Indirect Information Transfer: Three-Spined Sticklebacks Use Visual Alarm Cues From Frightened...

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: kate.laskowski@gmail.com

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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