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RESEARCH PAPER
Indirect Information Transfer: Three-Spined Sticklebacks UseVisual Alarm Cues From Frightened Conspecifics About anUnseen PredatorKelly E. Hogan & Kate L. Laskowski
School of Integrative Biology, University of Illinois, Urbana, IL, USA
Correspondence
Kate L. Laskowski, School of Integrative
Biology, University of Illinois, 515 Morrill Hall,
Urbana, IL 61801, USA.
E-mail: [email protected]
Received: April 4, 2013
Initial acceptance: July 8, 2013
Final acceptance: August 2, 2013
(D. Zeh)
doi: 10.1111/eth.12143
Abstract
Animals can attempt to reduce uncertainty about their environment by
gathering information personally or by observing others’ interactions with
the environment. There are several sensory modalities that can be used to
transmit social information from chemical to visual to audible cues. When
predation risk is variable, visual cues of conspecific behavior might be
especially telling about the presence of a potential threat; however, most
studies couple visual and chemical cues together. Here, we tested whether
visual behavioral cues from frightened conspecifics were sufficient to indi-
rectly transfer information about the presence of an unseen predator in
three-spined sticklebacks. Our results demonstrate that visual behavioral
cues from conspecifics about the presence of a predator are sufficient to
induce an antipredator response. This suggests that information transfer
can occur rapidly in the absence of chemical cues and that some individu-
als weigh social information more heavily than others.
Introduction
Animals must use imperfect information to make
decisions about where to forage, find a mate, and
avoid predators. One way to deal with this environ-
mental uncertainty is to use social information, which
has been broadly defined as the monitoring of others’
interactions with the environment (Danchin et al.
2004). Observing the behaviors of neighbors provides
rapid indirect information regarding the environment,
especially when acquiring direct information is unfea-
sible. Specifically, social information, whether as
deliberate signals or inadvertent cues, can help reduce
uncertainty by providing information regarding the
quality of a feature such as a foraging patch or draw
attention to the location of a stimulus such as the pres-
ence of a predator (Brown & Laland 2002). The intra- and
interspecific transfer of social information is taxonomically
widespread and has been observed in a variety of ecological
contexts including foraging, mate choice, and antipredatory
behavior (Rieucau & Giraldeau 2011). Arguably, any
action taken by one individual can be used as social
information to another individual; however, the reli-
ability of social information can vary dramatically.
Indeed, a growing body of the literature has provided
empirical evidence that individuals across taxa prefer
personally acquired information to socially acquired
information in many contexts (birds: Templeton &
Giraldeau 1996; Marchetti & Drent 2000; nine-spined
sticklebacks: van Bergen et al. 2004; reviewed in
Rieucau & Giraldeau 2011). One such context in
which individuals may weigh social information more
heavily is one in which there is a high predation risk
(Laland 2004). For example, guppies will prefer per-
sonal information in the absence of a predation risk,
but rely on social information when predation risk is
high, even if it conflicts with previously acquired
personal information (Kendal et al. 2004).
Social information can be transmitted using sev-
eral avenues, and the sensory modality of indirect
information transfer (i.e. chemical, visual, auditory)
can strongly influence its reliability. Within fishes,
particular attention has been given to assessing the
use of chemical cues (Brown 2003). However,
chemical cues of a predator–prey interaction may
linger long after the predator risk has passed.
Ethology 119 (2013) 1–7 © 2013 Blackwell Verlag GmbH 1
Ethology
Therefore, when direct information is not available
to an individual about the presence of a predator,
individuals may rely on more indirect methods, such
as observing the behavior of other conspecifics (Kats
& Dill 1998; Brown 2003). Visual cues may be espe-
cially salient in shoaling species; any individual that
behaves differently from surrounding individuals
might be more conspicuous and therefore more
susceptible to predation due to the ‘oddity effect’
(Landeau & Terborgh 1986). And so while it is well
known that many fish species rely on the use of
chemical cues (reviewed in Brown 2003), less is
known about whether visual cues are sufficient to
also induce an antipredator response in observing
individuals. This is despite the fact that visual cues
may provide a very rapid method through which to
transfer social information through a group of
animals.
Therefore, in this study, we tested whether visual
behavioral cues from conspecific demonstrators are
sufficient to induce an antipredator response in a focal
individual.
To address this question, we used three-spined
sticklebacks (Gasterosteaus aculeatus), a model behav-
ioral organism that is known to use social informa-
tion in other contexts (Coolen et al. 2005) and
shows extensive behavioral variation (Huntingford
1976; Bell 2005; Dingemanse et al. 2007). Three-
spined sticklebacks are geographically widespread
and can live in a variety of habitats (Bell & Foster
1994) where direct visual access to predators may
not always be possible. We created an experimental
paradigm where a focal individual could observe the
behavior of a group of demonstrator sticklebacks in
the absence of chemical cues. We presented the dem-
onstrator sticklebacks with a model Northern pike
predator (Esox lucius), which was not visible to the
focal individual and then observed the behavior of
both the demonstrators and focal individual. While
sticklebacks co-occur with pike across much of their
range in the Northern Hemisphere (Bell & Foster
1994), there are no pike present within our particu-
lar population; however, previous work has demon-
strated that a model pike will elicit a strong
antipredator response in na€ıve sticklebacks (Grobis
et al. 2013).
Materials and Methods
Animal Care and Maintenance
All fish were wild-caught adults from the Navarro
River in northern California. As pike do not occur in
this river, we can ensure that any behavioral differ-
ences among individuals are not due to previous per-
sonal experience with this predator in the wild. Fish
were housed in the laboratory for at least 6 mo prior
to the experiment on a light cycle that mimicked nat-
ural light conditions at their place of capture. Fish
were fed an ad libitum diet of bloodworms, mysis, and
brine shrimp daily. All fish were visibly non-
reproductive, free of parasites, and sized matched
(35–40 mm). Fish were haphazardly assigned as
either a focal or a demonstrator. Focal individuals
were only used once (n = 16), whereas demonstrator
fish were used repeatedly (two groups of three dem-
onstrators). Data were collected in Feb. 2012, and
after completion of the experiment, all fish were
housed at the University until their natural death.
Animal care and behavioral protocols are approved by
the University of Illinois’s Institutional Animal Care
and Use Committee (#11128).
Social Information Use Assay
The same observer (KEH) scored the behavior in all
assays. The social information use arena consisted of
two separate 37.8 L aquaria (50.8 9 25.4 9 30.5 cm)
placed adjacent to one another to form an ‘L’ shape
(Fig. 1). A model pike was attached to a runner that
fit on the top edge of the demonstrator aquarium, and
the pike could be moved remotely by the observer.
We chose to use a model pike, because pike are natu-
ral predators of sticklebacks, and models of pike have
Fig. 1: Schematic of the social information use assay arena. Two aqua-
ria were arranged so the focal individual (white) was in one and the
demonstrators (gray) and model pike (black) in the other. The focal indi-
vidual was visually separated from the model pike, but not the demon-
strators. The demonstrators and model pike were separated by a
permanent clear divider (dotted line) and an opaque divider (dashed
line) that could be removed during the the trial.
Ethology 119 (2013) 1–7 © 2013 Blackwell Verlag GmbH2
Indirect Information Transfer Through Behavioral Alarm Cues K. E. Hogan & K. L. Laskowski
been shown to induce a fear response in sticklebacks
(McGhee et al. 2012; Grobis et al. 2013). The pike
model (approx. 8 inches) was handmade (by KLL)
using waterproof epoxy and painted with lifelike
markings using a dead frozen pike as a model. The
demonstrator aquarium contained three size-matched
sticklebacks that were approx. 10% larger than the
focal individual. Within the demonstrator aquarium,
there were two barriers: a transparent, non-
removable barrier, which physically separated the
demonstrators from the model pike and an opaque,
removable barrier, which prevented the demonstra-
tors from seeing the model pike. It is important to
note that the demonstrators and focal individuals
were kept in separate (but closely adjacent) aquaria.
This arrangement allowed the demonstrators to view
the model pike, but prevented the focal individual
from seeing the pike. This reduced the chance for the
focal individual to pick up on vibrational cues that
may have occurred from the lifting and lowering of
the opaque barrier. To ensure that the raising and
lowering of the barrier did not influence focal behav-
ior, we also performed a series of control observations
using only focal individuals with no demonstrators or
pike model. We found focal behavior to be unaffected
by the raising and lowering of the barrier (data not
shown). These control focal individuals were not used
in any other part of the experiment. Therefore,
behaviors exhibited by the focal individual should
only be influenced by the demonstrators’ behavior.
A social information use trial consisted of three
3-min periods: baseline behavior (before pike), after
the opaque barrier was lifted to expose the model
pike (during pike), and after the barrier was closed
to remove the model pike from sight (after pike).
For each focal individual, we measured the total
amount of time spent frozen as other studies have
shown this to be an effective antipredator behavior
(Chivers & Smith 1998; McGhee et al. 2012). We
also measured the latency of each focal to begin
moving after the demonstrators had been shown
the pike. To determine whether focal individuals
were directly matching the behavior of the demon-
strators, we also measured the demonstrators’
latency to begin moving. Specifically, we measured
the latency for one demonstrator to begin moving
and the latency for all three demonstrators to begin
moving after being shown the pike. This meant we
recorded the time it took for just one demonstrator
individual to first move again after first being shown
the pike, and the time it took for all three demon-
strators to move at least once after first being shown
the pike.
Statistical Analysis
To determine whether individual sticklebacks used
visual behavioral cues from conspecifics about the
presence of a predator, we compared the average time
spent frozen by the focal individuals during each
period in the social information use assay. Time spent
frozen was compared across periods using a linear
mixed model with period as a fixed factor and focal
individual as a random factor. We used a Tukey’s post
hoc test to determine which, if any, periods differed
from each other. Because of our small sample size, we
calculated a Spearman’s rank correlation between the
focal latency to begin moving and the latency of one
demonstrator to begin moving and also between the
focal latency to begin moving and the latency of three
demonstrators to begin moving. This was carried out
to determine whether focal individuals were using the
activity of just one or all three demonstrators as a cue
to begin moving again after the predator scare. We
then used paired t-tests to test whether focal individu-
als had longer latencies to begin moving compared
with the latencies of one demonstrator or three dem-
onstrators to begin moving. We found no evidence of
differences in any focal behavior due to body size
(effect of body size on: focal latency F1,14 = 3.06,
p = 0.21; time spent frozen before F1,14 = 0.002,
p = 0.97; during F1,14 = 1.46, p = 0.25; after
F1,14 = 0.43, p = 0.53) or between the two different
demonstrator groups (effect of demonstrator group
on: focal latency F1,14 = 1.38, p = 0.26; time spent
frozen before F1,14 = 0.05, p = 0.83; during F1,14= 1.74, p = 0.21; after F1,14 = 0.01, p = 0.99; latency
of one demonstrator F1,14 = 1.53, p = 0.24; latency of
three demonstrators F1,14 = 0.18, p = 0.68), and so,
these factors were removed from all analyses. We also
checked whether the demonstrator groups were influ-
enced by repeated testing and found no evidence for
any effect of trial on either the latency of one demon-
strator to begin moving after the pike (F1,14 = 1.58,
p = 0.23) or the latency of all three demonstrators to
begin moving (F1,14 = 2.68, p = 0.12).
Additionally, we tested whether individual stickle-
backs consistently differ in their response to visual
behavioral conspecific cues over the course of the
social information use assay; we calculated repeatabil-
ity of time spent frozen across the three social infor-
mation use trial periods. Repeatability is a measure of
the proportion of variation that can be attributed to
individual differences (Lessells & Boag 1987). As we
had balanced observations on all individuals and the
data were approximately normal, we calculated an
adjusted repeatability using the variance components
Ethology 119 (2013) 1–7 © 2013 Blackwell Verlag GmbH 3
K. E. Hogan & K. L. Laskowski Indirect Information Transfer Through Behavioral Alarm Cues
from the linear mixed model including period as a
fixed factor and focal as a random factor and deter-
mined its significance using a log-likelihood ratio test
that compared the fit of a model with and without the
random focal factor (Nakagawa & Schielzeth 2010).
All analyses were conducted using R 2.14.0 (www.
r-project.org).
Results
Individuals Use Visual Behavioral Cues From
Demonstrators About the Presence of an Unseen
Predator
To determine whether individual sticklebacks used
visual behavioral cues from conspecifics concerning
the presence of an unseen predator, we compared the
time spent frozen across the three 3-min trial periods
in the social information use assay. Focal individuals
(n = 16) spent on average 47 � 11 s (mean � SE)
frozen before the pike stimulus. Time spent frozen sig-
nificantly increased during the pike (147 � 7 s) and
after the pike (128 � 13 s; F2,30 = 40.407, p < 0.001;
Tukey’s post hoc before pike vs during pike p < 0.001;
before pike vs after pike p < 0.001; during pike vs
after pike p = 0.241, Table 1, Fig. 2), supporting our
hypothesis that focal individuals used visual behav-
ioral cues from conspecific demonstrators about the
presence of unseen predators.
Focal individuals took on average 196 � 26 s to
begin moving after the demonstrators were exposed
to the pike, which is significantly longer than it took
for one demonstrator to recover (69 � 13 s;
t15 = 4.75, p < 0.001). However, this was not signifi-
cantly different from the time it took for all three
demonstrators to recover (180 � 26 s; t15 = 0.538,
p = 0.598). There was also no correlation between
the latency of the focal individual and the latency of
one demonstrator to begin moving (Spearman’s
R = 0.217, p = 0.419, n = 16), although this could be
driven by two focal individuals that never recovered
(Fig. 3a). There was a marginally significant correla-
tion between the latency of the focal individual to
being moving and the latency of all three demonstra-
tors to begin moving (Spearman’s R = 0.440,
p = 0.088, n = 16, Fig. 3b). Taken together, this sug-
gests that the focal individuals may have found visual
behavioral cues from all three demonstrators more
reliable than cues from just one demonstrator.
Even before the pike stimulus, there was variation
in the amount of time individuals spent frozen
(Table 1, Fig. 2). The presence of the pike stimulus
did not remove this variation, rather focal individuals
that were more active before the pike stimulus contin-
ued to be more active during the pike and after the
pike stimulus compared with other focal individuals
(repeatability estimate = 0.43, log-likelihood ratio:
7.41, p = 0.006).
Discussion
In this study, we demonstrate that visual behavioral
cues from conspecifics about the presence of an
unseen predator are sufficient to induce an antipreda-
tor response in individual three-spined sticklebacks.
The aquatic environment provides a medium in
which chemical cues are transferred easily, and there-
fore, a large body of literature has described the trans-
fer of chemical cues between fishes in a variety of
situations. Fewer studies have discriminated between
chemical and visual cues, especially in a predatory
Table 1: Period (fixed) and Focal Individual (random) both had a signifi-
cant effects on the time spent frozen during the social information use
assay
Factor df F-statistic p-Value
Intercept 1,15 160.5 <0.0001
Period 2,30 40.41 <0.0001
Focal Individual 15,30 3.23 0.003
Trial periodBefore During After
Tim
e sp
ent f
roze
n (s
econ
ds)
0
50
100
150
200p < 0.001
p < 0.001
Fig. 2: Time spent frozen by the focal individuals over the three trial
periods. Each line represents a separate focal individual and period
averages (�SE) are shown with the black dots.
Ethology 119 (2013) 1–7 © 2013 Blackwell Verlag GmbH4
Indirect Information Transfer Through Behavioral Alarm Cues K. E. Hogan & K. L. Laskowski
context. However, the transfer of alarm behavior
between conspecifics has been observed in several
non-aquatic taxa suggesting it could be a common
phenomenon (fiddler crabs: Wong et al. 2005; yellow-
hammer bird: van der Veen 2002). In fish, Magurran &
Higham (1988) found that when separated by a one-
way mirror, a shoal of minnows reacted defensively
when viewing alarmed conspecifics. Similarly, a shoal
of zebra danios responded to the fear response of a
chemically, but not visually, isolated shoal of conspe-
cifics (Suboski et al. 1990). These studies, however,
observed the behavior of shoals of fish, creating the
potential for individuals within the shoal to use cues
from their shoal-mates through their lateral line sys-
tem. By observing fish in separate aquaria, our study
provides strong evidence that individual three-spined
sticklebacks respond to visual behavioral cues of
alarmed demonstrators in the absence of chemical or
lateral line cues.
While we found that individuals were quick to
respond to the antipredator behavior of the demon-
strators when the pike was present, and they were
slower to resume normal behavior than individuals in
the demonstrator groups. Most individuals prefer pri-
vate information over social information (reviewed in
Giraldeau et al. 2002), and so, it seems likely that the
focal individuals were less certain the threat had
passed than were the demonstrators (see Laland
2004). The ‘costly information hypothesis’ predicts
that individuals should rely more heavily on social
information when the cost of gathering private infor-
mation may be too high, for example, when a preda-
tor is near (Boyd & Richerson 1985). Webster et al.
(2007) found that three-spined sticklebacks resumed
normal activity faster following a simulated predator
attack when tested in groups than when alone, likely
because the dilution effect reduces the probability of
predation in a group (Turner & Pitcher 1986; Roberts
1996). This may offer another explanation as to why
the group of demonstrators recovered more quickly
than the lone focal individual.
We found that some individuals were more active
than other individuals across the entire social infor-
mation use assay despite the presence of a potential
threat. It is important to note that we only measured
individuals once in this assay; future studies would be
needed to determine whether these differences
among individuals are maintained over longer periods
of time. However, if these differences are maintained,
they could be driven by differences in the individuals’
reliance on social information. Some individuals may
have matched their behavior more closely to the
behavior of the demonstrators. However, given that
there was already extensive variation the time spent
frozen among focal individuals before the pike,
another potential explanation is that the individuals
differ in their level of boldness (e.g. Harcourt et al.
2009; Kurvers et al. 2010). That is, some individuals
may have been more willing to take risks after a
threat than others, regardless of the social information
being provided by the demonstrators. So while there
may be underlying differences in boldness among
individuals, the fact that all individuals increase their
use of antipredator behavior after observing the behav-
ior of the demonstrators demonstrates that three-
spined sticklebacks use visual social information. Our
finding that some individuals were more active than
others over the entire trial adds to the growing body of
the literature that individual sticklebacks differ in their
antipredator behavior (Huntingford 1976; Bell 2005;
Alvarez & Bell 2007; Bell & Sih 2007) and suggest
that a potential reason for this variation may be
individual differences in reliance on social
information.
Latency for one demonstrator to recover (sec)
0 50 100 150 200La
tenc
y fo
r foc
al in
divi
dual
to
reco
ver (
sec)
0
100
200
300
400
Latency for three demonstrators to recover (sec)
0 100 200 300 400
R = 0.22, p = 0.419 R = 0.44, p = 0.088
(a) (b)
Fig. 3: Relationship between the latency for
the focal individual to recover and the latency
of one demonstrator to recover (a) and all
three demonstrators to recover (b). R-values
represent the Spearman rank correlation coef-
ficient.
Ethology 119 (2013) 1–7 © 2013 Blackwell Verlag GmbH 5
K. E. Hogan & K. L. Laskowski Indirect Information Transfer Through Behavioral Alarm Cues
In conclusion, our study demonstrates that visual
behavioral cues of demonstrators are sufficient to
induce an antipredator response in individual three-
spined sticklebacks and that individuals consistently
differ in this response. Our findings demonstrate that
visual cues represent a potentially rapid method of
information transfer and can influence an individual’s
behavior even in the absence of their own private
information.
Acknowledgements
We would like to thank Katie McGhee, Laura
Stein, Simon Pearish, members of the Bell lab, and
two anonymous reviewers for their thoughtful
comments on the manuscript. We also thank Ali-
son Bell for her continuing guidance and use of
her lab at the University of Illinois Urbana-Cham-
paign.
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K. E. Hogan & K. L. Laskowski Indirect Information Transfer Through Behavioral Alarm Cues