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The emergence of leaders and followers is a key factor in facilitating group cohesion in animals. Individual group members have been shown to respond strongly to each other’s behavior and thereby affect the emergence and maintenance of these social roles. However, it is not known to what extent previous social experience might still affect individual’s leading and following tendencies in later social interactions. Here, by pairing three-spined sticklebacks (Gasterosteus aculeatus) with 2 different consecutive partners, we show a carryover effect of a previous partner’s personality on the behavior of focal individuals when paired with a new partner. This carryover effect depended on the relative boldness of the focal individual. Relatively bold but not shy fish spent less time out of cover and led their current partner less if they had previously been paired with a bolder partner. By contrast, following behavior was mainly influenced by the personality of the current partner. Overall, the behavior of relatively bold fish was more consistent across the stages, whereas shy fish changed their behavior more strongly depending on the current context. These findings emphasize how the history of previous social interactions can play a role in the emergence and maintenance of social roles within groups, providing an additional route for individual differences to affect collective behavior.
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International Society for Behavioral Ecology
Original Article
The role of previous social experience on
risk-taking and leadership in three-spined
Jolle W.Jolles,a Adeline Fleetwood-Wilson,a ShinnosukeNakayama,a,b Martin C.Stumpe,c
Rufus A.Johnstone,a and AndreaManicaa
aDepartment of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK,
bDepartment of Biology and Ecology of Fishes, Leibniz Institute of Freshwater Ecology and Inland
Fisheries, Müggelseedamm 310, Berlin 12587, Germany, and cAnTracks Computer Vision Systems,
Mountain View, CA, USA
Received 24 January 2014; revised 2 July 2014; accepted 18 July 2014.
The emergence of leaders and followers is a key factor in facilitating group cohesion in animals. Individual group members have
been shown to respond strongly to each other’s behavior and thereby affect the emergence and maintenance of these social roles.
However, it is not known to what extent previous social experience might still affect individual’s leading and following tendencies in
later social interactions. Here, by pairing three-spined sticklebacks (Gasterosteus aculeatus) with 2 different consecutive partners, we
show a carryover effect of a previous partner’s personality on the behavior of focal individuals when paired with a new partner. This
carryover effect depended on the relative boldness of the focal individual. Relatively bold but not shy fish spent less time out of cover
and led their current partner less if they had previously been paired with a bolder partner. By contrast, following behavior was mainly
influenced by the personality of the current partner. Overall, the behavior of relatively bold fish was more consistent across the stages,
whereas shy fish changed their behavior more strongly depending on the current context. These findings emphasize how the history
of previous social interactions can play a role in the emergence and maintenance of social roles within groups, providing an additional
route for individual differences to affect collective behavior.
Key words: boldness, collective decision-making, leadership, personality, responsiveness, shoaling.
The emergence of leaders and followers plays a major role in pro-
moting group coordination and cohesion, with important conse-
quences for the social lives of humans as well as many nonhuman
animals (Krause and Ruxton 2002; Conradt and Roper 2009; Dyer
etal. 2009; King etal. 2009). There is a growing body of evidence
that individuals dier in their social roles, with some individuals
having a strong influence on group behavior while others mostly
follow (e.g., Reebs 2000; Harcourt etal. 2009; Nagy et al. 2010;
Flack etal. 2012; Nakayama etal. 2013). A key focus has been to
determine what factors predict which group members will become
leaders (Conradt and Roper 2003; Couzin et al. 2005; King etal.
2009). Many such factors have been identified in a large range of
species: body size (Krause et al. 1998; Reebs 2001), hunger level
(Krause et al. 1998; McClure etal. 2011; Nakayama, Johnstone,
et al. 2012), dominance (Peterson and Jacobs 2002; King et al.
2008; Jolles etal. 2013), social aliations (King et al. 2008; Jacobs
etal. 2011), sex (Peterson and Jacobs 2002; Barelli etal. 2008), age
(Réale and Festa-Bianchet 2003; Sueur and Petit 2008), boldness
(Beauchamp 2000; Ward etal. 2004; Harcourt etal. 2009; Kurvers
etal. 2009), sociability (Brown and Irving 2014), and knowledge or
experience (Reebs 2000; Couzin etal. 2005; Dyer etal. 2009; Flack
etal. 2012).
In recent years a few studies have started to go beyond the search
for such predictive factors and have shown that the actual dynam-
ics of interactions among individuals play an important role in
leading and following behavior (Harcourt etal. 2009; Nakayama,
Harcourt, et al. 2012; Nakayama et al. 2013; Pettit et al. 2013;
Ward et al. 2013). For example, although bold individuals typi-
cally lead and shy individuals mainly follow (Beauchamp 2000;
Harcourt etal. 2009; Kurvers etal. 2009; Nakayama et al. 2013),
these dierences in leading and following are strongly enhanced by
social feedback (Harcourt etal. 2009; Nakayama, Harcourt, etal.
Address correspondence to J.W. Jolles. E-mail:
Behavioral Ecology (2014), 00(00), 1–7. doi:10.1093/beheco/aru146
Behavioral Ecology Advance Access published August 21, 2014
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Behavioral Ecology
2012). Furthermore, although bolder individuals are generally less
responsive to their partner’s behavior, both bolder and shyer indi-
viduals readily adjust to their partner when in the following role
(Nakayama, Harcourt, et al. 2012; Nakayama, Johnstone et al.
2012). These findings not only highlight the important modifying
role of social feedback, they also suggest the exciting possibility that
interactions with previous partners may play a role in later leading
and following behavior. As also highlighted in the human leadership
literature (Amit etal. 2009; Emery 2010; DuBrin 2013), addressing
this key outstanding issue may contribute to our understanding of
the emergence and maintenance of leadership and ultimately of
collective behavior and group decision making.
Most gregarious animals live in highly dynamic groups in which
they interact with multiple conspecifics (Krause and Ruxton 2002),
and a strong influence of previous social experience has already
been shown for neophobic and aggressive behavior (Hsu and Wolf
1999; Frost et al. 2007). In a previous study on leadership, fish
were shown to change their behavior based on a partner’s ability
to successfully locate food during joint trips, with experience over-
riding personality dierences in the tendency to follow but not to
lead (Nakayama etal. 2013). Here by pairing three-spined stickle-
backs (Gasterosteus aculeatus) with 2 dierent consecutive partners, we
investigated how previous social experience with other individuals
aected the propensity of fish to leave cover, to lead, and to follow
their current partner during joint trips. If individuals fine-tune their
behavior based on previous experiences, this potentially represents
a mechanism through which social roles can be reinforced. Since
bold individuals are known to be less responsive than shy individu-
als during social interactions (Pike etal. 2008; Nakayama, Harcourt,
et al. 2012; Nakayama, Johnstone, et al. 2012), we hypothesized
that bolder fish would be more consistent in their behavior across
dierent social and nonsocial environments and shyer fish to be
more responsive to the present context. We therefore predicted that
the behavior of bolder fish would be mainly explained by their own
personality and to a lesser extent by that of their current and pre-
vious partners, whereas for shyer fish the personality of their cur-
rent partner would be the main determinant of their behavior. This
approach provides a unique opportunity to describe important new
aspects of social feedback and personality that have thus far been
neglected in studies on group movements and leadership.
Subjects and housing
We collected three-spined sticklebacks using a sweep net during
the summers of 2010–2012, from a small branch of the river Cam
(Cambridge, UK). Large groups of fish (~200 individuals) were
housed in a temperature-controlled laboratory (T=14 ± 1°C) with
a constant light regime (lights on from 09:00 to 19:00 h) and kept in
large glass holding aquaria (120 × 60 × 60 cm) that contained artifi-
cial plants, aeration, and undergravel filtration. Fish were fed frozen
bloodworm (Chironomidae) larvae ad libitum once a day before the
start of the experiment. During the experimental period, feeding
was rationed to one bloodworm a day to standardize hunger levels.
All fish used for the experiment were of similar length (50 ± 7 mm
from tip of snout to caudal peduncle) and were taken from a single
population to minimize population-specific genetic eects that may
influence personality (Bell 2005). Although the exact age of the fish
could not be determined, all caught individuals were juveniles and
are expected to only vary in age by a few weeks. Sex of the fish was
not identified as the temperature and photoperiod regime in the
lab prevented the fish from becoming sexually mature (Borg etal.
During the experimental period, we housed fish individually in cus-
tom-holding tanks (60 × 30 × 40 cm) lined with gravel and divided
lengthwise into 6 compartments by transparent perspex partitions.
Five compartments were used to house a fish each and contained
an artificial plant at one end and a white perspex plate (2 × 2 cm) at
the other end where food was delivered. The remaining compart-
ment contained the undergravel filter and was not used to house
any fish. Partner fish were never housed in adjacent compartments.
Fish were allowed to acclimatize in their individual compartments
for 3days before the start of testing.
To investigate fish’s propensity to explore a risky area and lead
and follow conspecifics, we used a tank setup previously used in
our lab for similar experiments (Harcourt etal. 2009; Nakayama,
Harcourt, et al. 2012; Nakayama, Johnstone, et al. 2012). In
short, experiments took place in 4 identical experimental tanks
(70 × 30 × 30 cm), each divided lengthwise with either an opaque
white perspex partition or a transparent perspex partition to create
2 long lanes (see Supplementary Figure S1). Each lane was lined
with gravel in a slope ranging from a deep (15 × 15 cm; 14 cm depth)
“safe area” that contained an artificial plant to an increasingly shal-
low “exposed” area (4-cm depth at the other side). Only when fish
had fully emerged from this safe area we defined them to be “out
of cover.” No food was provided during the trials and fish were
thus not rewarded for leaving cover. This setup reflects the ecologi-
cally relevant problem where fish can either rest in a safe place or
explore a risky area in search of food (analogous to the exposed
area where food is delivered in their holding compartments). Fish
prefer to spend time under cover but, even in the absence of food
in the experimental tank, keep making regular trips out of cover to
explore the exposed area. Since fish have dierent preferences for
the number and length of trips out of cover they make yet prefer
to synchronize their activities and shoal together, there is a con-
flict on the timing of leaving and returning to cover. We have used
this ecologically relevant setup to look at the emergence of leaders
and followers in a number of previous papers (e.g., Harcourt etal.
2009, 2010). The walls of the tank were covered by white perspex
to minimize any disturbances from outside the tank. When not run-
ning experiments, the water of the experimental tanks was oxygen-
ated with an air stone. HD video cameras (Camileo X100; Toshiba
Corporation) were used to record fish movements from a fixed posi-
tion above each tank.
Experimental procedure
We tested 4 batches of fish (N = 136 in total), each over a 7-day
cycle (November to December 2011 and November to -December
2012)and randomly selected 44 fish as focals, 44 as partner for the
“first pairing,” and 44 as partner for the “second pairing,”. Fish
were tested across 3 stages. We started by testing fish in the experi-
mental tank in isolation to quantify their boldness (“isolation stage”).
On day 1 and 2, each fish was put in 1 of 2 lanes of the experi-
mental tank that were separated by an opaque partition so that fish
could not interact with each other. The behavior of each fish was
recorded for an hour each day. After a rest day, we randomly paired
each focal fish with a partner (“previous pairing stage”), and put the
2 fish in the same experimental tank, but this time with a transpar-
ent partition so that they could interact. Behavior was recorded for
an hour on each of 2 consecutive days. Finally, we paired each focal
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Jolles etal. • Previous social experience aects leadership behavior
with a new socially naive partner and observed their behavior for
another two 1-h sessions over 2 consecutive days (“current pairing
stage”). On each testing day, fish were transferred to the deep end of
the tank using a dip net and allowed to acclimatize to the tanks for
7 min before we tracked their movements. After each trial, fish were
moved back to their housing compartment. For each experimental
cycle, we randomized the daily testing order as well as the assign-
ment to tank and to the left and right lanes of a tank. Fish were
housed in their individual compartments for a week before their first
pairing to minimize any social experiences from being housed with
conspecifics in social housing tanks.
Data analysis
We tracked the exact movements of the fish at 10 frames/s using
automated motion tracking software (AnTracks, version 0.99). For
tracking we used a background subtraction acquisition method
that determined what pixels diered between the video and a
background image that was created from a random 5-min period
in each 1-h recording. As processing parameters we used gauss
subtraction, gauss blur, dilate and final thresholding for which we
adjusted the levels according to the specific light levels in each video
to ensure fish movements were tracked correctly. After tracking was
complete we checked all trajectories for each video. Any possible
noise tracked by the software was eliminated and discontinuous
trips where the software had lost track of the fish for a few frames
were joined.
Data were analyzed in R 3.0.2 (R Development Core Team,
2013). Based on the positional coordinates of both members in a
pair we calculated the relative time fish spent out of cover and their
number of trips out of cover. On average, fish spent 12.89% of
the time out of over (range 0–62.3%) and were consistent in this
proportion of time out of cover across the 2days of the isolation
stage (rs=0.55, N=136, P<0.001). Therefore, we used the aver-
age proportion of time individuals were out of cover across both
days as the boldness score for each fish, an approach commonly
adopted for examining the boldness personality trait (e.g., Harcourt
et al. 2009; Magnhagen and Bunnefeld 2009; King et al. 2013).
Ten fish that did not come out of cover during the isolation stage
were excluded.
The behavior of pairs of fish in a similar setup but without
previous experience has been described in detailed in previous
work (Harcourt et al. 2009; Nakayama, Harcourt, et al. 2012;
Nakayama, Johnstone, et al. 2012; Nakayama etal. 2013). In this
paper, we focus on the eect of previous experience (the first pair-
ing) on later interactions (the second paring). We focused on the
proportion of time spent out of cover by the focal fish, and on the
number of trips it made out of cover on its own, as a leader, and
as a follower. Leading was defined as a fish going out of cover and
being joined by its partner; following as a fish going out of cover
to join its partner that is already out. We considered the eects on
leading and following behavior separately as previous work has
shown that dierent factors (e.g., success of a partner in finding
food) may aect the tendencies to lead and follow in dierent ways
(e.g., Nakayama etal. 2013). For each of the 4 variables (time out
of cover, and the 3 types of trips), we used linear models with the
focal fish own boldness, the boldness of the previous partner, and
that of the current partner as predictors. We started with full mod-
els with all the predictors and obtained a minimal model by back-
ward stepwise elimination (i.e., sequentially dropping terms until
all terms retained in the model were significant). Statistics for non-
significant terms were obtained by fitting the minimal model with
each nonsignificant term added individually. As previous work has
shown that the relative personality between partners is a key predic-
tor of collective movements and leadership (Harcourt etal. 2009;
Nakayama et al. 2013), we ran separate models for focals bolder
than their second partner (bold focals) and focals relatively shyer
than their second partner (shy focals). Results based on the absolute
boldness scores were qualitatively similar and are documented in
the Supplementary Material. As our dataset consists of batches in
2 subsequent years, we additionally ran all models with year as an
extra fixed factor and found it had no significant eect in any of
the models. The residuals for all models were visually inspected to
ensure homogeneity of variance, normality of error, and linearity.
Finally, paired t-tests were used to investigate how the risk-taking
behavior of bold and shy focals changed across the isolation and
2 pairing stages. Repeatability across the 6 days of the experiment
was estimated using the intra-class correlation coecient (ICC),
following the method by Lessells and Boag (1987). All results with
0.10> P > 0.05 are reported as trends and P ≤ 0.05 as significant.
Means are quoted ± standard error (SE) throughout.
We focus on the data collected during the second pairing and inves-
tigate how the personalities of the previous and current partner
aect the behavior of focal fish bolder than their current partner
(bold focals) and focal fish shyer than their current partner (shy
focals). The relative boldness of focal fish ranged from −0.62 for
shy focals to +0.50 for bold focals (mean ± SE=−0.09 ± 0.03).
Time spent out ofcover
Bold focals spent more time out of cover the bolder they were
themselves (Figure 1A) but also the shyer their previous partner
had been (F2,7 = 18.77, P = 0.002; Table 1), together explaining
more than 80% of the variance (R2 = 0.84). The personality of
their current partner had no eect on the time bold focals were
out of cover (F1,7= 0.04, P= 0.84). By contrast, shy focals tended
to spend more time out of cover the bolder their current partner
(F1,22 = 4.11, P = 0.055; R2 = 0.16), while their own personality
(F1,22=0.33, P=0.571; Figure1B) and that of their previous part-
ner (F1,22=0.04, P=0.845) had no significant eect.
Number oftrips
The number of solo trips, when focal fish went out and returned
to cover without being followed by their partner, was relatively
higher in bold compared with shy focals (t = 2.56, P = 0.028;
13.8 ± 4.24 and 2.65 ± 1.02 trips, respectively). Bold focals went
on more solo trips the bolder they were themselves (F1,8= 6.60,
P= 0.033; R2= 0.45) while the personality of the current partner
and the previous partner had no eect on this behavior (F1,7=0.09,
P=0.777; F1,7=1.67, P=0.237 respectively; Table 1). The num-
ber of solo trips made by shy focals was not explained by either
their own personality (F1,22=0.17, P=0.687), that of their current
partner (F1,22=0.25, P=0.624) or that of their previous partner
(F1,22=0.11, P=0.743).
There was no significant dierence in the number of joint trips
led by bold and shy focal fish during the second pairing (t= 1.31,
P=0.211; 7.15 ± 2.14 and 3.96 ± 1.19 trips, respectively). Bold focals
led more trips the relatively bolder the focal individual (Figure 2A)
but also the shyer their previous partner (F2,7 = 12.98, P = 0.004;
Figure2B; Table1), together explaining 79% of the variance. The per-
sonality of the current partner did not aect the number of leadership
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Behavioral Ecology
trips for bold focals (F1,6=1.53, P=0.262). By contrast, shy focals led
more trips the bolder their current partner (F1,22= 5.75, P = 0.025;
R2= 0.21), while their own personality (F2,21 = 0.28, P = 0.600) and
that of their previous partner (F2,21=0.13, P=0.719) had no eect.
There was no dierence in the number of trips bold and
shy focals followed their current partner out of cover (t = 1.91,
P = 0.083; 7.15 ± 2.14 and 2.91 ± 2.45 trips, respectively). Bold
focals followed their partner more the bolder it was (Figure3) and
the shyer their previous partner had been (F2,7=41.74, P <0.001;
Table1), together explaining 92% of the variance. Bold focal’s own
personality did not play a role (F1,6= 2.28, P = 0.182). Shy focals
followed more the bolder their current partner was (F1,21= 7.78,
P = 0.011; Figure 3; R2 = 0.26), with no eect of their own per-
sonality (F1,21=0.60, P=0.448) and that of their previous partner
(F1,21=0.39, P=0.537).
Behavioral consistency across thestages
Bold focals were highly repeatable in the time they spent out of cover
on the 6days across the 3 stages (ICC=0.76, 95% confidence inter-
val [CI]: 0.55–0.92), whereas shy focals were not (ICC=0.17, 95%
CI: 0.05–0.35). On average, bold focals spent similar amounts of time
out of cover during the isolation stage and the first pairing (t9=1.81,
P=0.104) but tended to spend less time out of cover during the sec-
ond pairing compared with the isolation stage (t9=2.18, P=0.058).
By contrast, shy focals spent more time out of cover when they
could see their partner compared with when in isolation (first pair-
ing: t31=−2.29, P=0.029; second pairing: t31=−2.62, P= 0.013).
Additionally, looking at focals based on their absolute boldness cat-
egory (with bold fish spending more time out and shy fish less time
out than the average focal fish) we found bold fish (ICC=0.65, 95 %
CI: 0.47–0.82) were more consistent than shy fish (ICC=0.17, 95 %
CI: 0.04–0.39), as reflected by their nonoverlapping CIs.
In this study, we show for the first time that the eect of the per-
sonality of a previous social partner can carry over to later social
interactions, modulating the willingness of individuals to go out of
cover and lead their partner. By contrast, the tendency to follow
was mainly aected by the personality of an individual’s current
partner. Although bolder fish were more consistent than shyer fish
in the time they spent out of cover across the contexts, it was only
bold fish that were susceptible to social reinforcement by their pre-
vious social interactions. Shyer fish behaved much more flexibly
and responded most strongly to their current partner.
Previously, some studies have shown that previous social experi-
ence may aect neophobia and aggression (Hsu and Wolf 1999;
Frost etal. 2007) and that experience within the same pair may
override personality dierences in leadership tendencies (Nakayama
etal. 2013). Here we show for the first time how social experiences
with previous partners may aect later leadership behavior: the
bolder their previous partner, the relatively less time bold focals
spent out of cover, making them less successful in taking the lead.
These findings help answer the important question in the leader-
ship literature of what makes an initiator successful in triggering
collective movement (Petit and Bon 2010). Although bolder indi-
viduals are less sensitive to failure in recruiting a partner, they are
responsive to their partner’s behavior when it has taken on the
role of leader. This may be especially the case when bold focals
are paired with a relatively bold partner. In such a situation, bold
focals partner is relatively more likely to take the lead compared
with a shyer partner. Consequently, the focal individual may be less
likely to be followed, resulting in a reduction of positive feedback in
leadership and reduced performance in the pair (Nakayama etal.
2013). Such experience may then subsequently modulate focal fish’
willingness to go out of cover and lead their partner. Not only does
this finding highlight that bolder individuals may be more suscepti-
ble to social reinforcement than shy individuals, it indicates that for
leadership social experience is important. To be an eective leader,
an individual may need experience with good followers, provid-
ing positive social feedback and leading experience, and ultimately
more successful leadership. These findings may have potential for
our understanding of human leadership as a lack of knowledge of
the social dynamics underlying leadership has been highlighted in
the social sciences (Amit et al. 2009; Emery 2010; DuBrin 2013).
0.2 0.3 0.4 0.5 0.6 0.7 0.8
Boldness score bold focals
Proportion of time out of cover
0.10.2 0.30.4 0.5
Boldness score shy focals
Proportion of time out of cover
The proportion of time focal fish spent out of cover during the current pairing was (A) positively correlated with the boldness scores of bold focals (N=10),
but (B) not significantly correlated with the boldness scores of shy focals (N=24). Boldness scores were square root transformed.
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Jolles etal. • Previous social experience aects leadership behavior
Future studies could look in more detail at the extent of the dier-
ence in personality scores between the partners and determine the
eect it may have on collective behavior.
The finding that bold but not shy focals were aected by a previ-
ous partner might be explained by the fact that shyer individuals
are in general more sociable (Ward et al. 2004; Pike etal. 2008)
and behaviorally less consistent (Nakayama, Johnstone, etal. 2012),
than bold individuals. Indeed, we found that the current partner’s
personality explains much more of shy focals’ behavior than that
of bold focals, which is in line with previous studies reporting that
shy individuals are more responsive to the actions of their (current)
group members (Pike etal. 2008; Nakayama, Harcourt, etal. 2012;
Nakayama, Johnstone, etal. 2012). This may also explain the more
general finding that shy but not bold focals spent considerably more
0.2 0.3 0.4 0.5 0.6 0.7
Boldness score bold focal
Nr of trips leading
0.00.1 0.20.3 0.40.5
Boldness score previous partner
The number of trips bold focals (N=10) initiated and were joined by their partner during the current pairing was (A) positively related to their own boldness
score and (B) negatively related to the boldness score of their previous partner. The y axis of plot B shows residuals of the model on leading trips with focal
boldness score as the only factor. Scores above 0 indicate individuals were joined more than may be expected based on their own boldness score and scores
below 0 individuals were joined less than may be expected based on their boldness score. Boldness scores and number of leading trips were square root
Linear models of proportion of time out, number of solo trips, number of led trips, and number of trips followed by bold and shy
focal fish
Bold focals Shy focals
Estimate SE F P Estimate SE F P
Proportion of time out
Constant 0.10 0.10 0.391 0.05 0.10 0.662
Personality focal 0.80 0.16 23.80 0.002 0.03 0.37 0.01 0.939
Personality current partner 0.07 0.32 0.04 0.844 0.45 0.22 4.11 0.055
Personality previous partner −0.46 0.19 6.01 0.044 −0.03 0.15 0.04 0.847
Number of solo trips
Constant −0.05 1.33 0.974 1.16 0.24 <0.001
Personality focal 6.61 2.57 6.60 0.033 −1.01 2.47 0.17 0.687
Personality current partner −1.48 5.04 0.08 0.777 0.78 1.57 0.25 0.624
Personality previous partner −3.72 2.88 1.67 0.237 0.35 1.05 0.11 0.743
Number of led trips
Constant 1.18 0.78 0.174 −0.09 0.72 0.899
Personality focal 4.28 1.23 12.13 0.010 −1.37 2.56 0.28 0.600
Personality current partner 2.62 2.12 1.53 0.262 3.71 1.55 5.75 0.025
Personality previous partner −3.88 1.39 7.79 0.027 0.38 1.05 0.13 0.719
Number of followed trips
Constant 1.05 0.47 0.062 −0.08 0.72 0.917
Personality focal 1.63 1.08 1.51 0.182 −1.96 2.53 0.60 0.447
Personality current partner 11.73 1.41 68.84 <0.001 4.30 1.54 7.78 0.010
Personality previous partner −2.93 1.06 7.51 0.029 0.65 1.04 0.39 0.537
These analyses looked at focals that were bolder than their final partner (N=10) and focals that were shyer than their final partner (N= 24). Statistics for sig-
nificant terms, shown in bold, were derived from the minimal model containing only significant terms, whereas statistics for nonsignificant terms were obtained
by running the minimal model with the term added individually. Coecient estimates represent the change in the dependent variable relative to the baseline
category and can therefore be interpreted as measures of eect size. All personality scores and response variables were square root transformed.
Page 5 of 7
at Cambridge University Library on August 22, 2014 from
Behavioral Ecology
time out of cover when there was a conspecific present compared
with when they were in isolation. Interestingly, in contrast to the
time spent out of cover and leading behavior, following behavior of
both bold and shy focals was primarily explained by the boldness of
their current partner. This result is in line with a number of recent
studies that have shown that both bold and shy individuals are
responsive when in the following position (Nakayama, Harcourt,
etal. 2012; Nakayama, Johnstone, etal. 2012) and that experience
may override personality dierences in the tendency to follow but
not in the tendency to lead (Nakayama etal. 2013). Together, these
findings thus suggest that regardless of an individual’s own person-
ality, its tendency to follow mainly depends on the behavior of its
current partner(s). Leadership, in contrast, is particularly dependent
on a bolder personality type, with a modifying eect of social feed-
back from previous experiences.
Overall, our findings demonstrate a general dierence in respon-
siveness between shy and bold individuals. Although both bold
and shy individuals adjusted their behavior, bold individuals were
more consistent in their behavior than shy individuals but adjusted
their behavior based on their previous partner, suggestive of social
reinforcement. In contrast, shy individuals mostly adjusted their
behavior based on their current partner. These results support 2
recent theoretical models that showed how a coevolutionary process
between responsiveness and consistency may eventually result in
populations that consist of highly responsive individuals that follow
and behaviorally consistent individuals that mainly lead (Johnstone
and Manica 2011; Wolf etal. 2011). Furthermore, these findings are
highly relevant in the light of the idea that individual dierences can
be seen as behavioral specializations (Dall etal. 2012). If individuals
dier in the extent that they change their behavior based on previ-
ous and current experiences, this represents a potential mechanism
through which social roles can be generated and reinforced to create
even longer lasting dierences between individuals. In other words,
personality dierences may be maintained in populations because
of their role in social coordination (see also King etal. 2009).
While the study of collective behavior, from pairs of individuals
to groups of thousands of individuals, was initially mostly focused
on homogeneous interaction rules (Couzin and Krause 2003; Petit
and Bon 2010; Vicsek and Zafeiris 2012), individual dierences
are increasingly taken into account when examining group behav-
ior (Conradt and List 2009; Herbert-Read etal. 2012; Jolles etal.
2013). Here we go one step further by showing that social dynam-
ics across time and social contexts may have a considerable eect
on individual and thereby group behavior. Our study is the first
to demonstrate that leadership roles are aected by social experi-
ences from previous partners and that this depends on an individ-
ual’s personality, with bold but not shy fish being aected by the
personality of a previous partner. These findings help understand
how leading and following behavior emerge and are maintained
and highlight the important influence current as well as previous
social experiences can have on individual and collective behavior.
Supplementary material can be found at http://www.beheco.
This study was supported by a BBSRC scholarship to J.W.J.and a
fellowship from the Japan Society for the Promotion of Science to
We thank 2 anonymous referees for their helpful feedback, N.Boogert for
her comments on a previous version of this paper, and B. Taylor for fish
husbandry. Animal care and experimental procedures were approved by the
Animal Users Management Committee of the University of Cambridge
under a nonregulated procedures regime.
Handling editor: Alison Bell
Amit K, Popper M, Gal R, Mamane-Levy T, Lisak A. 2009. Leadership-
shaping experiences: a comparative study of leaders and non-leaders.
Leadersh Organ Dev J. 30:302–318.
Barelli C, Boesch C, Heistermann M, Reichard UH. 2008. Female white-
handed gibbons (Hylobates lar) lead group movements and have priority of
access to food resources. Behaviour. 145:965–981.
Beauchamp G. 2000. Individual dierences in activity and explora-
tion influence leadership in pairs of foraging zebra finches. Behaviour.
Bell AM. 2005. Behavioural dierences between individuals and two popu-
lations of stickleback (Gasterosteus aculeatus). J Evol Biol. 18:464–473.
Borg B, Bornestaf C, Hellqvist A. 2004. Mechanisms in the photoperiodic
control of reproduction in the Stickleback. Behaviour. 141:1521–1530.
Brown C, Irving E. 2014. Individual personality traits influence group
exploration in a feral guppy population. Behav Ecol. 25:95–101.
Conradt L, List C. 2009. Group decisions in humans and animals: a survey.
Philos Trans R Soc B. 364:719–742.
Conradt L, Roper TJ. 2003. Group decision-making in animals. Nature.
Conradt L, Roper TJ. 2009. Conflicts of interest and the evolution of deci-
sion sharing. Philos Trans R Soc B. 364:807–819.
Couzin ID, Krause J, Franks NR, Levin SA. 2005. Eective leadership and
decision-making in animal groups on the move. Nature. 433:513–516.
Couzin ID, Krause J. 2003. Self-organization and collective behavior in ver-
tebrates. Adv Study Behav. 32:1–75.
Dall SRX, Bell AM, Bolnick DI, Ratnieks FLW, Sih A. 2012. An evolution-
ary ecology of individual dierences. Ecol Lett. 15:1189–1198.
0.0 0.1 0.2 0.3 0.40.5 0.60.7 0.8
Boldness score current partner
Number of trips following
The number of trips focals went out of cover and joined their partner
(following) during the current pairing is positively related to the boldness
score of the current partner, both for bold focals (N = 10, closed circles)
and shy focals (N= 24, closed triangles). Boldness scores and the number
of following trips were square root transformed. Two data points of the
bold focals overlap at the origin because they both never followed and had a
partner with a boldness score of 0.
Page 6 of 7
at Cambridge University Library on August 22, 2014 from
Jolles etal. • Previous social experience aects leadership behavior
DuBrin AJ. 2013. Leadership: research findings, practice, and skills. Mason:
South-Western, Cengage Learning.
Dyer JRG, Johansson A, Helbing D, Couzin ID, Krause J. 2009. Leadership,
consensus decision making and collective behaviour in humans. Philos.
Trans R Soc B. 364:781–789.
Emery C. 2010. Investigating leadership emergence using longitudinal lead-
ership networks. PhD Thesis, Università della Svizzera italiana.
Flack A, Pettit B, Freeman R, Guilford T, Biro D. 2012. What are leaders
made of ? The role of individual experience in determining leader–fol-
lower relations in homing pigeons. Anim Behav. 83:703–709.
Frost AJ, Winrow-Gien A, Ashley PJ, Sneddon LU. 2007. Plasticity in ani-
mal personality traits: does prior experience alter the degree of boldness?
Proc R Soc B. 274:333–339.
Harcourt JL, Ang TZ, Sweetman G, Johnstone RA, Manica A. 2009. Social
feedback and the emergence of leaders and followers. Curr Biol. 19:248–252.
Harcourt JL, Sweetman G, Manica A, Johnstone RA. 2010. Pairs of fish
resolve conflicts over coordinated movement by taking turns. Curr Biol.
Herbert-Read JE, Krause S, Morrell LJ, Schaerf TM, Krause J, Ward AJW.
2012. The role of individuality in collective group movement. Proc R Soc
B. 280:20122564.
Hsu Y, Wolf L. 1999. The winner and loser eect: integrating multiple
experiences. Anim Behav. 57:903–910.
Jacobs A, Sueur C, Deneubourg JL, Petit O. 2011. Social network influ-
ences decision making during collective movements in Brown Lemurs
(Eulemur fulvus fulvus). Int J Primatol. 32:721–736.
Johnstone RA, Manica A. 2011. Evolution of personality dierences in
leadership. Proc Natl Acad Sci. 108:8373–8378.
Jolles JW, King AJ, Manica A, Thornton A. 2013. Heterogeneous structure
in mixed-species corvid flocks in flight. Anim Behav. 85:743–750.
Jolles JW, Ostojić L, Clayton NS. 2013. Dominance, pair bonds and bold-
ness determine social-foraging tactics in rooks, Corvus frugilegus. Anim
Behav. 85:1261–1269.
King AJ, Douglas CMS, Huchard E, Isaac NJB, Cowlishaw G. 2008.
Dominance and aliation mediate despotism in a social primate. Curr
Biol. 18:1833–1838.
King AJ, Fürtbauer I, Mamuneas D, James C, Manica A. 2013. Sex-
dierences and temporal consistency in stickleback fish boldness. PLoS
One. 8:e81116.
King AJ, Johnson DDP, Van Vugt M. 2009. The origins and evolution of
leadership. Curr Biol. 19:R911–916.
Krause J, Reeves P, Hoare D. 1998. Positioning behaviour in Roach shoals:
the role of body length and nutritional state. Behaviour. 135:1031–1039.
Krause J, Ruxton GD. 2002. Living in groups. Oxford: Oxford University Press.
Kurvers RHJM, Eijkelenkamp B, van Oers K, van Lith B, van Wieren SE,
Ydenberg RC, Prins HHT. 2009. Personality dierences explain leader-
ship in barnacle geese. Anim Behav. 78:447–453.
Lessells CM, Boag PT. 1987. Unrepeatable repeatabilities: a common mis-
take. Auk. 104:116–121.
Magnhagen C, Bunnefeld N. 2009. Express your personality or go along
with the group: what determines the behaviour of shoaling perch? Proc
R Soc B. 276:3369–3375.
McClure M, Ralph M, Despland E. 2011. Group leadership depends on
energetic state in a nomadic collective foraging caterpillar. Behav Ecol
Sociobiol. 65:1573–1579.
Nagy M, Akos Z, Biro D, Vicsek T. 2010. Hierarchical group dynamics in
pigeon flocks. Nature. 464:890–893.
Nakayama S, Harcourt JL, Johnstone RA, Manica A. 2012. Initiative,
personality and leadership in pairs of foraging fish. PLoS One.
Nakayama S, Johnstone RA, Manica A. 2012. Temperament and hunger
interact to determine the emergence of leaders in pairs of foraging fish.
PLoS One. 7:e43747.
Nakayama S, Stumpe MC, Manica A, Johnstone RA. 2013. Experience
overrides personality dierences in the tendency to follow but not in the
tendency to lead. Proc R Soc B. 280:20131724.
Peterson R, Jacobs A. 2002. Leadership behavior in relation to domi-
nance and reproductive status in gray wolves, Canis lupus. Can J Zool.
Petit O, Bon R. 2010. Decision-making processes: the case of collective
movements. Behav Processes. 84:635–647.
Pettit B, Perna A, Biro D, Sumpter DJT. 2013. Interaction rules underlying
group decisions in homing pigeons. J R Soc Interface. 10:20130529.
Pike TW, Samanta M, Lindström J, Royle NJ. 2008. Behavioural phe-
notype aects social interactions in an animal network. Proc R Soc B
R Development Core Team. 2013. R: A language and environ-
ment for statistical computing. Vienna: R Foundation for Statistical
Réale D, Festa-Bianchet M. 2003. Predator-induced natural selection on
temperament in bighorn ewes. Anim Behav. 65:463–470.
Reebs S. 2001. Influence of body size on leadership in shoals of golden
shiners, Notemigonus crysoleucas. Behaviour. 138:797–809.
Reebs SG. 2000. Can a minority of informed leaders determine the forag-
ing movements of a fish shoal? Anim Behav. 59:403–409.
Sueur C, Petit O. 2008. Shared or unshared consensus decision in
macaques? Behav Processes. 78:84–92.
Vicsek T, Zafeiris A. 2012. Collective motion. Phys Rep. 517:71–140.
Ward AJW, Herbert-Read JE, Jordan LA, James R, Krause J, Ma Q ,
Rubenstein DI, Sumpter DJT, Morrell LJ. 2013. Initiators, leaders, and
recruitment mechanisms in the collective movements of damselfish. Am
Nat. 181:748–760.
Ward AJW, Thomas P, Hart PJB, Krause J. 2004. Correlates of boldness in
three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol.
Wolf M, Van Doorn GS, Weissing FJ. 2011. On the coevolution of
social responsiveness and behavioural consistency. Proc R Soc B.
Page 7 of 7
at Cambridge University Library on August 22, 2014 from
... Focusing solely on variability in individual personality (only one aspect of individual heterogeneity), for example, we would predict a negative relationship between boldness levels and the strength of social bonds [63], a positive relationship between boldness levels and the time needed to develop a social bond [64] and between homophily in personality and strength in social bonds [65], regardless of the type of experience. As bold individuals are less risk averse [66] and they show an overall more consistent behaviour [67,68], we would also predict fewer differences in the effect of positive or negative experiences for the development of social bonds compared to shy individuals. We would also hypothesize differences in the effect of positive or negative experiences for the development of social bonds depending not only on individual boldness level but also on partner personality. ...
... Although boldness level is consistent over time [69], there may be short-term behavioural variations due to partner personality (i.e. shy individuals become bolder when associated with bold individuals: [67], but see also [70]) or previous social experiences (i.e. bold individuals become bolder if they where previously associated with shy individuals: [67]). ...
... shy individuals become bolder when associated with bold individuals: [67], but see also [70]) or previous social experiences (i.e. bold individuals become bolder if they where previously associated with shy individuals: [67]). Thus, we would expect a smaller effect of partner personality, but also a stronger effect of prior social experiences, in the case of bold compared to shy individuals. ...
Full-text available
Group-living animals can develop social bonds. Social bonds can be considered a type of social relationship characterized by frequent and consistent affiliative (non-reproductive) interactions. Social bonds with conspecifics bring many advantages, also in terms of direct fitness. A characteristic of social bonds is that they need time to develop. Several studies on humans have emphasized the fact that sharing experiences can affect the strength of social bonds. A similar trend can be spotted in non-human species. For example, a recent experiment showed that if chimpanzees watched a video together with a conspecific, they spent more time in proximity compared to conspecifics with whom they did not actively watch a video. Another experiment on fish showed that individuals who experienced a situation of high predation risk together, showed preference for each other compared to those who did not. As the link between shared experiences and social bonds is not explicitly recognized in non-human animals, the main goal of this work is to propose the exploration of this novel research path. This exploration would contribute to shed light on the evolutionary mechanisms of social bond (or friendship) development and maintenance between individuals in different vertebrate species, from fish to non-human primates.
... This asymmetry can be reinforced by the social composition of the group with shy individuals enhancing leadership b y bold ones [98]. In addition, bolder individuals show a lower behavioural plasticity than shyer ones, even when rewarded after following a partner rather than taking the lead [115,168]. Thus, although each individual can initiate a collective movement, some characteristics may enhance the probability of some fish to take the leadership more often than others. ...
... We test the hypothesis that, to drive the biohybrid groups towards a predefined choice, the robots have to adopt some specific, fish-like behaviours. Several studies have shown the influence of personality in collective movements often described by the opposition of bold and shy behaviour [98,115,168,254]. Here, we test both a bold behaviour with a robot performing collective departures towards the target and a shy behaviour with a robot delaying collective departures from the target. ...
Collective movement can be observed throughout the animal kingdom, particularly in fish. Yet, despite many studies on the subject, the decision-making mechanisms of these collective events remain poorly understood.In this thesis, we want to better understand collective movement by studying more precisely the decision-making process, the organisation and the cohesion of groups of social fish. Our study focuses on the zebrafish (Danio rerio), a model used in different areas of research. To highlight those behaviours, we have developed a specific constrained environment composed of two rooms connected by a corridor. Cohesion on groups of different sizes and the organisation of leadership have been examined. The collective behaviour of zebrafish in a constrained environment was then described throughout a multi-contextual stochastic model. We have also developed a robotic agent to determine the importance of aspect and behaviour in conspecific recognition. Finally, after its integration into the group, we influenced the movements of the fish group with this biomimetic and autonomous fish robot to test our hypotheses on the different rules underlying collective movements.We have achieved the following results. In a constrained environment, fish use the rooms as resting areas and frequently move from one area to another. We observed that the size of fish groups influences the structure and proportion of these transitions. Group size also changes the cohesion between individuals and their spatial distribution. We studied more precisely the decision-making process during transitions, and in particular the mechanics of leadership. We have shown that leadership is shared among all individuals in a group, with heterogeneous sharing modalities between the different groups studied. The stochastic model developed from these results correctly simulates fish group behaviour in a constrained environment, using different parameter values according to the position of the agent. We have succeeded in integrating an autonomous and biomimetic fish robot into a group of zebrafish. The use of the stochastic model to drive the robot has highlighted the importance of biomimetic behaviour in the process of recognising a conspecific. Finally, we modulated the behaviour of the zebrafish with the fish robot by inducing collective departures as well as significantly biasing the distribution of fish between the two rooms. These positive results allow us to validate the hypotheses about leadership and cohesion among social fish.
... Finally, because of the close proximity of individuals in the pair housing, we expected social conformity effects 23,[31][32][33] where pen-mates would show greater similarity in distance travelled and residence times than other randomly chosen individuals in the population (prediction 5). Lastly, we investigated the potential for carry-over effects from the pair housing [34][35][36] , where the behaviour in the group housing may be affected by the individuals previous experience in the pair housing, and specifically partner personality (prediction 6). ...
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Individual consistency in behaviour, known as animal personality, and behavioural plasticity in response to environmental changes are important factors shaping individual behaviour. Correlations between them, called personality-dependent plasticity, indicate that personality can affect individual reactions to the environment. In farm animals this could impact the response to management changes or stressors but has not yet been investigated. Here we use ultra-wideband location sensors to measure personality and plasticity in the movement of 90 dairy calves for up to 56 days starting in small pair-housing enclosures, and subsequently moved to larger social housings. For the first time calves were shown to differ in personality and plasticity of movement when changing housing. There were significant correlations between personality and plasticity for distance travelled (0.57), meaning that individuals that travelled the furthest in the pair housing increased their movement more in the social groups, and for residence time (− 0.65) as those that stayed in the same area more decreased more with the change in housing, demonstrating personality-dependent plasticity. Additionally, calves conformed to their pen-mate’s behaviour in pairs, but this did not continue in the groups. Therefore, personality, plasticity and social effects impact how farm animals respond to changes and can inform management decisions.
... For instance, it has been previously described that fish are more active and display increased exploratory behaviour when in the company of others [308][309][310] . Conversely, when isolated, fish are more persistent in their attention towards novel visual stimuli 310 . ...
Social behaviours are essential for the survival and reproduction of many species, including our own. A fundamental feature of all social behaviour is social preference, which is an individual’s propensity to interact with members of their species (termed conspecifics). In an average population, various social preference behaviours are readily observed, ranging from uninterested (not engaging with conspecifics) to very social (engaging with conspecifics). Individuals expressing these behaviours are typically labelled as having an asocial or prosocial, respectively. Little is known about how the underlying social circuitry gives rise to such distinct social behaviours in the population. It is well established that adverse social experiences can impact social behaviour, including isolation during early development. Undesired social isolation (loneliness) alters behavioural patterns, neuroanatomy (e.g., brain volume) and neurochemistry in ways that resemble developmental neuropsychiatric disorders, including autism and schizophrenia. However, few studies have investigated the impact of early life isolation on social circuitry, and how this results in dysfunctional social behaviour commonly associated with these and other disorders. In this thesis, juvenile zebrafish was used to model social preference behaviour, as it is an excellent translational model for human developmental and behavioural disorders. Population-level analysis revealed that several features of social preference behaviour could be summarised via Visual Preference Index (VPI) scores representing sociality. Using multiple behavioural parameters, comprehensive investigations of asocial and prosocial fish identified via VPIs revealed distinct responses towards conspecifics between the two phenotypes. These initial results served as a baseline for facilitating the identification of atypical social behaviour following periods of social isolation. The impact of isolation on social preference was assessed by applying either the full isolation over the initial three weeks of development or partial isolation, 48 hours or 24 hours, before testing. Following periods of social isolation, juvenile zebrafish displayed anxiety-like behaviours. Furthermore, full and partial isolation of 48 hours, but not 24 hours, altered responses to conspecifics. To assess the impact of social isolation on the social circuitry, the brain activities of fish were analysed and compared between different rearing conditions using high-resolution two-photon imaging. Whole-brain functional maps of isolated social phenotypes were distinct from those in the average population. Isolation-induced activity changes were found mainly in brain regions linked to social behaviour, social cue processing, and anxiety/stress (e.g., the caudal hypothalamus and preoptic area). Since some of these affected regions are modulated by serotonin, the reversibility of the adverse effects of social isolation on preference behaviour was investigated by using pharmacological manipulation of the monoaminergic system. The administration of an anxiolytic the drug buspirone demonstrated that altered social preference behaviour in isolated fish could be rescued by acutely reducing serotonin levels. By investigating social preference at the behavioural and functional level in wild-type juvenile zebrafish, this work contributes to our understanding of how the social brain circuity produces diverse social preferences. Furthermore, it provides important information on how early-life environmental adversity gives rise to atypical social behaviour and the neurotransmitters modulating the circuit, offering new opportunities for effective intervention.
... This hypothesis is motivated by previous work indicating that individual animals can strongly influence group behaviour [1,2,[29][30][31][32]. However, that literature has generally not focused on prior social experience as a factor that generates differences among influential group members (but see [33][34][35]), and we know of no studies that implicate IGE as a cause of such differences. ...
Full-text available
Understanding how individual differences arise and how their effects propagate through groups are fundamental issues in biology. Individual differences can arise from indirect genetic effects (IGE): genetically based variation in the conspecifics with which an individual interacts. Using a clonal species, the Amazon molly ( Poecilia formosa ), we test the hypothesis that IGE can propagate to influence phenotypes of the individuals that do not experience them firsthand. We tested this by exposing genetically identical Amazon mollies to conspecific social partners of different clonal lineages, and then moving these focal individuals to new social groups in which they were the only member to have experienced the IGE. We found that genetically different social environments resulted in the focal animals experiencing different levels of aggression, and that these IGE carried over into new social groups to influence the behaviour of naive individuals. These data reveal that IGE can cascade beyond the individuals that experience them. Opportunity for cascading IGE is ubiquitous, especially in species with long-distance dispersal or fission–fusion group dynamics. Cascades could amplify (or mitigate) the effects of IGE on trait variation and on evolutionary trajectories. Expansion of the IGE framework to include cascading and other types of carry-over effects will therefore improve understanding of individual variation and social evolution and allow more accurate prediction of population response to changing environments.
... Indeed, experiments with pairs of stickleback fish (Harcourt et al. 2009;Nakayama et al. 2012Nakayama et al. , 2016 have shown that individuals that are more likely to leave cover and explore their environment when tested alone ("bolder" individuals) are more likely to lead their partners, whereas fish that are less likely to leave cover when alone ("shyer" individuals) follow their partners motion and elicit greater leadership tendencies in their bold partners. Other work has shown the likelihood of individuals to approach conspecifics is negatively correlated with an individual's tendency to leading stickleback dyads and shoals (Jolles et al. 2014(Jolles et al. , 2017. In this study, we tested whether fish motion in small start boxes prior to the start of trials predicted leadership. ...
Full-text available
Studies of self-organizing groups like schools of fish or flocks of birds have sought to uncover the behavioral rules individuals use (local-level interactions) to coordinate their motion (global-level patterns). However, empirical studies tend to focus on short-term or one-off observations where coordination has already been established or describe transitions between different coordinated states. As a result, we have a poor understanding of how behavioral rules develop and are maintained in groups. Here, we study the emergence and repeatability of coordinated motion in shoals of stickleback fish (Gasterosteus aculeatus). Shoals were introduced to a simple environment, where their spatio-temporal position was deduced via video analysis. Using directional correlation between fish velocities and wavelet analysis of fish positions, we demonstrate how shoals that are initially uncoordinated in their motion quickly transition to a coordinated state with defined individual leader-follower roles. The identities of leaders and followers were repeatable across two trials, and coordination was reached more quickly during the second trial and by groups of fish with higher activity levels (tested before trials). The rapid emergence of coordinated motion and repeatability of social roles in stickleback fish shoals may act to reduce uncertainty of social interactions in the wild, where individuals live in a system with high fission-fusion dynamics and non-random patterns of association.
... We believe that more studies are warranted to explore variation in emergence time between social and solo test conditions. In adult individuals of other fish species, social conditions have also been shown to affect behavioural tendencies, with individuals that were kept in a group instead of solo prior to testing being more active and explorative (Gómez-Laplaza and Morgan 1991;Jolles et al. 2014). If the context is compared in one and the same experiment, unlike our current comparison between two different studies (Tudorache et al. 2014 and the current study), it is also easier to exclude potentially confounding variables for the current speculation, such as subtle variation in light or handling conditions, which may vary per room and experimenter and which may affect relative stress levels of the larvae in the test. ...
Full-text available
Standardization and reduction of variation is key to behavioural screening of animal models in toxicological and pharmacological studies. However, individual variation in behavioural and physiological phenotypes remains in each laboratory population and can undermine the understanding of toxicological and pharmaceutical effects and their underlying mechanisms. Here, we used zebrafish (ABTL-strain) larvae to explore individual consistency in activity level and emergence time, across subsequent days of early development (6–8 dpf). We also explored the correlation between these two behavioural parameters. We found inter-individual consistency over time in activity level and emergence time, but we did not find a consistent correlation between these parameters. Subsequently, we investigated the impact of variation in activity level on the effect of a 1% ethanol treatment, suitable for our proof-of-concept case study about whether impact from pharmacological treatments might be affected by inter-individual variation in basal locomotion. The inter-individual consistency over time in activity level did not persist in this test. This was due to the velocity change from before to after exposure, which turned out to be a dynamic individual trait related to basal activity level: low-activity individuals raised their swimming velocity, while high-activity individuals slowed down, yielding diametrically opposite response patterns to ethanol exposure. We therefore argue that inter-individual consistency in basal activity level, already from 6 dpf, is an important factor to take into account and provides a practical measure to improve the power of statistical analyses and the scope for data interpretation from behavioural screening studies.
Personality widely exists in diverse animal taxa. Such inter-individual variance in behaviour is supposed to be influenced by social context. However, it remains unknown whether the experience of social life has any carryover effects on the subsequent expression of personality. Here, we examined exploratory behaviour in caged Java Sparrows (Lonchura oryzivora) using exploration assays. Birds were assigned to live in either a solitary or a social context for four weeks. We compared the expressions of exploration before and after the treatments, and found that birds showed higher exploration tendencies after than before social life, while the isolated birds were consistent in their exploratory behaviours. Different living experience led to differences in the exploration activities for birds without significant differences in exploration before. Our results indicate that social experience can make birds more proactive.
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Behavioral flexibility is considered important for a species to adapt to environmental change. Yet behavioral flexibility relates to problem solving ability and speed in unpredictable ways. This leaves an open question of whether behavioral flexibility instead varies with differences in individual behaviors, such as neophobia or exploration. If present, such correlations would mask which behavior causes individual variation. I investigated whether behavioral flexibility (reversal learning) performances were linked with other behaviors in great-tailed grackles, an invasive bird. I found that behavioral flexibility did not significantly correlate with neophobia, exploration, risk aversion, persistence, or motor diversity. This suggests that great-tailed grackle performance in behavioral flexibility tasks reflect a distinct source of individual variation. Maintaining multiple distinct sources of individual variation, and particularly variation in behavioral flexibility, may be a mechanism for this species’ invasion success by permitting populations to cope with the diversity of novel elements in their environments.
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Behavioral flexibility is considered important for a species to adapt to environmental change. Yet behavioral flexibility relates to problem solving ability and speed in unpredictable ways. This leaves an open question of whether behavioral flexibility instead varies with differences in individual behaviors, such as neophobia or exploration. If present, such correlations would mask which behavior causes individual variation. I investigated whether behavioral flexibility (reversal learning) performances were linked with other behaviors in great-tailed grackles, an invasive bird. I found that behavioral flexibility did not significantly correlate with neophobia, exploration, risk aversion, persistence, or motor diversity. This suggests that great-tailed grackle performance in behavioral flexibility tasks reflect a distinct source of individual variation. Maintaining multiple distinct sources of individual variation, and particularly variation in behavioral flexibility, may be a mechanism for this species’ invasion success by permitting populations to cope with the diversity of novel elements in their environments.
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There is no information on whether the daily foraging movements of fish shoals are the result of chance, the collective will of all shoalmates, or the leadership of a few individuals. This study tested the latter possibility. Shoals of 12 golden shiners, Notemigonus crysoleucas, were trained to expect food around midday in one of the brightly lit corners of their tank. They displayed daily food-anticipatory activity by leaving the shady area of their tank and spending more and more time in the food corner up to the normal time of feeding. Past this normal time they remained in the shade, even on test days when no food was delivered. Most of these experienced individuals were then replaced by naïve ones. The resulting ratio of experienced:naïve fish could be 5:7, 3:9 or 1:11. On their own, naïve individuals would normally spend the whole day in the shade, but in all tests the experienced individual(s) were able to entrain these more numerous naïve fish out of the shade and into the brightly lit food corner at the right time of day. Entrainment was stronger in the 5:7 than in the 1:11 experiment. The test shoals never split up and were always led by the same fish, presumably the experienced individuals. These results indicate that in a strongly gregarious species, such as the golden shiner, a minority of informed individuals can lead a shoal to food, either through social facilitation of foraging movements or by eliciting following behaviour. Copyright 2000 The Association for the Study of Animal Behaviour.
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We examined whether variation in group exploratory behavior was linked with variation in personality traits (boldness, activity, and sociability) in a population of feral guppies (Poecilia reticulata). A huge amount of variation was observed in dispersal tendency between shoals. Surprisingly, no significant correlations were found between group exploratory behavior and average group personality scores, which suggests that the movement of the shoal was not generated by group conformity. However, our analysis revealed correlations between group exploration and the activity score of the least active member of a group and the sociality index of the most social member of a group. These results indicate that a minority of key individuals with certain personality types can have substantial effects on group behavior. These results are discussed in the broader context of group decision making in social animals.
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Socially foraging animals can search for resources themselves (produce) or exploit the discoveries made by others (scrounge). The extensive literature on producer-scrounger dynamics has mainly focused on scramble competition over readily accessible resources, thereby largely neglecting the variety of scrounging techniques individuals may use as well as the role of investment in food handling. Furthermore, although individual differences in boldness and social factors such as dominance have been described to influence foraging tactics, their potential interplay and effect in foraging contexts beyond the conventional producer-scrounger game remains unclear. We investigated the relationship between social-foraging tactic use and dominance, pair bonds and boldness in a foraging experiment focused on food handling and alternative scrounging tactics. We conducted a producer-scrounger experiment in a captive group of rooks in which individuals could produce by pulling up baited strings, or scrounge by retrieving fallen food items or joining a producer. There were three key findings: (1) dominant rooks adopted the producer tactic more often and more successfully than subordinates; (2) producing and scrounging by tolerance led to mixed benefits to paired birds; (3) bold birds scrounged by retrieving more often than shy birds. Importantly, individuals were highly consistent in their tactic use across conditions differing in food availability. Our study highlights the importance of taking both social factors and boldness (heterogeneity) into account when studying social-foraging dynamics and offers empirical data on food handling and alternative scrounging tactics that can be used to extend current models and experiments on social foraging.
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Behavioural traits that co-vary across contexts or situations often reflect fundamental trade-offs which individuals experience in different contexts (e.g. fitness trade-offs between exploration and predation risk). Since males tend to experience greater variance in reproductive success than females, there may be considerable fitness benefits associated with "bolder" behavioural types, but only recently have researchers begun to consider sex-specific and life-history strategies associated with these. Here we test the hypothesis that male three-spined sticklebacks (Gasterosteus aculeatus) show high risk but potentially high return behaviours compared to females. According to this hypothesis we predicted that male fish would show greater exploration of their environment in a foraging context, and be caught sooner by an experimenter than females. We found that the time fish spent out of cover exploring their environment was correlated over two days, and males spent significantly more time out of cover than females. Also, the order in which fish were net-caught from their holding aquarium by an experimenter prior to experiments was negatively correlated with the time spent out of cover during tests, and males tended to be caught sooner than females. Moreover, we found a positive correlation between the catch number prior to our experiments and nine months after, pointing towards consistent, long-term individual differences in behaviour.
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Travelling in groups gives animals opportunities to share route information by following cues from each other's movement. The outcome of group navigation will depend on how individuals respond to each other within a flock, school, swarm or herd. Despite the abundance of modelling studies, only recently have researchers developed techniques to determine the interaction rules among real animals. Here, we use high-resolution GPS (global positioning system) tracking to study these interactions in pairs of pigeons flying home from a familiar site. Momentary changes in velocity indicate alignment with the neighbour's direction, as well as attraction or avoidance depending on distance. Responses were stronger when the neighbour was in front. From the flocking behaviour, we develop a model to predict features of group navigation. Specifically, we show that the interactions between pigeons stabilize a side-by-side configuration, promoting bidirectional information transfer and reducing the risk of separation. However, if one bird gets in front it will lead directional choices. Our model further predicts, and observations confirm, that a faster bird (as measured from solo flights) will fly slightly in front and thus dominate the choice of homing route. Our results explain how group decisions emerge from individual differences in homing flight behaviour.
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Flocks of birds in flight represent a striking example of collective behaviour. Models of self-organization suggest that repeated interactions among individuals following simple rules can generate the complex patterns and coordinated movements exhibited by flocks. However, such models often assume that individuals are identical and interchangeable, and fail to account for individual differences and social relationships among group members. Here, we show that heterogeneity resulting from species differences and social structure can affect flock spatial dynamics. Using high-resolution photographs of mixed flocks of jackdaws, Corvus monedula, and rooks, Corvus frugilegus, we show that birds preferentially associated with conspecifics and that, like high-ranking members of single-species groups, the larger and more socially dominant rooks positioned themselves near the leading edge of flocks. Neighbouring birds showed closer directional alignment if they were of the same species, and neighbouring jackdaws in particular flew very close to one another. Moreover, birds of both species often flew especially close to a single same-species neighbour, probably reflecting the monogamous pair bonds that characterize these corvid social systems. Together, our findings demonstrate that the characteristics of individuals and their social systems are likely to result in preferential associations that critically influence flock structure.
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In many animal groups, coordinated activity is facilitated by the emergence of leaders and followers. Although the identity of leaders is to some extent predictable, most groups experience frequent changes of leadership. How do group members cope with such changes in their social role? Here, we compared the foraging behaviour of pairs of stickleback fish after a period of either (i) role reinforcement, which involved rewarding the shyer follower for following, and the bolder leader for leading, or (ii) role reversal, which involved rewarding the shyer follower for leading, and the bolder leader for following. We found that, irrespective of an individual's temperament, its tendency to follow is malleable, whereas the tendency to initiate collective movement is much more resistant to change. As a consequence of this lack of flexibility in initiative, greater temperamental differences within a pair led to improved performance when typical roles were reinforced, but to impaired performance when typical roles were reversed.
In sticklebacks, sexual maturation is stimulated by long photoperiods but not by short photoperiods, even at high temperatures. Extra-retinal photoreception can mediate this response, and appears to be more important than retinal photoreception. Although plasma melatonin levels are high at night and low during the day, experiments using melatonin administration via the water indicate that melatonin is of no or little importance for the photoperiodic response. Androgens can be aromatised to estrogens in the stickleback brain. Treatment with aromatase inhibitors stimulates maturation of males also under short photoperiod, suggesting that aromatase is involved in the suppressive actions of short photoperiod. Expression of both follicle stimulating hormone (FSH)-beta and luteinizing hormone (LH)-beta is higher under long than under short photoperiod. FSH-beta is controlled by a negative steroid feedback on the brain-pituitary-gonad axis under short photoperiod and by a positive steroid feedback under long photoperiod. It is suggested that the former can suppress reproduction under short photoperiod and the latter can stimulate breeding under long photoperiod.
We analyzed the leadership behavior of breeding and nonbreeding gray wolves (Canis lupus) in three packs during winter in 1997-1999. Scent-marking, frontal leadership (time and frequency in the lead while traveling), initiation of activity, and nonfrontal leadership were recorded during 499 h of ground-based observations in Yellowstone National Park. All observed scent-marking (N=158) was done by breeding wolves, primarily dominant individuals. Dominant breeding pairs provided most leadership, consistent with a trend in social mammals for leadership to correlate with dominance. Dominant breeding wolves led traveling packs during 64% of recorded behavior bouts (N=591) and 71% of observed travel time (N=64 h). During travel, breeding males and females led packs approximately equally, which probably reflects high parental investment by both breeding male and female wolves. Newly initiated behaviors (N=104) were prompted almost 3 times more often by dominant breeders (70%) than by nonbreeders (25%). Dominant breeding females initiated pack activities almost 4 times more often than subordinate breeding females (30 vs. 8 times). Although one subordinate breeding female led more often than individual nonbreeders in one pack in one season, more commonly this was not the case. In 12 cases breeding wolves exhibited nonfrontal leadership. Among subordinate wolves, leadership behavior was observed in subordinate breeding females and other individuals just prior to their dispersal from natal packs. Subordinate wolves were more often found leading packs that were large and contained many subordinate adults.