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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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Research
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.
http://dx.doi.org/10.1098/rsbl.2019.0556
Received: 29 July 2019
Accepted: 20 November 2019
Subject Areas:
behaviour, ecology, evolution
Keywords:
consensus, coordination, information,
Poecilia reticulata
Author for correspondence:
J. E. Herbert-Read
e-mail: james.herbert.read@gmail.com
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.4772591.
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
1
Department of Zoology, University of Cambridge, Cambridge, UK
2
Department of Biology, Aquatic Ecology Unit, Lund University, Lund, Sweden
3
School of Biological Sciences, Bristol University, Bristol, UK
4
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
gravel
low predation
total number of switches
high predation
80
0
284
group size
20
13
5
4
67
8
240
60
(a)(b)
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.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 15: 20190556
2
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
material.
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).
120
speed (mm s–1)
decisions per second
no. switches
3.0 low predation simulated low update
simulated high update
high predation
150
0
50
100
0
0.5
1.0
1.5
2.0
2.5
010
248
9876
time (s)
g
roup size 248
g
roup size
54321
20
40
60
80
100
(a)(b)(c)
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.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 15: 20190556
3
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:
https://doi.org.10.5061/dryad.nvx0k6dn6 [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.
References
1. Conradt L, Roper TJ. 2005 Consensus decision
making in animals. Trends Ecol. Evol. 20, 449456.
(doi:10.1016/j.tree.2005.05.008)
2. Conradt L, Roper TJ. 2003 Group decision-making in
animals. Nature 421, 155. (doi:10.1038/
nature01294)
3. Conradt L, List C. 2008 Group decisions in humans
and animals: a survey. Phil. Trans. R. Soc. B 364,
719742. (doi:10.1098/rstb.2008.0276)
4. Bevan PA, Gosetto I, Jenkins ER, Barnes I, Ioannou
CC. 2018 Regulation between personality traits:
individual social tendencies modulate whether
boldness and leadership are correlated. Proc. R. Soc.
B285, 20180829. (doi:10.1098/rspb.2018.0829)
5. Johnstone RA, Manica A. 2011 Evolution of
personality differences in leadership. Proc. Natl
Acad. Sci. USA 108, 83738378. (doi:10.1073/pnas.
1102191108)
6. Wolf M, Van Doorn GS, Weissing FJ. 2008
Evolutionary emergence of responsive and
unresponsive personalities. Proc. Natl Acad. Sci. USA
105, 15 82515 830. (doi:10.1073/pnas.
0805473105)
7. Conradt L, Roper TJ. 2008 Conflicts of interest and
the evolution of decision sharing. Phil. Trans. R. Soc.
B364, 807819. (doi:10.1098/rstb.2008.0257)
8. Conradt L. 2011 Models in animal collective
decision-making: information uncertainty and
conflicting preferences. Interface Focus 2, 226240.
(doi:10.1098/rsfs.2011.0090)
9. Magurran AE. 2005 Evolutionary ecology: the
Trinidadian guppy. Oxford, UK: Oxford University Press.
10. Seghers BH. 1974 Schooling behavior in the guppy
(Poecilia reticulata): an evolutionary response to
predation. Evolution 28, 486489. (doi:10.1111/j.
1558-5646.1974.tb00774.x)
11. Ioannou CC, Guttal V, Couzin ID. 2012 Predatory fish
select for coordinated collective motion in virtual
prey. Science 337, 12121215. (doi:10.1126/science.
1218919)
12. Ioannou CC, Rocque F, Herbert-Read JE, Duffield C,
Firth JA. 2019 Predators attacking virtual
prey reveal the costs and benefits of leadership.
Proc. Natl Acad. Sci. USA 116, 89258930. (doi:10.
1073/pnas.1816323116)
13. Burns AL, Herbert-Read JE, Morrell LJ, Ward AJ.
2012 Consistency of leadership in shoals of
mosquitofish (Gambusia holbrooki) in novel and in
familiar environments. PLoS ONE 7, e36567. (doi:10.
1371/journal.pone.0036567)
14. Ward AJ, Herbert-Read JE, Sumpter DJ, Krause J.
2011 Fast and accurate decisions through
collective vigilance in fish shoals. Proc. Natl Acad.
Sci. USA 108, 23122315. (doi:10.1073/pnas.
1007102108)
15. Pettit B, Ákos Z, Vicsek T, Biro D. 2015 Speed
determines leadership and leadership determines
learning during pigeon flocking. Curr. Biol. 25,
31323137. (doi:10.1016/j.cub.2015.10.044)
16. Nagy M, Akos Z, Biro D, Vicsek T. 2010 Hierarchical
group dynamics in pigeon flocks. Nature 464, 890.
(doi:10.1038/nature08891)
17. Herbert-Read JE, Perna A, Mann RP, Schaerf TM,
Sumpter DJ, Ward AJ. 2011 Inferring the rules of
interaction of shoaling fish. Proc. Natl Acad. Sci. USA
108,1872618 731. (doi:10.1073/pnas.1109355108)
18. Ioannou CC, Ramnarine IW, Torney CJ. 2017
High-predation habitats affect the social dynamics of
collective exploration in a shoaling fish. Sci. Adv. 3,
e1602682. (doi:10.1126/sciadv.1602682)
19. Branson K, Robie AA, Bender J, Perona P, Dickinson
MH. 2009 High-throughput ethomics in large
groups of Drosophila.Nat. Methods 6, 451. (doi:10.
1038/nmeth.1328)
20. Herbert-Read JE et al. 2017 How predation shapes
the social interaction rules of shoaling fish.
Proc. R. Soc. B 284, 20171126. (doi:10.1098/rspb.
2017.1126)
royalsocietypublishing.org/journal/rsbl Biol. Lett. 15: 20190556
4
21. Swain DT, Couzin ID, Leonard NE. 2015
Coordinated speed oscillations in schooling
killifish enrich social communication. J. Nonlinear
Sci. 25, 10771109. (doi:10.1007/s00332-015-
9263-8)
22. Ioannou CC. 2017 Swarm intelligence in fish?
The difficulty in demonstrating distributed and
self-organised collective intelligence in (some)
animal groups. Behav. Process. 141, 141151.
(doi:10.1016/j.beproc.2016.10.005)
23. Kao AB, Couzin ID. 2014 Decision accuracy in
complex environments is often maximized by small
group sizes. Proc. R. Soc. B 281, 20133305. (doi:10.
1098/rspb.2013.3305)
24. Kao AB, Couzin ID. 2019 Modular structure
within groups causes information loss but
can improve decision accuracy. Phil. Trans. R.
Soc. B 374, 20180378. (doi:10.1098/rstb.2018.
0378)
25. Botham MS, Hayward RK, Morrell LJ, Croft DP, Ward
JR, Ramnarine I, Krause J. 2008 Risk-sensitive
antipredator behavior in the Trinidadian guppy,
Poecilia reticulata.Ecology 89, 31743185. (doi:10.
1890/07-0490.1)
26. Svendsen JC, Banet AI, Christensen RH, Steffensen
JF, Aarestrup K. 2013 Effects of intraspecific
variation in reproductive traits, pectoral fin use and
burst swimming on metabolic rates and swimming
performance in the Trinidadian guppy (Poecilia
reticulata). J. Exp. Biol. 216, 35643574. (doi:10.
1242/jeb.083089)
27. Herbert-Read J, Wade A, Ramnarine I, Ioannou C.
2019 Data from: Collective decision-making appears
more egalitarian in populations where group fission
costs are higher, v3. Dryad Digital Repository.
(doi:10.5061/dryad.nvx0k6dn6)
royalsocietypublishing.org/journal/rsbl Biol. Lett. 15: 20190556
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... These interindividual interactions, the variability with which individuals respond to others and an individual's assessment of environmental cues are dependent on internal motivational states and environmental selection pressures (Conradt, Krause, Couzin, & Roper, 2009;Hansen et al., 2020;Herbert-Read et al., 2017;Kelley, Morrell, Inskip, Krause, & Croft, 2011;Wilson et al., 2019). However, the empirical investigation into how collective decision making has been shaped by natural selection in response to environmental pressures, such as predation level, has only recently begun (Cl ement et al., 2017;Herbert-Read, Wade, Ramnarine, & Ioannou, 2019;Ioannou, Ramnarine, & Torney, 2017). ...
... More recently, this system has been used to explore the effect of predation risk on aspects of collective decision making. Herbert-Read et al. (2019) showed that guppies from highpredation environments switched positions more than fish from low-predation environments when making group directional decisions and, similar to Bode et al., 2010, utilized a combined empirical and modelling approach to show that this positional behaviour could be explained by an increase in individual update frequency. In terms of decision-making performance, however, the observed differences in behaviour did not affect decision-making speed and the study did not assess decision accuracy (Herbert-Read et al., 2019). ...
... Herbert-Read et al. (2019) showed that guppies from highpredation environments switched positions more than fish from low-predation environments when making group directional decisions and, similar to Bode et al., 2010, utilized a combined empirical and modelling approach to show that this positional behaviour could be explained by an increase in individual update frequency. In terms of decision-making performance, however, the observed differences in behaviour did not affect decision-making speed and the study did not assess decision accuracy (Herbert-Read et al., 2019). In a different study, guppies from high-predation populations, tested in groups of four, were found to be more consistent in their movement behaviour within a single trial, resulting in differentiation into leaders and followers when making group directional decisions . ...
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Making fast and accurate group decisions under uncertain and risky conditions is a fundamental problem for groups. Currently, there is little empirical evidence of how natural selection (such as environmental predation risk) has shaped the mechanisms of group decision making. We repeatedly tested individually marked guppies, Poecilia reticulata, from the upper and lower reaches of the Aripo and Turure rivers in a Y-maze and found that populations that had evolved under different predation regimes differed in their decision-making speed. All groups decreased decision time over successive trial rounds, but fish from low-predation environments did so at a greater rate than fish from high-predation environments. This effect was only significant when fish were tested in groups of eight, not when tested individually. Decision-making accuracy was not significantly different between high- and low-predation populations. Group behaviour differed according to predation risk and trial round, most notably with low-predation groups reducing the amount of positional switching over successive trial rounds at a greater rate than high-predation groups. While fish from both predator risk environments had repeatable within-shoal positioning behaviour as they swam down the maze, only fish from the high-predation groups had repeatable finishing positions. Meaningful measures of information transfer (mean pairwise transfer entropy) were only recorded in low-predation groups, and here there was a significant effect of source river on information flow within groups. Aripo groups increased information flow over successive trial rounds, while Turure groups did not. Variation in mean pairwise transfer entropy increased over successive trial rounds for both low-predation populations, suggesting that information used to make movement decisions became less homogeneously distributed and increasingly directed through a subset of individuals. Predation pressure is a ubiquitous selection force, and these findings may apply to a variety of natural social groups.
... For example, in threespine sticklebacks, natural polymorphisms in the ectodysplasin a (eda) locus contribute to the differences in inter-fish alignment observed between benthic and marine populations [10][11][12][13]. In Trinidadian guppies, individuals descended from low-predation environments display diminished social cohesions [8,9,[14][15][16][17][18], though exposure to alarm pheromones leads to the formation of tighter schoolss [15]. Sensory cues also influence social cohesion, such as in sticklebacks, in which modulation of visibility (light vs dark) and acoustic noise leads to differences in group dynamics [19]. ...
... Modern advances in computer vision and modeling of collective behavior provide an unprecedented opportunity to resolve the role of eye loss on schooling behavior. Motion tracking and kinematic analysis have been used to probe schooling interactions in several fish species [14,16,[38][39][40][41][42]. Pair correlation functions (probability distributions involving the position and orientation of one fish relative to another) are particularly useful to disentangle positional and orientational interactions and build mechanistic models of collective motion that can simulate the trajectories of a group of virtual fish [38][39][40][41]. ...
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Fish display a remarkable diversity of social behaviors, both within and between species. While social behaviors are likely critical for survival, surprisingly little is known about how they evolve in response to changing environmental pressures. With its highly social surface form and multiple populations of a largely asocial, blind, cave-dwelling form, the Mexican tetra, Astyanax mexicanus , provides a powerful model to study the evolution of social behavior. Here we use motion tracking and analysis of swimming kinematics to quantify social swimming in four Astyanax mexicanus populations. In the light, surface fish school, maintaining both close proximity and alignment with each other. In the dark, surface fish no longer form coherent schools, however, they still show evidence of an attempt to align and maintain proximity when they find themselves near another fish. In contrast, cavefish from three independently-evolved populations (Pachón, Molino, Tinaja) show little preference for proximity or alignment, instead exhibiting behaviors that suggest active avoidance of each other. Two of the three cave populations we studied also slow down when more fish are present in the tank, a behavior which is not observed in surface fish in light or the dark, suggesting divergent responses to conspecifics. Using data-driven computer simulations, we show that the observed reduction in swimming speed is sufficient to alter the way fish explore their environment: it can increase time spent exploring away from the walls. Thus, the absence of schooling in cavefish is not merely a consequence of their inability to see, but may rather be a genuine behavioral adaptation that impacts the way they explore their environment.
... Each trial lasted approximately 25 min and group behaviour was analysed during five 2.5 min time intervals that were separated by the presentation of a food item (see Material and methods, and [7] for analyses of responses to the food item presentations). We used high-resolution video tracking to examine changes over time in six traits of collective motion that are known to be functionally important: polarization, which measures the alignment of individuals between 0 (no alignment) and 1 (complete alignment, where higher levels of polarization can improve social information transfer and reduce the risk of predation due to confusion effects: [40,41]), the speed of the group centroid (where group speed can affect responses to predators and encounter rates with food: [14]), convex hull area as a measure of spacing between individuals (where less cohesive groups are at greater risk of predation: [42]), the rate of transitions in state between polarized (aligned) and unpolarized (swarm-like) states [43,44], the maximum cross-correlation in speed (which is a measure of information transfer: [45]), and the rate of switches in leadership over time (where individuals at the front of the group have greater access to foraging rewards at a cost of greater risk of predation, and increased switching is observed in shoals from high-predation habitats: [10,[46][47][48]). Using a reaction norm approach combined with model selection procedures [35,49], we then determined whether the groups differed from one another in the dynamics of their collective behaviour over shorter (within trials) and longer (between days) timescales. ...
... Studies of animal collective motion typically only provide a snapshot of group behaviour. Demonstrating that groups show variation in their plasticity over time has significant implications for the study of collective behaviour as this magnifies variation between groups, making the detection of differences between treatments [61], populations (for example along with an environmental gradient; [47]) or species [68] more difficult. A greater number of independent experimental groups may be required than originally thought, and reliance on a few replicate groups may be inadequate. ...
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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.
... In multiple river catchments in the Northern Range mountains of Trinidad, colonisation by predatory fish in upstream stretches is limited by rapids and waterfalls, generating distinct high (downstream) and low (upstream) predation habitats for the guppies that live throughout the rivers (Deacon et al., 2018). A number of studies have shown guppies from high predation habitats show a greater social tendency and form larger groups (Seghers, 1974;Magurran et al., 1992;Huizinga et al., 2009), and more recently, guppies from high and low predation populations have been shown to differ in other collective behaviours such as their collective motion (Herbert-Read et al., 2017) and how they make decisions collectively Herbert-Read et al., 2019). Previous studies have shown improved accuracy by pairs of guppies versus single individuals under standardised conditions (Bisazza et al., 2014), and by naturally occurring groups versus single individuals in situ (Clément et al., 2017). ...
... While some mechanisms that cause individuals to be safer from predators in groups do not rely on group-level decision making or information transfer, such as the dilution and confusion effects (Foster & Treherne, 1981;Duffield & Ioannou, 2017), improved decision making by groups can act to further reduce the risk of predation (Magurran et al., 1985;Godin et al., 1988;Ward et al., 2011). Little attention has been given to how ecological factors affect group decision making or collective behaviour more generally (Chamberlain & Ioannou, 2019;Tidau & Briffa, 2019;Ginnaw et al., 2020), and only a handful of studies have examined how collective decision making changes with predation risk Herbert-Read et al., 2019). Despite the differences between this study and that of Clément et al. (2017), the general trend found here, that group size was more important in decision speed in fish from low predation habitats, supports their findings. ...
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While larger groups tend to be better at making decisions, very few studies have explored how ecological variables, including predation pressure, shape how group size affects decision making. Our cross-population study of wild-caught guppies ( Poecilia reticulata ) shows that leading individuals from larger groups made faster decisions when deciding to leave the start area and reach the junction of a Y-maze, which allows for compromise over timing. However, at the junction of the Y when the fish needed to make a mutually exclusive decision that does not allow for compromise, there was no effect of group size in high predation fish on decision speed. In fish from low predation habitats, speed was fastest at the intermediate group size with a decline in speed in the largest group size. These results challenge the view that decision making always improves with group size and shows this effect depends on ecological and decision-making conditions.
... 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.
... Individuals in groups with a high degree of fission-fusion dynamics are expected to be good at solving problems that require conditional discrimination (Aureli and Schino, 2019). For instance, when comparing guppies from low and high predation environments, groups of fish from high predation environments switched their positions more often and made movement decisions within the group more frequently, most likely because the costs of group fission are higher in such environments (Herbert-Read et al., 2019). Whether decision-making processes under particular environmental conditions differ between polarization and control females remains to be tested. ...
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The evolution of collective behaviour has been proposed to have important effects on individual cognitive abilities. Yet, in what way they are related remains enigmatic. In this context, the ‘distributed cognition’ hypothesis suggests that reliance on other group members relaxes selection for individual cognitive abilities. Here, we test how cognitive processes respond to evolutionary changes in collective motion using replicate lines of guppies ( Poecilia reticulata ) artificially selected for the degree of schooling behaviour (group polarization) with >15% difference in schooling propensity. We assessed associative learning in females of these selection lines in a series of cognitive assays: colour associative learning, reversal-learning, social associative learning, and individual and collective spatial associative learning. We found that control females were faster than polarization selected females at fulfilling a learning criterion only in the colour associative learning assay, but they were also less likely to reach a learning criterion in the individual spatial associative learning assay. Hence, although testing several cognitive domains, we found weak support for the distributed cognition hypothesis. We propose that any cognitive implications of selection for collective behaviour lie outside of the cognitive abilities included in food-motivated associative learning for visual and spatial cues.
... For zebrafish, Danio rerio, tested alone, this has recently been shown to lose information and require larger sample sizes than using trajectory data from all three dimensions (Macrì et al., 2017). In studying collective movement of freely moving animals, 3D tracking of the motion of individuals is considerably more difficult (Puckett, Kelley, & Ouellette, 2014), and laboratory studies of fish collective motion typically use shallow water to minimize possible movement in the depth plane and only use 2D tracking (Berdahl et al., 2013;Herbert-Read et al., 2019;Herbert-Read, Kremer, Bruintjes, Radford, & Ioannou, 2017;Perez-Escudero, Vicente-Page, Hinz, Arganda, & de Polavieja, 2014). In a rare example that 3D trajectories for individuals in shoals were obtained, it was found that identifying leaders could be done reliably using only 2D data (Watts, Nagy, Holbrook, Biro, & Burt de Perera, 2017). ...
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Collective movement is critical to the survival of some animals. Despite substantial progress in understanding animal collectives such as fish shoals and bird flocks, it is unknown how collective behaviour is affected by changes in multiple environmental conditions that can interact as stressors. Using a fully factorial repeated-measures design, we tested the independent and combined effects of darkness and acoustic noise on the collective motion of three-spined sticklebacks, Gasterosteus aculeatus, quantified using high-resolution tracking data from video. Corresponding to the importance of vision in shoaling behaviour, darkness increased nearest-neighbour distances and reduced coordination, measured as speed correlations and differences in directional heading between nearest neighbours. Although individual swimming speeds were not impacted by darkness, the group's centre of mass was slower, an emergent effect of reduced polarisation (i.e. greater group disorder) in darkness. While additional acoustic noise had no detectable effect on these variables, it altered group structure, with fish being more likely to be found side by side one another. Fish were also further from the arena wall (i.e. showed reduced wall following) when there was additional acoustic noise. There was only weak evidence for additive or interactive effects of the two stressors. Across the different environmental contexts, there were consistent, repeatable differences between groups (i.e. group personality variation) in the speed, turning angle and distance from the arena wall of individuals, but the only collective behaviour that was repeatable was group polarization. Our study demonstrates that multiple stressors can have independent effects that impact different aspects of behaviour and highlights the need for empirical studies on multiple stressors as their effects can be unpredictable.
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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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A long-standing assumption in social behavior is that leadership incurs costs as well as benefits, and this tradeoff can result in diversified social roles in groups. The major cost of leadership in moving animal groups is assumed to be predation, with individuals leading from the front of groups being targeted more often by predators. Nevertheless, empirical evidence for this is limited, and experimental tests are entirely lacking. To avoid confounding effects associated with observational studies, we presented a simulation of virtual prey to real fish predators to directly assess the predation cost of leadership. Prey leading others are at greater risk than those in the middle of groups, confirming that any benefits of leading may be offset by predation costs. Importantly, however, followers confer a net safety benefit to leaders, as prey leading others were less likely to be attacked compared with solitary prey. We also find that the predators preferentially attacked when solitary individuals were more frequent, but this effect was relatively weak compared with the preference for attacking solitary prey during an attack. Using virtual prey, where the appearance and behavior of the prey can be manipulated and controlled exactly, we reveal a hierarchy of risk from solitary to leading to following social strategies. Our results suggest that goal-orientated individuals (i.e., potential leaders) are under selective pressure to maintain group cohesion, favoring effective leadership rather than group fragmentation. Our results have significant implications for understanding the evolution and maintenance of different social roles in groups.
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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.
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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.