers extend to
data points not considered outliers. Biol. Lett. 15: 20190556
4. Discussion
Groups of fish from high predation environments switched
positions more often, and made more movement decisions
per second, than fish from low predation environments. In
a simple agent-based model, the increased frequency of asyn-
chronous movement decisions was associated with this
increased positional switching. These results are consistent
with theoretical predictions that collective decision-making is
more equally shared between group members in environments
where the costs of group fission are higher [7,8].
Oscillations in speed and switching of positions are
thought to break visual occlusion between group members,
thereby facilitating the more efficient spread of information
through groups [21]. Mechanisms that promote the likelihood
that multiple individuals contribute towards detecting and
sharing information about potential sources of risk, therefore,
might be favoured in environments where those threats are
higher. Indeed, such mechanisms could allow the collective
pooling of information and the emergence of swarm intelli-
gence [22], especially when information collected by group
members is uncorrelated [23,24]. While, in our model,
increased asynchronous movements could explain increased
positional switching, more frequent movements are also
likely to be coupled with increased energetic requirements.
This may explain why increased positional switching may
not be adopted in environments where information sharing
might be less important, such as when predation risk is
relatively lower.
While we interpret our results in the context of decision-
making, it is important to consider other mechanisms that
could contribute towards increased positional switching in
high compared with low predation environments. Higher
sensitivity to risk [25], swimming performance [26] or
trade-offs in occupying rewarding yet risky positions in
groups [12] may contribute towards increased positional
switching in high compared with low predation environ-
ments. While these factors are not mutually exclusive from
more or less distributed decision-making processes, future
work should attempt to control for these factors when inves-
tigating the importance of positional switching during
decision-making. Our work suggests, however, that popu-
lations have intrinsic differences in the degree to which
decision-making is shared between group members, and
this could be ultimately shaped by differences in the ecologi-
cal conditions that these populations experience.
Ethics. All procedures were approved by the University of Bristol
Ethical Review Group (UIN 13/028).
Data accessibility. Data available from the Dryad Digital Repository: [27].
Authorscontributions. J.E.H.-R., A.S.I.W. and C.C.I. contributed to the
conception and design of experiments. A.S.I.W. and C.C.I. contribu-
ted to the acquisition of data. J.E.H.-R., A.S.I.W., I.W.R. and C.C.I.
contributed to the analysis and interpretation of data. All authors
contributed intellectual content to drafting the article and revising
it critically. All authors approved the final version of the manuscript
and agree to be held accountable for the content therein.
Competing interests. The authors declare they have no conflicts of interest.
Funding. This work was supported by the Natural Environment
Research Council grants nos NE/K009370/1 and NE/P012639/1
awarded to C.C.I. and a Swedish Research Council grant no. 2018-
04076 awarded to J.E.H.-R.
Acknowledgements. We thank Kharran Deonarinesingh and Dr Matthew
Edenbrow for support and helpful discussions, and Dr Kurvers and
two anonymous reviewers for their critiques of our work.
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Despite extensive interest in the dynamic interactions between individuals that drive collective motion in animal groups, the dynamics of collective motion over longer time frames are understudied. Using three-spined sticklebacks, Gasterosteus aculeatus, randomly assigned to 12 shoals of eight fish, we tested how six key traits of collective motion changed over shorter (within trials) and longer (between days) timescales under controlled laboratory conditions. Over both timescales, groups became less social with reduced cohesion, polarization, group speed and information transfer. There was consistent inter-group variation (i.e. collective personality variation) for all collective motion parameters, but groups also differed in how their collective motion changed over days in their cohesion, polarization, group speed and information transfer. This magnified differences between groups, suggesting that over time the ‘typical’ collective motion cannot be easily characterized. Future studies are needed to understand whether such between-group differences in changes over time are adaptive and represent improvements in group performance or are suboptimal but represent a compromise between individuals in their preferences for the characteristics of collective behaviour.
... 11,[15][16][17] How these local interactions manifest in group level dynamics has been established in various fish species that display robust schooling and shoaling. 11,15,[18][19][20][21][22][23] However, how evolution impacts these local interaction rules to produce group level differences in collective behaviors is poorly understood. Establishing how changes to individual behaviors lead to variation in collective motion is critical to revealing how collective behaviors evolve in natural populations. ...
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Collective motion emerges from individual interactions which produce group-wide patterns in behavior. While adaptive changes to collective motion are observed across animal species, how local interactions change when these collective behaviors evolve is poorly understood. Here, we use the Mexican tetra, Astyanax mexicanus, which exists as a schooling surface form and a non-schooling cave form, to study differences in how fish alter their swimming in response to neighbors across ontogeny and between evolutionarily diverged populations. We find that surface fish undergo a transition to schooling mediated by changes in the way fish modulate speed and turning relative to neighbors. This transition begins with the tendency to align to neighbors emerging by 28 days post-fertilization and ends with the emergence of robust attraction by 70 days post-fertilization. Cavefish exhibit neither alignment nor attraction at any stage of development. These results reveal how evolution alters local interactions to produce striking differences in collective behavior.
... Methods include: biologgers or mounted video to record changes in animal behaviour indicative of predator selection or prey detection (Watanabe & Takahashi, 2013;Lynch et al., 2015;Williams et al., 2017;Watanabe et al., 2019;Wilson et al., 2020;Ryan et al., 2022a); computer vision-tracking software (Dell et al., 2014;Couzin & Heins, 2022;Koger et al., 2023); and unmanned aerial vehicles (UAVs), global positioning system (GPS) and accelerometers to record spatiotemporal data (Shubkina et al., 2010;Strandburg-Peshkin et al., 2015, 2017 Biological Reviews (2023) Christie et al., 2016;Harvey et al., 2016;Hodgson & Koh, 2016;Hubel et al., 2016b,a;Marras et al., 2015b;Jackson et al., 2016;Handley et al., 2018;Torney et al., 2018;Westley et al., 2018;Wilson et al., 2018;Hughey et al., 2018;King et al., 2018;Couzin & Heins, 2022;Hansen et al., 2022;Koger et al., 2023). Differences in predator locomotion and within-group position may indeed correspond to changes in informational state (Bode et al., 2010;Shubkina et al., 2010Shubkina et al., , 2012Herbert-Read et al., 2019) and network-based diffusion analysis (Franz & Nunn, 2009;Hoppitt, 2017) or methodology borrowed from information theory and tested in laboratory animals Hansen et al., 2021;Burns et al., 2022) can then assess if these state changes are transferred socially (Fig. 4B). ...
Group-hunting is ubiquitous across animal taxa and has received considerable attention in the context of its functions. By contrast much less is known about the mechanisms by which grouping predators hunt their prey. This is primarily due to a lack of experimental manipulation alongside logistical difficulties quantifying the behaviour of multiple predators at high spatiotemporal resolution as they search, select, and capture wild prey. However, the use of new remote-sensing technologies and a broadening of the focal taxa beyond apex predators provides researchers with a great opportunity to discern accurately how multiple predators hunt together and not just whether doing so provides hunters with a per capita benefit. We incorporate many ideas from collective behaviour and locomotion throughout this review to make testable predictions for future researchers and pay particular attention to the role that computer simulation can play in a feedback loop with empirical data collection. Our review of the literature showed that the breadth of predator:prey size ratios among the taxa that can be considered to hunt as a group is very large (<100 to >102 ). We therefore synthesised the literature with respect to these predator:prey ratios and found that they promoted different hunting mechanisms. Additionally, these different hunting mechanisms are also related to particular stages of the hunt (search, selection, capture) and thus we structure our review in accordance with these two factors (stage of the hunt and predator:prey size ratio). We identify several novel group-hunting mechanisms which are largely untested, particularly under field conditions, and we also highlight a range of potential study organisms that are amenable to experimental testing of these mechanisms in connection with tracking technology. We believe that a combination of new hypotheses, study systems and methodological approaches should help push the field of group-hunting in new directions.
... Early studies revealed that guppies from sites with high-predation pressure form larger shoals [137]. More recently, comparing guppies from rivers varying in predation risk has demonstrated differences in their fine-scale interindividual interactions during collective motion [138], and in collective decision making when tested both in situ in the field [139] and under standardized conditions [140]. Further evidence that collective behaviour adapts to local environmental conditions within species comes from the Mexican tetra (Astyanax mexicanus), where ancestral populations live in rivers exposed to light (surface populations) and show attraction and alignment to their neighbours, while multiple populations of this species have independently adapted to live in dark caves and show avoidance of conspecifics [141]. ...
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Collective behaviours, such as flocking in birds or decision making by bee colonies, are some of the most intriguing behavioural phenomena in the animal kingdom. The study of collective behaviour focuses on the interactions between individuals within groups, which typically occur over close ranges and short timescales, and how these interactions drive larger scale properties such as group size, information transfer within groups and group-level decision making. To date, however, most studies have focused on snapshots, typically studying collective behaviour over short timescales up to minutes or hours. However, being a biological trait, much longer timescales are important in animal collective behaviour, particularly how individuals change over their lifetime (the domain of developmental biology) and how individuals change from one generation to the next (the domain of evolutionary biology). Here, we give an overview of collective behaviour across timescales from the short to the long, illustrating how a full understanding of this behaviour in animals requires much more research attention on its developmental and evolutionary biology. Our review forms the prologue of this special issue, which addresses and pushes forward understanding the development and evolution of collective behaviour, encouraging a new direction for collective behaviour research. This article is part of a discussion meeting issue ‘Collective behaviour through time’.
... Although much slower swimming speeds were exhibited in the latter treatment, both scenarios likely led to increased vigilance, as they are non-natural situations that would alarm individuals. Previous research has shown that group organization tends to increase under alarming situations (Schaerf et al., 2017), and that collective decision-making can differ between populations from high-versus low-risk environments (Herbert-Read et al., 2019). Thus, our investigation examines how groups of each species organize during collective motion in somewhat confined environments under heightened vigilance. ...
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Collective behaviors in biological systems such as coordinated movements have important ecological and evolutionary consequences. While many studies examine within‐species variation in collective behavior, explicit comparisons between functionally similar species from different taxonomic groups are rare. Therefore, a fundamental question remains: how do collective behaviors compare between taxa with morphological and physiological convergence, and how might this relate to functional ecology and niche partitioning? We examined the collective motion of two ecologically similar species from unrelated clades that have competed for pelagic predatory niches for over 500 million years—California market squid, Doryteuthis opalescens (Mollusca) and Pacific sardine, Sardinops sagax (Chordata). We (1) found similarities in how groups of individuals from each species collectively aligned, measured by angular deviation, the difference between individual orientation and average group heading. We also (2) show that conspecific attraction, which we approximated using nearest neighbor distance, was greater in sardine than squid. Finally, we (3) found that individuals of each species explicitly matched the orientation of groupmates, but that these matching responses were less rapid in squid than sardine. Based on these results, we hypothesize that information sharing is a comparably important function of social grouping for both taxa. On the other hand, some capabilities, including hydrodynamically conferred energy savings and defense against predators, could stem from taxon‐specific biology.
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The movement of groups can be heavily influenced by 'leader' individuals who differ from the others in some way. A major source of differences between individuals is the repeatability and consistency of their behaviour, commonly considered as their 'personality', which can influence both position within a group as well as the tendency to lead. However, links between personality and behaviour may also depend upon the immediate social environment of the individual; individuals who behave consistently in one way when alone may not express the same behaviour socially, when they may be conforming with the behaviour of others. Experimental evidence shows that personality differences can be eroded in social situations, but there is currently a lack of theory to identify the conditions where we would expect personality to be suppressed. Here, we develop a simple individual-based framework considering a small group of individuals with differing tendencies to perform risky behaviours when travelling away from a safe home site towards a foraging site, and compare the group behaviours when the individuals follow differing rules for aggregation behaviour determining how much attention they pay to the actions of their fellow group-members. We find that if individuals pay attention to the other members of the group, the group will tend to remain at the safe site for longer, but then travel faster towards the foraging site. This demonstrates that simple social behaviours can result in the repression of consistent inter-individual differences in behaviour, giving the first theoretical consideration of the social mechanisms behind personality suppression.
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Collective decision-making constitutes a core function of social systems and is, therefore, a central tenet of collective intelligence research. From fish schools to human crowds, we start by interrogating ourselves about the very definition of collective decision-making and the scope of the scientific research that falls under it. We then summarize its history through the lenses of social choice theory and swarm intelligence and their accelerating collaboration over the past 20 or so years. Finally, we offer our perspective on the future of collective decision-making research in 3 mutually inclusive directions. We argue (1) that the possibility to collect data of a new nature, including fine-grain tracking information, virtual reality, and brain imaging inputs, will enable a direct link between plastic individual cognitive processes and the ontogeny of collective behaviors; (2) that current theoretical frameworks are not well suited to describe the long-term consequences of individual plasticity on collective decision-making processes and that, therefore, new formalisms are necessary; and finally (3) that applying the results of collective decision-making research to real-world situations will require the development of practical tools, the implementation of monitoring processes that respect civil liberties, and, possibly, government regulations of social interventions by public and private actors.
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Studying animal behavior as collective phenomena is a powerful tool for understanding social processes, including group coordination and decision-making. However, linking individual behavior during group decision-making to the preferences underlying those actions poses a considerable challenge. Optimal foraging theory, and specifically the marginal value theorem (MVT), can provide predictions about individual preferences, against which the behavior of groups can be compared under different models of influence. A major strength of formally linking optimal foraging theory to collective behavior is that it generates predictions that can easily be tested under field conditions. This opens the door to studying group decision-making in a range of species; a necessary step for revealing the ecological drivers and evolutionary consequences of collective decision-making.
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Many animal groups exhibit signatures of persistent internal modular structure, whereby individuals consistently interact with certain groupmates more than others. In such groups, information relevant to a collective decision may spread unevenly through the group, but how this impacts the quality of the resulting decision is not well understood. Here, we explicitly model modularity within animal groups and examine how it affects the amount of information represented in collective decisions, as well as the accuracy of those decisions. We find that modular structure necessarily causes a loss of information, effectively silencing the input from a fraction of the group. However, the effect of this information loss on collective accuracy depends on the informational environment in which the decision is made. In simple environments, the information loss is detrimental to collective accuracy. By contrast, in complex environments, modularity tends to improve accuracy. This is because small group sizes typically maximize collective accuracy in such environments, and modular structure allows a large group to behave like a smaller group (in terms of its decision-making). These results suggest that in naturalistic environments containing correlated information, large animal groups may be able to exploit modular structure to improve decision accuracy while retaining other benefits of large group size. This article is part of the theme issue ‘Liquid brains, solid brains: How distributed cognitive architectures process information’.
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Significance Across a wide range of animals, it is assumed that leading from the front of a group exposes individuals to greater predation risk, generating a cost that explains variation between individuals in their tendencies to lead and follow. Remarkably, there is scant empirical evidence to support this, and there are no experimental tests. By presenting real predators with a simulation of collective behavior, we were able to exclude any correlation between social behavior and other traits that could confound effects on predation risk. We show that virtual prey leading others were preferentially attacked, but leaders were still safer than solitary prey. Leaders benefit from being followed, and they should act to maintain group cohesion and avoid splitting from their followers.
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Although consistent behavioural differences between individuals (i.e. personality variation) are now well established in animals, these differences are not always expressed when individuals interact in social groups. This can be key in important social dynamics such as leadership, which is often positively related to personality traits such as boldness. Individuals consistently differ in how social they are (their sociability), so if other axes of personality variation, such as boldness, can be suppressed during social interactions, this suppression should be stronger in more sociable individuals. We measured boldness (latency to leave a refuge when alone) and sociability (time spent with a conspecific) in three-spined sticklebacks (Gasterosteus aculeatus) and tested the boldness-leadership association in pairs of these fish. Both boldness and sociability were repeatable, but were not correlated. When splitting the data between the 50% most sociable and 50% less sociable fish, boldness was more strongly associated with leadership in less rather than more sociable individuals. This is consistent with more sociable fish conforming to their partner's behaviour due to their greater social tendency. One axis of personality variation (sociability) can thus modulate the relationship between others (boldness and leadership), with potential implications for selection on personality variation in social animals.
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Predation is thought to shape the macroscopic properties of animal groups, making moving groups more cohesive and coordinated. Precisely how predation has shaped individuals' fine-scale social interactions in natural populations, however, is unknown. Using high-resolution tracking data of shoaling fish (Poecilia reticulata) from populations differing in natural predation pressure, we show how predation adapts individuals' social interaction rules. Fish originating from high predation environments formed larger, more cohesive, but not more polarized groups than fish from low predation environments. Using a new approach to detect the discrete points in time when individuals decide to update their movements based on the available social cues, we determine how these collective properties emerge from individuals' microscopic social interactions. We first confirm predictions that predation shapes the attraction–repulsion dynamic of these fish, reducing the critical distance at which neighbours move apart, or come back together. While we find strong evidence that fish align with their near neighbours, we do not find that predation shapes the strength or likelihood of these alignment tendencies. We also find that predation sharpens individuals' acceleration and deceleration responses, implying key perceptual and energetic differences associated with how individuals move in different predation regimes. Our results reveal how predation can shape the social interactions of individuals in groups, ultimately driving differences in groups' collective behaviour.
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Collective decisions play a major role in the benefits that animals gain from living in groups. Although the mechanisms of how groups collectively make decisions have been extensively researched, the response of within-group dynamics to ecological conditions is virtually unknown, despite adaptation to the environment being a cornerstone in biology. We investigate how within-group interactions during exploration of a novel environment are shaped by predation, a major influence on the behavior of prey species. We tested guppies (Poecilia reticulata) from rivers varying in predation risk under controlled laboratory conditions and find the first evidence of differences in group interactions between animals adapted to different levels of predation. Fish from high-predation habitats showed the strongest negative relationship between initiating movements and following others, which resulted in less variability in the total number of movements made between individuals. This relationship between initiating movements and following others was associated with differentiation into initiators and followers, which was only observed in fish from high-predation rivers. The differentiation occurred rapidly, as trials lasted 5 min, and was related to shoal cohesion, where more diverse groups from high-predation habitats were more cohesive. Our results show that even within a single species over a small geographical range, decision-making in a social context can vary with local ecological factors.
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Larger groups often have a greater ability to solve cognitive tasks compared to smaller ones or lone individuals. This is well established in social insects, navigating flocks of birds, and in groups of prey collectively vigilant for predators. Research in social insects has convincingly shown that improved cognitive performance can arise from self-organised local interactions between individuals that integrates their contributions, often referred to as swarm intelligence. This emergent collective intelligence has gained in popularity and been directly applied to groups of other animals, including fish. Despite being a likely mechanism at least partially explaining group performance in vertebrates, I argue here that other possible explanations are rarely ruled out in empirical studies. Hence, evidence for self-organised collective (or ‘swarm’) intelligence in fish is not as strong as it would first appear. These other explanations, the ‘pool-of-competence’ and the greater cognitive ability of individuals when in larger groups, are also reviewed. Also discussed is why improved group performance in general may be less often observed in animals such as shoaling fish compared to social insects. This review intends to highlight the difficulties in exploring collective intelligence in animal groups, ideally leading to further empirical work to illuminate these issues.
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A key question in collective behavior is how individual differences structure animal groups, affect the flow of information, and give some group members greater weight in decisions [1-8]. Depending on what factors contribute to leadership, despotic decisions could either improve decision accuracy or interfere with swarm intelligence [9, 10]. The mechanisms behind leadership are therefore important for understanding its functional significance. In this study, we compared pigeons' relative influence over flock direction to their solo flight characteristics. A pigeon's degree of leadership was predicted by its ground speeds from earlier solo flights, but not by the straightness of its previous solo route. By testing the birds individually after a series of flock flights, we found that leaders had learned straighter homing routes than followers, as we would expect if followers attended less to the landscape and more to conspecifics. We repeated the experiment from three homing sites using multiple independent flocks and found individual consistency in leadership and speed. Our results suggest that the leadership hierarchies observed in previous studies could arise from differences in the birds' typical speeds. Rather than reflecting social preferences that optimize group decisions, leadership may be an inevitable consequence of heterogeneous flight characteristics within self-organized flocks. We also found that leaders learn faster and become better navigators, even if leadership is not initially due to navigational ability. The roles that individuals fall into during collective motion might therefore have far-reaching effects on how they learn about the environment and use social information.
We examine the spatial dynamics of individuals in small schools of banded killifish (Fundulus diaphanus) that exhibit rhythmic, oscillating speed, typically with sustained, coordinated, out-of-phase speed oscillations as they move around a shallow water tank. We show that the relative motion among the fish yields a periodically time-varying network of social interactions that enriches visually driven social communication. The oscillations lead to the regular making and breaking of occlusions, which we term “switching.” We show that the rate of convergence to consensus (biologically, the capacity for individuals in groups to achieve effective coordinated motion) governed by the switching outperforms static alternatives, and performs as well as the less practical case of every fish sensing every other fish. We show further that the oscillations in speed yield oscillations in relative bearing between fish over a range that includes the angles previously predicted to be optimal for a fish to detect changes in heading and speed of its neighbors. To investigate systematically, we derive and analyze a dynamic model of interacting agents that move with oscillatory speed. We show that coordinated circular motion of the school leads to systematic cycling of spatial ordering of agents and possibilities for enriched spatial density of measurements of the external environment. Our results highlight the potential benefits of dynamic communication topologies in collective animal behavior, and suggest new, useful control laws for the distributed coordination of mobile robotic networks.