Do dogs (Canis lupus familiaris) make counterproductive choices because they are sensitive to human ostensive cues?

Abstract

Dogs appear to be sensitive to human ostensive communicative cues in a variety of situations, however there is still a measure of controversy as to the way in which these cues influence human-dog interactions. There is evidence for instance that dogs can be led into making evaluation errors in a quantity discrimination task, for example losing their preference for a larger food quantity if a human shows a preference for a smaller one, yet there is, so far, no explanation for this phenomenon. Using a modified version of this task, in the current study we investigated whether non-social, social or communicative cues (alone or in combination) cause dogs to go against their preference for the larger food quantity. Results show that dogs' evaluation errors are indeed caused by a social bias, but, somewhat contrary to previous studies, they highlight the potent effect of stimulus enhancement (handling the target) in influencing the dogs' response. A mild influence on the dog's behaviour was found only when different ostensive cues (and no handling of the target) were used in combination, suggesting their cumulative effect. The discussion addresses possible motives for discrepancies with previous studies suggesting that both the intentionality and the directionality of the action may be important in causing dogs' social biases.

Full text

Page 1

Do Dogs (Canis lupus familiaris) Make Counterproductive
Choices Because They Are Sensitive to Human Ostensive
Cues?
Sarah Marshall-Pescini1*, Chiara Passalacqua1, Maria Elena Miletto Petrazzini1, Paola Valsecchi2,
Emanuela Prato-Previde1
1Psychology, Department of Biomedical Sciences and Technologies, University of Milan, Milan, Italy, 2Department of Evolutionary and Functional Biology, University of
Parma, Parma, Italy
Abstract
Dogs appear to be sensitive to human ostensive communicative cues in a variety of situations, however there is still a
measure of controversy as to the way in which these cues influence human-dog interactions. There is evidence for instance
that dogs can be led into making evaluation errors in a quantity discrimination task, for example losing their preference for
a larger food quantity if a human shows a preference for a smaller one, yet there is, so far, no explanation for this
phenomenon. Using a modified version of this task, in the current study we investigated whether non-social, social or
communicative cues (alone or in combination) cause dogs to go against their preference for the larger food quantity.
Results show that dogs’ evaluation errors are indeed caused by a social bias, but, somewhat contrary to previous studies,
they highlight the potent effect of stimulus enhancement (handling the target) in influencing the dogs’ response. A mild
influence on the dog’s behaviour was found only when different ostensive cues (and no handling of the target) were used in
combination, suggesting their cumulative effect. The discussion addresses possible motives for discrepancies with previous
studies suggesting that both the intentionality and the directionality of the action may be important in causing dogs’ social
biases.
Citation: Marshall-Pescini S, Passalacqua C, Miletto Petrazzini ME, Valsecchi P, Prato-Previde E (2012) Do Dogs (Canis lupus familiaris) Make Counterproductive
Choices Because They Are Sensitive to Human Ostensive Cues? PLoS ONE 7(4): e35437. doi:10.1371/journal.pone.0035437
Editor: Attila Szolnoki, Hungarian Academy of Sciences, Hungary
Received July 13, 2011; Accepted March 16, 2012; Published April 25, 2012
Copyright: ? 2012 Marshall-Pescini et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was supported by a doctoral and post-doctoral grant from Milan University to Chiara Passalacqua and Sarah Marshall-Pescini. The funders
had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: sarah.marshall@unimi.it
Introduction
Recent research in the infant literature has shown the power of
specific ‘ostensive signals’ i.e. cues such as direct gazing, motherese
and use of the child’s name and body orientation in assisting social
learning ([1–3] and [4] for a recent review). The demonstrator’s
ostensive cues and/or actions perceived as ‘intentional’ have also
been shown to lead to inefficient choices in young children. For
example children ‘over-imitate’, i.e. copy redundant actions [2–6]
and carry out ‘obvious’ errors in their decision making process [7],
when ostensive cues are being used, showing that reliance on social
information may not always be the most adaptive strategy [8,9].
It has been proposed that dogs, potentially uniquely amongst
non-human species, also respond to human ostensive cues in
similar contexts and support has been gathering from various
studies. For example, dogs were shown to be faster at socially
learning a detour task when the demonstrator talked and looked at
them during the demonstration [10]; furthermore, ostensive cues
are thought to have played a role in dogs’ selective imitation of a
conspecific’s action ([11] but see [12] for an alternative
explanation of the imitative effect). However, more recent studies
have been less consistent, with one study showing no preferential
imitation of bodily actions in a communicative context [13] and
another finding a hindering effect of communicative signals in the
social acquisition of an object manipulation task [14].
Like in children, also in dogs there is some indication of various
kinds of evaluation errors caused by a greater reliance on socially
acquired rather than individually available information. In one
study [15] dogs were found to rely more on a human pointing
gesture than on their own olfactory abilities when attempting to
obtain hidden food, whereas another study found that dogs would
select a visibly non-baited container more after a communicative
than a non-communicative demonstration by the experimenter, if
the experimenter then stayed in the dog’s presence [16]. Finally,
dogs that preferentially choose the larger of two food quantities
when alone, can be induced to lose that preference when their
owner (or a stranger [17]) vocally and behaviourally shows an
interest for the smaller food quantity [18]. In the latter studies the
owner and stranger used ostensive cues, such as gaze-alternation
and a high pitched voice, to express their interest for the smaller
food quantity, suggesting that these behaviours may have been
responsible for the dogs’ evaluation errors.
Ostensive cues have also been used in the classic A-not-B
paradigm, where infants and dogs have to choose between two
locations after observing the demonstrator hiding a toy behind one
of them. Dogs, like infants, have been shown to be sensitive to the
use of ostensive signals (voice, gaze alternation and movement), in
PLoS ONE | www.plosone.org1April 2012 | Volume 7 | Issue 4 | e35437

Page 2

that more perseverative errors were carried out when such signals
were observed (social-communicative trials) than when they were
not (non-communicative trials) [19]. However, this point is still a
matter of debate since in this particular study it was difficult to
disentangle the effects of enhancing a stimulus through non-social
(e.g. movement/sound of the target alone) vs. social (presence of a
person) vs. communicative (the person manifests specific cues)
means [20,21]. Furthermore, a combination of communicative
cues (calling the dogs’ name and looking at it whilst holding up the
ball) were presented against a single non-social cue (holding the
ball and making it squeak), hence it was not possible to disentangle
whether it was the communicative nature of the stimuli or the
intensity of the combined behaviours which attracted the dogs’
attention more and hence affected their subsequent choice.
In a number of previous studies, it appeared difficult to tease
apart the influence of communicative cues and other social
mechanisms such as stimulus and local enhancement. Stimulus
enhancement occurs when an animal directs its behaviour towards
an object [22,23], while local enhancement occurs when an animal
directs its behaviours towards the place in which it witnessed
another individual act [24,25]. Together these mechanisms can be
considered simple forms of social enhancement, which have been
shown to be widespread and potentially very powerful in many
animal species [25,26].
Hence in the current study we used the experimental paradigm
adopted in Prato-Previde et al. [18] to: 1. ascertain whether the
evaluation error (i.e. loss of preference for the larger food quantity
when the experimenter shows interest in the smaller one) observed
in previous studies was due to social enhancement, 2. whether it
would be elicited only with the presentation of ostensive
communicative cues and 3. if so which communicative cues alone
or in combination would influence dogs more strongly.
Inthecurrentparadigmanumberofelementswereconsideredto
potentially play an important role in influencing the dogs’
behaviour, i.e. the presence/absence of a model approaching the
target;thehand-to-mouthactionwithorwithouthand-foodcontact;
the use of voice and gaze alternation; and the combination of
elementsoutlined above.Accordingly, dogswereallocatedtooneof
nine groups differing in the presence/absence of specific social and
communicative cues: 1. Independent choice- dogs were presented
with a discrimination task between large and small quantity of food
with no human intervention; this group formed the baseline against
which all other groups could be compared; 2. Non-social
enhancement- the target stimulus was enhanced in a non-social
manner (by lifting remotely); 3. Local enhancement- the (human)
model approached the target stimulus; 4. Stimulus enhancement-
the model approached and picked the target stimulus up bringing it
to the mouth (hand-food contact); 5. Ostensive enhancement- the
model approached the target picking the food up, gaze alternating
and talking to the dog; 6. Voice- the model approached the target
and talked with a high-pitched tone of voice without looking at the
dog; 7. Gaze alternation- the model approached the target and
alternatedhergazebetweenitandthedog;8.Voice+Gaze-asabove
combiningbothcommunicativecues;9.Hand-to-mouth-themodel
approached the target moved the hand from target to mouth but
without making contact with the food.
Prato-Previde et al.’s experimental paradigm is particularly well
suited for testing the relative weight of social vs. ostensive cues
because in the crucial condition it places dogs in a visibly
conflicting situation, where a valuable resource (the large food
quantity) is placed in direct opposition with the social/communi-
cative behaviours exhibited by the person choosing the less
valuable resource (small food quantity).
If dogs are not affected by the cues presented to them, we expect
either an improvement (due to learning/practice) or no change in
the preference for the larger food quantity from the trials in which
dogs choose independently (no influence condition) to trials with a
demonstration (counterproductive influence condition), whereas, if
the cues presented influence the dogs’ choices we expect a drop in
the preference for the larger food quantity, as observed in previous
studies [17,18]. Thus, following the person comes at a cost. The
more powerful the cues exhibited the more willing the dogs should
be to ignore their own independent source of information and go
with the social information instead.
If, as has been suggested, ostensive cues are particularly salient
for domestic dogs, then we would expect dogs in the communi-
cative cues groups (Voice, Gaze, Voice+Gaze and Ostensive
enhancement) to lose their preference for the larger food quantity
in the crucial counterproductive condition more than dogs in our
independent choice group. If however the evaluation error shown
by dogs is due to a simpler social enhancement effect then we
would expect dogs in the stimulus enhancement and local
enhancement group to also show a loss of preference compared
to the independent choice group. Finally, if the effect is not linked
to social factors at all, but any kind of attention-getting cues (e.g.
the food swinging and falling on the plate with an audible plop) are
enough to confuse dogs and make them loose their preference for
the large food quantity, then we would expect a loss of preference
for the large food quantity also in the non-social enhancement
group.
Methods
Ethics Statement
No special permission for use of animals (dogs) in such socio-
cognitivestudiesisrequiredinItaly.Therelevantethicalcommittee
is the Ethical Committee of the Universita ` degli Studi di Milano.
Subjects
149 dog-owner dyads were recruited through personal contacts,
advertisements in parks and veterinary surgeons. The dog sample
consisted of 60 males and 89 females whose ages ranged from 1 to
10 years (mean=4.4 years, SD=3.3). One hundred and two dogs
were pure-breed (see Text S1) and 47 mixed-breed. All the dogs
were kept for companionship, lived within the human household
and had either no or only basic training experience. A number of
dogs had participated in other studies by our group but not in
studies using the experimental paradigm adopted here. Dogs were
semi-randomly allocated to one of nine groups, counterbalancing
as much as possible for age, sex and participation in other studies.
Procedure
All testing took place in a relatively bare testing room at the
‘Canis sapiens’ laboratory of the University of Milan. The behaviour
of the dog and its owner during testing was video-recorded using a
wide-angle video camera positioned on a tripod located in one
corner of the testing area (Figure 1).
Prior to testing the owner was asked to enter with his/her dog
into the testing room and the dog was allowed to freely explore the
environment whilst the experimenter described the procedure to
the owner. In order to be sure that the dogs would be sufficiently
motivated to perform the food choice task the owners were asked
not to feed their dogs at least four hours prior to testing. In
addition, the palatability of the food used was always evaluated by
offering the dog a few pieces prior to testing.
The food was presented in two plastic dishes (22 cm in
diameter62 cm). Two different quantities of food were used:
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org2April 2012 | Volume 7 | Issue 4 | e35437

Page 3

small, consisting of a single piece of food, and large, consisting of
six pieces of food evenly spread out on the plate.
The procedure consisted of three conditions: Condition 1-
Neutral influence: the choice between the two equally small
quantities (one piece of food in each plate) with the demonstrator
showing an interest for either one or the other; Condition 2- No
influence: dogs can choose between the large and small food
quantity with no person influence (this condition was identical for
all groups); and Condition 3- Counterproductive influence:
the choice between the large and small food quantity with the
demonstrator showing an interest for the small one.
Dogs received a total of 18 trials, i.e. six trials in each condition.
The position of the large and small food quantity was counterbal-
anced both in Condition 2 and Condition 3. To avoid the
development of a side preference the same food quantity was never
placedinthesamelocationmorethantwiceinarow.InCondition1
the position of the demonstrator was counterbalanced in the same
manner. In all conditions the dogs were on a leash held by their
seated owners1.5 mfromtheaxisonwhichtheplateswereset.The
plates were set 1 m apart equally distant from the dog (Figure 1).
In most conditions (apart from the non-social enhancement
group- see below) the experimenter started the procedure by
taking two steps towards the dog, crouching and simultaneously
placing the plates on the ground in their specified positions. After
exhibiting the communicative signals appropriate to the group
condition (see below) the experimenter took two steps back
reaching a central position between the plates and with her back
turned to the dog. Once in position the experimenter told the
owner to drop the leash, allowing the dog to make its choice. After
the dog had chosen one of the two plates, the other was quickly
removed by the experimenter.
Dogs were allocated to one of the following groups (see Movie
S1 for demonstrations of procedures for each group):
Group1-Independentchoice(learning).
plates on the ground the experimenter took up the neutral back-
turned position between the two plates. Thus, dogs were presented
with the large and small quantity with no interference from the
experimenter, for a total of 12 trials. This group allows us to assess
whetherwithnointerferencefrompresentedcues,dogswillshowan
improvementornochangeintheirchoiceofthelargerfoodquantity
between the first six vs. latter six trials.
Group 2- Non-social enhancement (no person visible).
person hidden behind a 126678 cm screen manipulated the
presentation of the plates (sliding them simultaneously in front of
the dog from behind the panel) and the enhancement of the target
piece of food which was lifted and then dropped with an audible
‘plop’ on the plate by using a ‘fishing rod’. Thus throughout this
condition dogs never saw the person although the timing of the
presentation was the same as for other groups.
Group 3- Local enhancement (approach only).
placed the plates on the ground the experimenter stood up, took a
steptowardsoneoftheplates,andcroucheddownlookingintentlyat
the food for 5 seconds. She then stood up again and took up the
neutral back-turned position between the two plates.
Group 4- Stimulus enhancement (approach+ +hand-food
contact).
Having placed the plates on the ground the
experimenter stood up, took a step towards one of the plates, and
croucheddown.Whilstlookingattheplate,theexperimenterpicked
up the food bringing it level to the mouth and holding it there for
5 seconds. She then placed the food back down, stood and took up
the neutral back-turned position between the two plates.
Group 5- Ostensive enhancement (approach+ +hand-food
contact+ +voice+ +gaze-alternation).
thegroundtheexperimenterstoodup,tookasteptowardsoneofthe
plates,andcroucheddownagain,pickedupthefoodbringingitlevel
to her mouth and looking intently first at the food then at the dog
then at the food again, said with a friendly tone of voice ‘‘Oh wow,
thisisgood,thisissogood!’’(forthetotaldurationof5 seconds).She
thenstoodandtookuptheneutralback-turnedpositionbetweenthe
two plates.
Group 6- Voice (approach+ +voice).
onthegroundtheexperimenterstoodup,tookasteptowardsoneof
the plates, and crouched down looking intently at the food for
5 seconds whilst saying in a friendly tone of voice ‘‘Oh wow, this is
good,this issogood!’’.Shethenstood andtookuptheneutral back-
turned position between the two plates.
Group 7-Gaze alternation
alternation).
Having placed the plates on the ground the
experimenter stood up, took a step towards one of the plates, and
croucheddownlookingintentlyfirstatthefoodthenatthedogthen
at the food again, for the duration of 5 seconds. She then stood and
took up the neutral back-turned position between the two plates.
Group 8- Voice+ +Gaze alternation (approach+ +voice+ +gaze-
alternation).
Having placed the plates on the ground the
experimenter stood up, took a step towards one of the plates, and
croucheddownlookingintentlyfirstatthefoodthenatthedogthen
at the food again whilst saying in a friendly tone of voice ‘‘Oh wow,
this is good, this is so good!’’ (total duration being 5 seconds). She
thenstoodandtookuptheneutralback-turnedpositionbetweenthe
two plates.
Group9-Hand-to-mouth
movement).
Having placed the plates on the ground the
experimenter stood up, took a step towards one of the plates, and
crouched down again looking intently at the food for 5 seconds
whilst heropen and visibly empty hand moved from the plate to her
Havingplacedthe
A
Having
Having placed the plates on
Having placed the plates
(approach+ +gaze-
(approach+ +hand-to-mouth
Figure 1. Schematic depiction of the experimental setup.
doi:10.1371/journal.pone.0035437.g001
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org3April 2012 | Volume 7 | Issue 4 | e35437

Page 4

mouth.Shethenstoodandtookuptheneutralback-turnedposition
between the two plates.
Data analysis
The dogs’ choices were scored from video. Only dogs that were
placed in a central position between the plates and had looked at
both plates before being released were included in the analysis. We
recorded the number of times a dog chose the large food quantity
in Condition 2 and 3 and the number of times it followed the
demonstrator’s indication in Condition 1 (i.e., dogs scored 0 to 6 in
each condition).
Furthermore, the dog’s gazing behaviour whilst being held by
the owner and prior to making a choice was coded using the
Solomon (beta 091110, Copyright 2006–2008 by Andra ´s Pe ´ter)
program. In Condition 1 and 3, whilst the experimenter was
expressing her choice of plates we recorded the time spent by the
dog looking at 1. the plate chosen by the experimenter, 2. the
other (non-chosen) plate and 3. elsewhere. The dog’s looking time
was recorded from the moment the person placed the plates on the
ground, to the moment the dog was released. A looking index was
computed with (time spent looking at the target plate)/(time spent
looking at the target plate+the other plate)*100, over the 6 trials in
each condition.
For both the gazing behaviour and the dogs choice 20% of the
data was coded by a second observer. Reliability for choice was
100%; reliability for the duration of gazing were all above a=0.76
(Cronbach’s alpha).
To assess whether dogs in each group showed a preference for
the larger food quantity in the no influence condition (Condition 2)
a One-sample Wilcoxon test was used. A Generalized Linear
model (Poisson distribution) was run to compare groups in
Condition 1 (Neutral influence), with number of times the dogs
followed the person as the dependent variable and group as the
factor. Furthermore, a Generalized Estimating Equation and post-
hoc pairwise comparisons with Bonferroni correction were used to
assess the between and within group differences in the dogs’
preference for the larger quantity in Condition 2 (No influence)
and Condition 3 (Counterproductive influence). The dependent
variable was the number of times dogs chose the larger food
quantity; the ‘independent choice’ group was set as the control
group; factors were group and condition and both main effects and
interactions were calculated.
Finally, a Generalized Estimating Equation (with Linear
distribution) and post-hoc comparisons with Bonferroni correction
were also used to assess the between and within group differences
in the dog’s looking time to the target/person’s plate in the neutral
influence (Condition 1) and counterproductive influence (Condi-
tion 3). The dependent variable was the looking time index, the
factors were group and condition and both main effects and
interactions were calculated.
Statistical tests were two-tailed, the a value was set at 0.05 and
the statistical package SPSS version 19 was used.
Results
Twelve of the 149 dogs tested were removed from analysis
either because over the 18 trials they revealed a 100% side bias or
because they did not complete all 18 trials. All dogs looked at both
plates prior to choice. This resulted in the following group
composition: Group 1- Independent choice: 14 dogs (7 F, 7 M);
Group 2- Non-social enhancement: 15 dogs (10 F, 5 M); Group 3-
Local enhancement: 15 dogs (9 F, 6 M); Group 4- Stimulus
enhancement 14 dogs (9 F, 5 M); Group 5- Ostensive enhance-
ment: 15 dogs (9 F, 6 M); Group 6- Voice: 17 dogs (11 F, 6 M);
Group 7- Gaze alternation: 17 dogs (9 F, 8 M); Group 8-
Voice+Gaze alternation: 15 dogs (8 F, 7 M); Group 9- Empty
hand-pick: 15 dogs (11 F, 4 M). Looking time was analysed only
for dogs who had witnessed a demonstration (thus excluding the
independent choice group): however, due to video malfunction
only 116 of the 123 dogs could be analysed for looking time, thus
results are based on this data.
Figure 2. Dogs’ choice of the large food quantity. Mean choice (and SEM) of the large food quantity in the no influence and counterproductive
influence condition for each group (significant differences are shown for within group comparison *P,0.01). In the counterproductive influence
condition dogs in the Ostensive enhancement and Stimulus enhancement group chose the larger quantity significantly less than dogs in the
Independent choice group.
doi:10.1371/journal.pone.0035437.g002
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org4April 2012 | Volume 7 | Issue 4 | e35437

Page 5

Overall, in Condition 2 (no influence) 100 (73%) dogs chose the
larger food quantity more often (i.e. on either four or more trials
out of the total six); 31 (23%) dogs chose at random (i.e. chose the
larger food quantity on three out of six trials), 6 (4%) dogs chose
the larger food quantity twice or less. Thus overall, dogs
significantly preferred choosing the larger food quantity (One-
sample Wilcoxon: Group 1: z=2.63, p=0.02; Group 2: z=3.43,
p,0.001; Group 3: z=2.97, p=0.001; Group 4: z=2.62,
p=0.02; Group 5: z=2.38, p,0.01; Group 6: z=3.64,
p,0.001; Group 7: z=3.63, p,0.001; Group 8: z=3.45,
p,0.001; Group 9: z=3.43, p,0.001).
Nodifferences betweengroupsemergedinthedogs’choiceofthe
target plate in Condition 1 (Neutral influence) (Wald=7.75; df=7,
p=0.35).However,thegeneralizedestimatingequation comparing
allgroupsinCondition2vs.Condition3,withthechoiceofthelarge
food quantity as dependent variable, revealed main effects for both
group (Wald=37.8, df=8, p,0.001) and condition (Wald=3.8,
df=1,p=0.051)aswellasasignificant interactionbetweenthe two
(Wald=84.8, df=8, p,0.001), with the Ostensive, Stimulus
enhancement and Voice+Gaze group, showing a significantly
different performance from the baseline independent choice group
in Condition 3 (Ostensive p,0.001; Stimulus p,0.001; Voice+-
Gaze p=0.01) but not in Condition 2 (Ostensive p=0.99; Stimulus
p=0.47; Voice+Gaze p=0.65) (Figure 2).
Post-hoc analyses were also carried out to assess the change in
preference for the large food quantity between Condition 2 (No
influence) and Condition 3 (Counterproductive influence) in each
group. A significant difference emerged in the Independent choice
(p=0.007), Local enhancement (p=0.003), Stimulus enhancement
(p=0.009)andOstensivecues(p=0.001)groupwithdogsinthefirst
two groups showing an improvement in performance from
Condition 2 to Condition 3, and dogs in the latter two groups
showing a drop in their preference for the larger food quantity
(Figure 2).
As regards looking time, a main effect of both group
(Wald=113.96, df=7, p,0.001) and condition (Wald=78.22,
df=7, p,0.001) emerged as well as an interaction between the
two factors (Wald=17.66, df=7, p=0.01). Post-hoc analyses
showed that dogs looked at the person/target plate more in the
Neutral than in the Counterproductive condition in the Non-social
enhancement (p=0.04), Local enhancement (p=0.003), Voice
(p=0.001) and Hand-to-mouth group (p=0.02), whereas no such
difference emerged in the Stimulus enhancement (p=0.14),
Ostensive enhancement (p=1), Gaze (p=1) and Voice+Gaze
(p=1) group. Furthermore, in Condition 1 dogs in the Ostensive,
Stimulus enhancement and Hand-to mouth group looked at the
person/target plate more than dogs in most other groups (Table 1
and Figure 3). In the Counterproductive condition however, dogs
in the Ostensive group continued to look at the person as much as
dogs in the Stimulus enhancement and Hand-to-mouth group, but
whereas dogs in the Ostensive group differed from all other
groups, dogs in the Stimulus and Hand-to-mouth group continued
to look more at the person than dogs only in the Non-social and
Local enhancement groups (Table 2 and Figure 3).
Discussion
There is currently some debate as to the extent of dog’s
sensitivity to ostensive cues, the mechanisms behind this
phenomenon and its function in the dog-human relationship. At
present it is not clear whether ostensive cues influence the dogs’
learning process above and beyond simply attracting the dog’s
attention more to the demonstrated actions, in fact in a recent
study, dogs were shown to learn a detour task as efficiently from a
partial demonstration from an inanimate object than from a
human demonstrating the action whilst calling the dog [27].
In the current study, by placing dogs in a conflict situation we
were able to assess the relative weight of each communicative cue
both in attracting the dog’s attention (looking time) during the
demonstration, and in influencing the dog’s choice behaviour. The
results from the looking time data show that even in the condition
where a conflict between larger food quantity and demonstration
exists (Counterproductive influence) dogs in all groups looked at
the demonstrator for more than 57% of the trial time (with the
remaining time spent looking at the other plate). However,
differences between demonstrations emerged clearly: the most
powerful attention-getting behaviours were not the communicative
cues (neither alone nor combined), but rather the Hand-to-mouth
action with our without food-contact. Yet, although dogs in the
Hand-to-mouth group looked at the demonstration to the same
extent as dogs in the Stimulus and Ostensive enhancement group,
their choices were not affected in the same way since dogs in the
hand-to-mouth group did not go against their preference for the
larger food quantity. Interestingly, this shows that although human
cues can strongly influence both aspects of the dogs’ behaviour
they may not necessarily do so in parallel.
In terms of the dogs’ choices in the current study we investigated
whether dogs would choose against their preference in a food
quantity discrimination task according to the type of non-social,
social and communicative cues presented.
With no interference from the demonstrator (i.e. No influence
condition) dogs in all groups showed an overall preference for the
larger food quantity and dogs that were allowed to continue
choosing with no interference for 12 trials (Independent choice
group) showed an improvement across the first and last six trials.
Thus dogs, overall, prefer the larger food quantity and with
practice become better at discriminating between the two.
Given that dogs in the absence of interference prefer a larger
food quantity the central question is under which conditions they
would choose against their preference. The same pattern of
improvement in quantity discrimination found in the Independent
choice group was replicated also in the Local enhancement group,
thus dogs who witnessed a person approaching and squatting
down next to the plate but showing no communicative cues and no
handling of the food, were able to improve their choice of the
larger food quantity across trials. Contrary to this pattern, dogs in
the Stimulus enhancement and Ostensive enhancement groups
(presented with the demonstrator either handling the food or both
handling the food and looking and talking to them) started
choosing against their preference more often giving up the larger
food quantity to follow the model’s choice of the smaller one. Dogs
in the other groups (Non-social enhancement, Voice, Gaze, Hand-
to-mouth, Voice+Gaze) showed neither a significant improvement
nor a significant drop in performance.
Predictably (given results from the within group comparisons),
when compared to the Independent choice group dogs in the
Stimulus and Ostensive group showed a significantly lower
preference for the larger food quantity in the counterproductive
influence condition, however the same pattern of results emerged
also for the Voice+Gaze group, suggesting that dogs in this group
are also, to a certain extent, affected by the demonstration.
Given dogs did not go against their preference if they saw food
being lifted and falling with no human intervention (the Non-social
enhancement group) we can conclude that the evaluation error
observed in the current study was caused by a social bias, which
could be induced either by a highly salient social cue such as
handling the food (Stimulus enhancement group) or, to a lesser
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org5April 2012 | Volume 7 | Issue 4 | e35437

Page 6

extent, by using a combination of communicative cues such as
talking inafriendlyvoiceand gazealternation(Voice+Gazegroup).
Current results highlight the potent effect of stimulus enhance-
ment (in this case handling the food) as a social influencing/
learning mechanism and are somewhat at odds with other
published work where stimulus enhancement unaccompanied by
communicative cues did not
[16,19,21]. It is perhaps interesting to note however, that in both
the Topal et al. studies [19,21] and the Kupan et al. study [16]
toys were used as the target object, whereas in our own study food
was the source of interest. The discrepancy in results may thus be
linked to the use of these different stimuli. It may be that dogs
considered picking up the food (with no other signal) as a
communicative cue directed at them (showing them ‘their’ food),
but did not view manipulation of an object (with no other cue) as
influence the dogs’choices
an invitation to interact with it. Dogs may be used to seeing us
manipulate objects that are of no concern to them, but
manipulating food from the ground may be more easily considered
an explicit invitation even with no further communicative cue
present. This may be supported by the fact that when the
demonstrator did not pick the food up (thus only local
enhancement was used) dogs were able to totally ignore the
experimenter’s behaviour.
Another possibility is that the perception of the other’s action as
intentional may be in some cases sufficient to produce a social bias
even when no communicative cue indicates to whom the action is
directed to. Infants of a very young age have been shown to
perceive grasping an object as an intentional action [28,29] and
evidence from mirror neuron studies in macaques also suggest that
grasping is perceived as goal-directed [30]. Furthermore, a recent
Figure 3. Looking index. Mean (and SEM) durations (in percentage) of looking to the target/experimenter plate in the neutral choice and
counterproductive influence condition for each group (significant differences are shown for within group comparison *P,0.05, **P,0.01; see Tables 1
and 2 for between group results).
doi:10.1371/journal.pone.0035437.g003
Table 1. Looking at the target/person plate in the Neutral condition (Condition 1) for dogs in each group.
non-soc enhlocal enh stim enh ost enh voicegazevoice+ +gaze
hand-to-
mouth
mean in %69.5974.7488.3187.3175.9577.6679.3788.76
non-soc enh1
,0.001
,0.00110.9641
,0.001
local enh10.0010.0071110.001
stimulus enh
,0.0010.00110.0030.03 0.21
ostensive enh
,0.0010.00710.03 0.2 0.91
voice11 0.0030.03110.004
gaze11 0.031110.03
voice+ +gaze0.111 0.2 0.9211 0.2
hand-to-mouth
,0.001 0.001110.0040.030.2
Results (p-values) of the between group post-hoc comparisons (with Bonferroni corrections).
doi:10.1371/journal.pone.0035437.t001
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org6April 2012 | Volume 7 | Issue 4 | e35437

Page 7

study showed that children’s ‘over-imitation’ (copying obviously
useless actions) is linked to the perceived intentionality of the
demonstrator’s actions [6]. In our study the same hand movement
(hand-to-mouth) with or without the grasping of the target,
produced similar levels of looking/attention but very different
effects on the dogs’ behaviour. Only in the latter case did dogs go
against their preference. It is thus possible that whereas both
demonstrations attracted the dogs’ attention only the grasping
motion was perceived as intentional and that this may play a role
in causing the observed social bias. This would be in line with
results showing that the intentionality of a pointing gesture can be
discerned and may be sufficient to affect dogs’ choices in a classic
two-choice task [31].
Thus, what seems to emerge from previous studies and our own
is that the dog’s social bias may be influenced by a combination of
the perception of the intentionality behind the action and the
communicative framework within which it is placed. In line with
other studies [31] we found that the latter appears to be perceived
the strongest when communicative cues are used in combination
(voice+gaze) rather than singularly, most probably since this
reflects the naturalistic interactions between dogs and humans. A
further element, which may be important in the emergence of a
social bias is the dog’s motivation to interact with the stimuli (i.e.
the potential differences of food vs. toys). Future studies will need
to consider these aspects separately to tease apart the relative
importance of each.
Finally, current results have interesting implication for the
hypothesis that social learning may in some cases be maladaptive.
A recent review [9] highlighted the need for studies which would
address the potential occurrence of ‘‘informational cascades’’,
where suboptimal methods may spread rapidly across a population
because social information comes to outweigh personal experi-
ence, however very few studies have explored under what
conditions an animal will choose to rely on private vs. social
information [8,9,32–36]. The current study adds to a small but
growing literature showing that social learning is not necessarily
always the best strategy [34–39] and provides an experimental
paradigm which may potentially be used to explore when an
animal will rely on private vs. social information.
Supporting Information
Movie S1
dogs in each group.
(WMV)
Videos of the demonstrations witnessed by
Text S1
(DOC)
Breeds of participating dogs.
Acknowledgments
We would like to thank all the owners and dogs that participated as
volunteers, Isabella Merola for invaluable aid in data collection, Stefano
Leonardi from Parma University and Nicola Ferrari from Milan University
for help with statistical analyses, and two anonymous referees for insightful
suggestions on a previous version of this manuscript.
Author Contributions
Conceived and designed the experiments: SMP PV EPP. Performed the
experiments: SMP CP MEMP. Analyzed the data: SMP CP MEMP.
Wrote the paper: SMP PV EPP.
References
1. Southgate V, Chevallier C, Csibra G (2009) Sensitivity to communicative
relevance tells young children what to imitate. Dev Sci 12: 1013–1019.
Brugger A, Lariviere LA, Mumme DL, Bushnell EW (2007) Doing the right
thing: Infants’ selection of actions to imitate from observed event sequences.
Child Dev 78: 806–824.
Nielsen M (2006) Copying Actions and Copying Outcomes: Social Learning
Through the Second Year. Dev Psychol 42: 555–565.
Csibra G, Gergely G (2011) Natural pedagogy as evolutionary adaptation.
Philos T Roy Soc B 366: 1149–1157.
Lyons DE, Young AG, Keil FC (2007) The hidden structure of overimitation.
PNAS 104(19): 1158–1167.
Lyons DE, Damrosch DH, Lin JK, Macris DM, Keil FC (2011) The scope and
limits of overimitation in the transmission of artifact culture. Philos T Roy Soc B
366: 1158–1167.
2.
3.
4.
5.
6.
7. Topal J, Gergely G, Miklo ´si A´, Erdohegyi A, Csibra G (2008) Infants’
perseverative search errors are induced by pragmatic misinterpretation. Science
321: 1831–1834.
Laland KN (2004) Social learning strategies. Learn Behav 32: 4–14.
Rieucau G, Giraldeau LA (2011) Exploring the costs and benefits of social
information use: an appraisal of current experimental evidence. Philos T Roy
Soc B 366: 949–957.
10. Pongra ´cz P, Miklo ´si A´, Timar-Geng K, Csa ´nyi V (2004) Verbal attention getting
as a key factor in social learning between dog (Canis familiaris) and human.
J Comp Psych 118: 375–383.
11. Range F, Vira ´nyi Z, Huber L (2007) Selective imitation in domestic dogs. Curr
Biol 17: 868–872.
12. Kaminski J, Nitzschner M, Wobber V, Tennie C, Bra ¨uer J, et al. (2011) Do dogs
distinguish rational from irrational acts? Anim Behav 81: 195–203.
8.
9.
Table 2. Looking at the target/person plate in the Counterproductive condition (Condition 3) for dogs in each group.
non-soc enhlocal enhstim enh ost enhvoicegaze voice+ +gazehand-to-mouth
mean in %57.4660.55 79.53 85.1665.0168.07 72.73 80.59
non-soc enh1
,0.001
,0.00111 0.1
,0.001
local enh10.006
,0.0011110.002
stimulus enh
,0.0010.00610.27111
ostensive enh
,0.001
,0.0011
,0.0010.010.041
voice110.27
,0.00111 0.1
gaze1110.01111
voice+ +gaze 0.1110.04111
hand-to-mouth
,0.0010.00211 0.111
Results (p-values) of the between group post-hoc comparisons (with Bonferroni corrections).
doi:10.1371/journal.pone.0035437.t002
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org7April 2012 | Volume 7 | Issue 4 | e35437

Page 8

13. Tennie C, Glabsch E, Tempelmann S, Brauer J, Kaminski J, et al. (2009) Dogs,
Canis familiaris, fail to copy intransitive actions in third-party contextual imitation
tasks. Anim Behav 77: 1491–1499.
14. Range F, Heucke SL, Gruber C, Konz A, Huber L, et al. (2009) The effect of
ostensive cues on dogs’ performance in a manipulative social learning task. Appl
Anim Behav Sci 120: 170–178.
15. Szetei V, Miklo ´si A´, Topa ´l J, Csa ´nyi V (2003) When dogs seem to lose their
nose: an investigation on the use of visual and olfactory cues in communicative
context between dog and owner. Appl Anim Behav Sci 83: 141–152.
16. Kupa ´n K, Miklo ´si A´, Gergely G, Topa ´l J (2011) Why do dogs (Canis familiaris)
select the empty container in an observational learning task? Anim Cogn 14:
259–268.
17. Marshall-Pescini S, Prato-Previde E, Valsecchi P (2011) Are dogs (Canis familiaris)
misled more by their owners than by strangers in a food choice task? Anim Cogn
14: 137–142.
18. Prato-Previde E, Marshall-Pescini S, Valsecchi P (2008) Is your choice my
choice? The owners’ effect on pet dogs’ (Canis lupus familiaris) performance in a
food choice task. Anim Cogn 11: 167–174.
19. Topal J, Gergely G, Erdohegyi A, Csibra G, Miklo ´si A´(2009) Differential
Sensitivity to Human Communication in Dogs, Wolves, and Human Infants.
Science 325: 1269–1272.
20. Marshall-Pescini S, Passalacqua C, Valsecchi P, Prato-Previde E (2010)
Comment on ‘‘Differential Sensitivity to Human Communication in Dogs,
Wolves, and Human Infants’’. Science 329(5988): 142.
21. Topal J, Miklo ´si A´, Sumegi Z, Kis A (2010) Response to Comments on
‘‘Differential Sensitivity to Human Communication in Dogs, Wolves, and
Human Infants’’. Science 329(5988): 142.
22. Whiten A, Ham R (1992) On the nature and evolution of imitation in the animal
kingdom: reappraisal of a century of research. Adv Study Behav 21: 239–283.
23. Heyes CM (1994) Social-learning in animals: categories and mechanisms. Biol
Rev Camb Phil Soc 69: 207–231.
24. Galef BG, Giraldeau LA (2001) Social influences on foraging in vertebrates:
causal mechanisms and adaptive functions. Anim Behav 61: 3–15.
25. Hoppitt A, Laland K (2008) Social processes influencing learning in animals: a
review of the evidence. Adv Study Behav 38: 105–165.
26. Franz M, Matthews J (2010) Social enhancement can create adaptive, arbitrary
and maladaptive cultural traditions. Proc R Soc B 277: 3363–3372.
27. Mersmann D, Tomasello M, Call J, Kaminski J, Taborsky M (2011) Simple
mechanisms can explain social learning in domestic dogs (Canis familiaris).
Ethology 117: 1–16.
28. Woodward AL (1999) Infants’ ability to distinguish between purposeful and non-
purposeful behviours. Inf Beh Devel 17: 515–21.
29. Woodward AL (1998) Infants selectively encode the goal object of an actor’s
reach. Cognition 69: 1–34.
30. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, et al. (2005) Parietal lobe:
from action organization to intention understanding. Science 308(5722):
662–667.
31. Kaminski J, Schulz L, Tomasello M. How dogs know when communication is
intended for them. Developmental Science, (in press)DOI: 10.1111/j.1467-
7687.2011.01120.x.
32. Cladie `re N, Whiten A. Integrating the study of conformity and culture in
Humans and Non-human Animals. Psychological Bulletin, (in press).
33. Kendal RL, Coolen I, Laland K (2004) The role of conformity in foraging when
personal and social information conflict. Behav Ecol 15(2): 269–277.
34. Giraldeau LA, Valone TJ, Templeton JJ (2002) Potential disadvantages of using
socially acquired information. Philos T Roy Soc B 357: 1559–1566.
35. Laland KN, Williams K (1998) Social transmission of maladaptive information
in the guppy. Behav Ecol 9: 493–499.
36. van Bergen Y, Coolen I, Laland KN (2004) Nine-spined sticklebacks exploit the
most reliable source when private and public information conflict. P Roy Soc B
271: 957–962.
37. Price EE, Lambeth SP, Schapiro SJ, Whiten A (2009) A potent effect of
observational learning on chimpanzee tool construction. Philos T Roy Soc B
276: 3377–3383.
38. Marshall-Pescini S, Whiten A (2008) Chimpanzees (Pan troglodytes) and the
question of cumulative culture: an experimental approach. Anim Cogn 11:
449–456.
39. Hopper LM, Schapiro SJ, Lambeth SP, Brosnan SF (2011) Chimpanzees’
socially maintained food preferences indicate both conservatism and conformity.
Anim Behav 81(6): 1195–1202.
Effect of Ostensive Communication on Dogs’ Choices
PLoS ONE | www.plosone.org8April 2012 | Volume 7 | Issue 4 | e35437