Animal Behaviour xxx (2011) 1e7
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
Social eavesdropping in the domestic dog
S. Marshall-Pescini a, *, C. Passalacqua a, A. Ferrario a, P. Valsecchi b,1, E. Prato-Previde a
a
b
Sezione di Psicologia, Dipartimento di Scienze e Tecnologie Biomediche, Università di Milano
Dipartimento di Biologia Evolutiva e Funzionale, Università di Parma
a r t i c l e i n f o
Article history:
Received 21 December 2010
Initial acceptance 15 February 2011
Final acceptance 22 February 2011
Available online xxx
MS. number: 10-00880
Keywords:
Canis familiaris
cooperation
dog
eavesdropping
food sharing
social evaluation
Eavesdropping on third-party interactions has been observed in a number of species and is considered an
important source of information in decision-making processes relating to fighting and mate choice.
Human beings, however, use publicly available information flexibly in many different contexts including
assessing others’ altruistic tendencies, which may in turn inform their choice of the most appropriate
cooperative partner. We assessed whether dogs, Canis familiaris, were capable of discerning a generous
versus selfish food-sharing interaction between humans, and investigated which communicative cues
(voice versus gestures) may be more salient for them. Importantly a control condition was included to
ascertain whether it was in fact the interaction between individuals as opposed to the direct actions of
the actors that the dogs evaluated. We found that the dogs were capable of eavesdropping on human
food-sharing interactions, and vocal communication was particularly important to convey the human’s
cooperative versus noncooperative intent.
Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Social eavesdropping, that is, the use of information gathered by
observing interactions between others (Bonnie & Earley 2007;
Parejo & Aviles 2007) has been observed in a plethora of species
from primates to invertebrates (reviewed in Danchin et al. 2004;
Valone 2007). However, most studies have shown the use of
eavesdropping in specific contexts such as dominance assessment/
fighting and mate choice, leading some authors to suggest that
these abilities are domain specific and qualitatively different from
the generalized ability to evaluate others socially that is observed in
humans (Nowak & Sigmund 1998, 2005; Subiaul et al. 2008).
In humans, social evaluation based on third-party interactions
influences cooperative decisions, in that a person will more willingly cooperate with someone who is known to have been generous
to a third party (Wedekind & Milinski 2000; Milinski et al. 2002).
Furthermore, infants as young as 6e10 months prefer individuals
who help rather than hinder a third party (Hamlin et al. 2007). To a
certain extent cooperative behaviour is a trait we share with our
closest living relatives. Spontaneous cooperation and choice of the
best cooperator based on previous direct food-sharing experiences
have been shown in chimpanzees, Pan troglodytes (Melis et al.
* Correspondence: S. Marshall-Pescini, Sezione di Psicologia, Dipartimento di
Scienze e Tecnologie Biomediche, Università di Milano, Via Fratelli Cervi 93, 20090
Segrate (MI), Italy.
E-mail address: [email protected] (S. Marshall-Pescini).
1
P. Valsecchi is at the Dipartimento di Biologia Evolutiva e Funzionale, Università
di Parma, Via Usberti 11/A, Parma 43100, Italy.
2006a, b). There is also some evidence that chimpanzees may
assess an individual’s altruistic/food-sharing tendency based on
third-party interactions (Russell et al. 2008; Subiaul et al. 2008).
These results have led authors to consider the ability to evaluate
generous actions towards third parties as a key element in the
evolution of human cooperation (Nowak & Sigmund 1998, 2005).
However, a study by Bshary & Grutter (2006) showed that client
fish are more likely to invite interaction from cleaner fish that they
had witnessed being cooperative (i.e. cleaning and not feeding
selfishly) with another client fish. Thus, it seems that assessing
another individual’s generosity or fair behaviour is an ability that,
like others, will evolve if useful for survival, for example in
a cleaner/client fish mutualisitc relationship. Arguably, the ability
to assess food-sharing tendencies both directly (on past experience) and indirectly (through ‘eavesdropping’) should be important
for any social species that depends on cooperative/mutualistic
interactions, and/or where interactions with unfavourable partners
may be costly.
Dogs, Canis familiaris, in relation to humans, would seem to fit
both these criteria. They show forms of cooperation (Boitani &
Ciucci 1995; Naderi et al. 2001; Bauer & Smuts 2007; Bonanni
et al. 2010), may be averse to ‘inequity’ (Range et al. 2009), easily
follow human communicative cues (reviewed in Miklosi & Soproni
2006) and may even perform counterproductive actions to follow
a person’s indications (Prato-Previde et al. 2008; Marshall-Pescini
et al. 2010). However, dogs’ understanding of third-party interactions has been scarcely explored. Consolation (third-party-initiated
0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2011.02.029
Please cite this article in press as: Marshall-Pescini, S., et al., Social eavesdropping in the domestic dog, Animal Behaviour (2011), doi:10.1016/
j.anbehav.2011.02.029
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S. Marshall-Pescini et al. / Animal Behaviour xxx (2011) 1e7
loser-directed affiliation) has been shown in dogs (Cools et al.
2008), suggesting they are capable of recognizing the outcome
and individual roles of conspecifics in third-party conflicts, and also
in a conspecific play context (Ward et al. 2009). Furthermore,
Rooney & Bradshaw (2006) showed that dogs could assess
a potential human play partner, according to his/her behaviour
towards another dog (Rooney & Bradshaw 2006). Dogs preferentially chose the winning partner (whether human or canine) in
a tug-of-war game; however, they preferred the losing partner if
the tug-of-war was not preceded by play signals hence suggesting
a competition over resources rather than a playful interaction.
Finally, Kundey et al. (2010) looked at whether dogs could understand a third-party interaction between humans involving
competition over food. Results showed that dogs preferentially ate
food placed close to a person who had previously allowed a human
(or mechanical) recipient take it from her, as opposed to food
adjacent to a person who had removed it when the recipient
reached out for it. Thus, taken together these results suggest that
dogs, like many other species, can eavesdrop on third-party
conflicts when these involve resources, but they can also assess
a social partner in a playful context.
Similarly to the study by Kundey et al. (2010), we were also
interested in assessing the dog’s ability to eavesdrop on an interaction between humans. However, our first, specific aim was to
ascertain whether it was indeed the interaction between the actors
that dogs used to evaluate the human partners, as opposed to the
direct behaviours exhibited by the actors themselves. It has been
noted that social eavesdropping studies often lack this important
control condition (Bonnie & Earley 2007). Thus, to address this
issue, we included a ‘ghost control group’ where the actors’
behaviour was exactly the same as that exhibited in the experimental group, but, crucially, no recipient was present. The second
aim of the study was to start teasing apart what kinds of communicative cues allow dogs to understand the generous versus selfish
attitude of humans in the third-party interaction. To this aim we
reduced the visibility of the food during the interaction and rather
emphasized the communicative behaviour of the donors, who
signalled their generous/cooperative or selfish/noncooperative
intent towards the beggar using either a combination of gestural
and vocal cues (experimental group) or each element separately
(voice versus gestures groups).
METHODS
Subjects
We recruited 100 dogeowner dyads through personal contacts,
advertisements in parks and veterinary surgeons. The dog sample
consisted of 44 males and 56 females whose ages ranged from 1 to
10 years (mean 4.2 2.7 years); 68 were pure breeds and 32 mixed
breeds (see Appendix for details). Most dogs (67 individuals) had
participated during the previous year in a study involving a food
choice task (procedures similar to Prato-Previde et al. 2008). Given
the amount of time elapsed and the different nature of the test we
considered that this previous experience would not affect their
behaviour; however, to control for these differences, test-naïve and
experienced dogs were equally distributed between experimental
and control groups. This research complies with the Italian laws on
animal welfare.
Procedure
All testing took place in a relatively bare (4 3 m) test room of
the laboratory Canis Sapiens of the University of Milan. The chosen
area was unfamiliar to the dogs. The behaviour of the dog during
1.5 m
2.5 m
Figure 1. Schematic depiction of the experimental set-up. The owner and dog were
always in the same position whereas the generous and selfish donors swapped places
(unseen by the dog) prior to each new observation trial.
the whole procedure (observation and testing) was videorecorded
using a wide-angle video camera positioned on a tripod located in
one corner of the test area (see Fig. 1).
Prior to testing, the owner was asked to enter the test area, with
his/her dog, and the dog was allowed to explore the environment
freely while the experimenter briefly described the procedure to
the owner.
The procedure involved two phases: (1) observation and (2) test.
Although the observation phase varied according to group allocation, the test was identical for all groups.
Observation Phase
Experimental group: the owner was asked not to interact with
the dog during the experiment and simply remain seated, keeping
the dog on the leash between his/her legs. Two chairs were placed
equidistant and to either side of the seated owner (Fig. 1). Two
people, both unfamiliar to the dog, entered the test room holding
two identical bowls containing sausages (strong smelling and
appetizing to dogs) and (in a separate compartment) a small
quantity of cereal (which was used to feed the human beggar). They
both simultaneously approached the dog and allowed it to inspect
the interior of both bowls, thus making sure the dog had both seen
and smelled the contents. The dog, however, was not allowed to
take food from the bowls. The researchers then sat in their allocated
positions, and simultaneously started eating the cereal. A third
person (the beggar) entered the room, approached one of the
researchers, knelt down and peered inside the bowl while tapping
on her arm. The behaviour of the donor varied according to her role.
The selfish donor said ‘No’ in a firm voice while flicking her hand
out from holding the bowl thus gesturing the beggar away. The
generous donor said, ‘Have it’ in a friendly tone of voice, and placed
a small bit of cereal in the beggar’s mouth. The beggar moved from
one person to the other a total of six times, in a semirandom order,
never begging more than twice from the same person and spending
the same amount of time next to each donor. The selfish and
generous donor continued eating throughout the observation
phase taking care that they both ate the same amount of food. The
Please cite this article in press as: Marshall-Pescini, S., et al., Social eavesdropping in the domestic dog, Animal Behaviour (2011), doi:10.1016/
j.anbehav.2011.02.029
S. Marshall-Pescini et al. / Animal Behaviour xxx (2011) 1e7
bits of cereal were too small to be visible when held in the hand and
did not make a crunching sound when being eaten. The beggar then
left the room, asking the owner to release the dog as soon as the
door closed behind her.
Ghost control group: in the observation phase for dogs in the
ghost control group, no beggar was present; however, the selfish
and the generous donors pronounced the same words and carried
out the same gestures, following the same timing and order, as
that for dogs in the experimental group. Thus the selfish donor
said ‘No’ in a firm voice while flicking her hand out from holding
the bowl, while the generous donor said ‘Have it’ in a friendly tone
of voice, holding out a bit of cereal to an ‘invisible beggar’. The
generous donor then held the cereal in the palm of her hand, and
after dipping her hand in the bowl, brought the titbit to her mouth
and ate it. The ghost condition was run to discern whether, in
their response, dogs take into account the third-party interaction
or simply use an avoidance strategy, keeping a distance from the
selfish person using a word (‘No’) and tone of voice that they may
have previously associated with a negative outcome.
Gestures group: dogs in the gestures group saw the selfish
donor brusquely push the beggar away from the bowl, and
the beggar losing her balance and almost falling to the ground.
The generous donor took the food out of the bowl and placed the
cereal in the beggar’s mouth. Neither person said anything. In all
other respects the procedure was identical to the experimental
group.
Voice group: dogs in the voice group saw both the selfish and
generous donors always keep their hand on the bowl, except when
bringing food to their own mouth. When the beggar approached,
the selfish donor simply said ‘No’ in a harsh tone of voice and the
beggar moved away. The generous donor said ‘Have it’ in a friendly
tone of voice, at which point the beggar put her own hand into the
bowl and removed a piece of cereal and ate it. In all other respects
the procedure was identical to that described for the experimental
group.
Test Phase
The selfish and generous donors remained seated and still,
holding the bowl on their lap with both hands (so as not to use
hand cues inadvertently, which may influence the dog’s choice),
and looking down at the bowl (never at the dog). The dog was
allowed free movement in the room for 20 s. If dogs tried to jump
up and snatch the bowl from the researcher’s hands, the researcher
held the bowl out of reach until the dog was back on the ground,
and then resumed the position described above. No food was ever
given to the dogs.
After the test phase, the dog and owner were asked to leave the
room, the selfish and generous donors swapped sitting places, and
the owner was instructed to re-enter the room. Once the dog
had settled down, another observation trial, identical to that
described above, began. Overall, dogs witnessed three observation
trials (each lasting approximately 60 s), followed each time by a test
period lasting 20 s. Prior to each new observation trial, when the
owner and dog left the test room, its owner, outside the test room
to maintain the dog’s motivation with the test procedure, delivered
a small slice of sausage to the dog.
The researchers maintained their roles as selfish and generous
donors throughout the experiment for each dog. However, their
roles were counterbalanced across subjects and within each group.
Furthermore, the order in which the beggar approached the selfish
and generous donors was counterbalanced so that 50% of dogs in
each group saw the beggar approach the selfish donor last (before
the start of the test trial), and 50% saw the generous donor being
approached last.
3
Analysis
The Solomon (beta 091110, copyright 2006e2008 by András
Péter, Eötvös Loránd University, Department of Ethology, Budapest,
Hungary) software for behavioural analysis was used to code the
frequency and duration of behaviour from the video. During the
observation phase, the duration of the dog’s gazing behaviour was
coded in terms of where/whom it focused on: (1) gaze at owner;
(2) gaze at beggar; (3) gaze at selfish donor; (4) gaze at generous
donor; (5) gaze other. Gazing was defined as the dog orienting its
body and/or head towards a specific person, while remaining in its
original location. During the observation phase, when the beggar
was adjacent to the donors, it was not always possible to discern at
whom the dog was looking; thus in this case the dog was considered to be looking at the donor to which the beggar was closest (the
beggar spent an equal amount of time close to each donor).
During the test phase, the duration of the following behaviours
was coded: (1) interact with selfish donor; (2) interact with
generous donor; (3) interact with owner; (4) other (any other
behaviour not described above); (5) out of sight. The dog’s first
approach behaviour was also coded as (1) approach generous
donor, (2) approach selfish donor or (3) ambiguous approach. An
approach/interaction was defined as the dog moving towards
a specific person and either stopping in front of her (within arm’s
length) and adopting a static position (sitting, standing, lying
down) oriented to that person, or interacting with the person in
a more direct manner (pawing, nudging with nose, jumping up
with both forepaws on the donor’s lap, rubbing body against the
donor’s legs, etc.). For the first-choice data, an approach was
considered ambiguous if a dog moved towards the centre of the
room, equidistant from both donors, with a body orientation either
towards the owner or towards some other undetermined location,
or if it moved towards one of the donors, but then sat oriented
towards the other, or if it moved around the room but then
returned to a location adjacent to the owner.
A second coder analysed 35% of trials for the duration of gazing
behaviour in observation trials and interaction behaviour in test
trials. Spearman correlations for both behaviours were high
(observation trials: N ¼ 90: gaze at generous donor: rS ¼ 0.90,
P < 0.001; gaze at selfish donor: rS ¼ 0.93, P < 0.001; test trials:
N ¼ 90: interact with generous donor: rS ¼ 0.93, P < 0.001; interact
with selfish donor: rS ¼ 0.90, P < 0.001). Furthermore, the dog’s
first approach on 30% of trials was coded by a second observer
resulting in a substantial level of agreement (Kappa ¼ 0.81).
To assess the potential group differences in the preference for
gazing at the generous versus selfish donors during the observation
phase, a gaze preference index was calculated: gaze at generous
donor/(gaze at generous þ gaze at selfish donor) 100. To evaluate
the potential preference for each donor in the test phase, we
calculated the percentage of overall test time spent interacting with
the generous and the selfish donors and compared this within each
group (one-sample t test) and between groups (univariate ANOVA
followed by Tukey post hoc comparisons). Chi-square and binomial
tests were used to compare first-choice data. Statistical tests were
two tailed and the P value was set at 0.05. Data conformed to
assumptions for the use of parametric statistics.
RESULTS
We excluded 16 dogs from the study because during either the
observation phase or the test phase they hid under/behind
the owner, or showed other signs of stress and gave no attention to
the events during the observation phase. This left 20 dogs in the
experimental group (seven males and 13 females, mean 4.5 2.8
years), 24 in the ghost control group (12 males and 12 females,
Please cite this article in press as: Marshall-Pescini, S., et al., Social eavesdropping in the domestic dog, Animal Behaviour (2011), doi:10.1016/
j.anbehav.2011.02.029
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mean 3.7 2.4 years), 20 in the gestures group (six males,
14 females, mean 4.4 3 years) and 20 in the voice group (10
males, 10 females, mean 4 2.8 years).
During the observation phase, a significant difference emerged
between groups in the dogs’ looking preference towards the
generous donor (experimental: 62% (mean 64 s); ghost control:
56% (mean 50 s); voice: 61% (mean 66 s); gestures: 51% (mean
47 s); F3,80 ¼ 5.05, P ¼ 0.003) with dogs in the experimental and
voice groups looking longer at the generous donor than dogs in the
gestures group (post hoc: experimental versus gestures: P ¼ 0.007;
voice versus gestures: P ¼ 0.01) and no other difference occurring
(post hoc: experimental versus ghost control: P ¼ 0.2; experimental versus voice: P ¼ 0.9; Fig. 2).
To evaluate whether dogs showed a clear preference in their
choice of donor from the start, we compared the dogs’ first choice
between the generous and selfish donors (thus excluding dogs that
performed an ambiguous approach) in all three trials for each group.
Binomial tests (two tailed; test value set ¼ 0.5) showed that dogs in
the experimental group significantly preferred the generous donor
throughout (test 1: P ¼ 0.007; test 2: P ¼ 0.049; test 3: P ¼ 0.0002);
however, this preference did not occur in either the ghost control
group (test 1: P ¼ 1; test 2: P ¼ 1; test 3: P ¼ 0.7) or the gestures
group (test 1: P ¼ 0.3; test 2: P ¼ 0.8; test 3: P ¼ 1). In the voice
group, no significant preference for the generous donor occurred in
the first test (P ¼ 0.3); however, it approached and then reached
significance in the second and third tests (test 2: P ¼ 0.057; test 3:
P ¼ 0.03).
We carried out two separate between-group comparisons in
accordance with the aims of the study. (1) To assess whether dogs
were capable of distinguishing between a generous and selfish
donor on the basis of a third-party interaction, we compared the
experimental with the ghost control group and found that significantly more dogs chose the generous donor first in the experimental
group (c22 ¼ 3.98, P ¼ 0.046; Table 1). (2) To assess which human
communicative cues dogs used more to evaluate the interaction, we
compared the first choice carried out by the voice and gestures
groups; however, no significant difference emerged (Table 2).
In the test phase, we further compared groups on the percentage
of trial time spent interacting with the generous donor. A significant
difference emerged (experimental: 45%; ghost control: 15%; voice:
27%; gestures: 21%; F3,79 ¼ 9.14, P < 0.001) with dogs in the experimental group spending more time interacting with the generous
Table 1
Number (and percentage) of dogs whose first approach was towards either the
generous or selfish donor, or was considered ambiguous, in the experimental and
ghost control group
Test 1
Test 2
Experimental Ghost
Generous
15 (75)
donor
Selfish donor 3 (15)
Ambiguous
2 (10)
Experimental Ghost Experimental Ghost
10 (42) 13 (65)
9 (38)
5 (21)
Test 3
4 (20)
3 (15)
8 (33) 13 (65)
7 (30)
9 (37)
0
7 (35)
4 (17)
6 (25)
14 (58)
donor than dogs in all other groups (post hoc: experimental versus
ghost control and experimental versus gestures: P < 0.001; experimental versus voice: P ¼ 0.03; Fig. 3). Conversely, dogs in the ghost
control group spent significantly more time interacting with the
selfish donor (experimental: 2%; ghost control: 11%; voice: 2%;
gestures: 9%; F3,79 ¼ 3.67, P ¼ 0.015) than dogs in the experimental
and voice groups (post hoc: ghost control versus experimental:
P ¼ 0.045; experimental versus voice: P ¼ 0.046).
To assess further whether the dogs within each group exhibited
a preference for the generous versus the selfish donor, we
compared the percentage of time spent interacting with each actor.
Dogs in the experimental (mean: generous: 45%; selfish: 2%;
t20 ¼ 7.17, P < 0.001) and voice (mean: generous: 27%; selfish: 2%;
t20 ¼ 5.95, P < 0.001) groups spent significantly more time with the
generous than the selfish donor, but this was not the case for dogs
in the ghost control (mean: generous: 4%; selfish: 11%; t24 ¼ 0.72,
NS) and gestures group (mean: generous: 21%; selfish: 9%; t20 ¼ 1.8,
P ¼ 0.08).
DISCUSSION
The first aim of the study was to assess whether dogs could
eavesdrop on a food-sharing interaction between humans, where
the generous versus selfish intent was expressed by communicating with the beggar. Given that a clear preference for the
generous donor emerged in the experimental group (in all three
tests), that significantly more dogs in the experimental than the
ghost control group approached the generous donor first and spent
more time interacting with her, we can conclude that dogs are
effectively using third-party interactions to gain information on the
100
90
80
% Trial time
70
60
50
40
30
20
10
0
Experimental
Ghost control
Voice
Gestures
Group
Figure 2. Gaze preference index (time spent looking at generous/generous þ selfish donor 100): mean percentage of time spent looking at the generous (dark grey) and selfish
(light grey) donors during the observation phases for each group.
Please cite this article in press as: Marshall-Pescini, S., et al., Social eavesdropping in the domestic dog, Animal Behaviour (2011), doi:10.1016/
j.anbehav.2011.02.029
S. Marshall-Pescini et al. / Animal Behaviour xxx (2011) 1e7
behaviours with no recipient present; however, this kind of ‘ghost’
condition has been fruitfully employed in the context of other
social-learning studies (Hopper 2010), and, we think, could be
successfully adopted in studies involving humanedog third-party
interactions.
Our results, however, are also consistent with the possibility
that dogs are not so much showing a preference for the person
interacting generously, but rather seek to avoid the person who
behaved more brusquely with the third party. We do not think this
is in fact the case, since in the gestures group the selfish donor’s
behaviour was more aggressive than in the other two groups (she
did not just flick a hand but actually pushed the beggar away so that
the latter fell back). Given studies showing that dogs tend to read
human aggressive behaviour in terms of bodily movement
(Vas et al. 2005), we would have expected a strong avoidance of the
selfish individual in this group if dogs had been showing an
avoidance of the selfish donor rather than a preference for the
generous donor. However, this possibility cannot be totally
excluded and further studies will be necessary to discriminate
between competing hypotheses.
The second aim of the study was to start investigating which
kind of communicative cues dogs use to interpret third-party
interactions between humans in a food-sharing context. To this aim
we started by assessing whether dogs would rely more on the
humans’ vocal or gestural communication towards the beggar.
Although dogs in neither group showed a preferential approach to
the generous donor in the first test, in the voice group the dogs’
preference for the generous donor gradually emerged in the second
and reached significance in the third test. Furthermore, overall,
dogs in the voice group spent significantly more time interacting
with the generous than the selfish donor, whereas no such preference was shown by dogs in the gestures group. Finally, in the
observation phase, whereas dogs in both the experimental and
voice groups spent more time looking at the generous donor
(suggesting a preference already at this stage), dogs in the gestures
group did not. These results show that the use of gestures alone was
insufficient for dogs to discriminate between the selfish and
generous intent of the donors, and that the voice was the more
salient cue for understanding the interaction. However, dogs in the
Table 2
Number (and percentage) of dogs whose first approach was towards either the
generous or selfish donor, or was considered ambiguous, in the voice and gestures
group
Test 1
Generous donor
Selfish donor
Ambiguous
Test 2
Test 3
Gestures
Voice
Gestures
Voice
Gestures
Voice
10 (50)
5 (40)
5 (10)
10 (50)
5 (40)
5 (10)
10 (50)
8 (25)
2 (25)
11 (55)
3 (15)
6 (30)
5 (25)
6 (30)
9 (45)
12 (60)
3 (15)
5 (25)
5
potential likelihood of sharing food with a human stranger. The lack
of a preference for either donor in the ghost control condition
suggests that the effect observed in the experimental condition is
not simply due to a preference or avoidance of the behaviours
exhibited by the donors per se (e.g. avoiding the selfish donor
because she shows brusque movements and a harsh tone of voice),
but rather it is the interaction between the donors and the beggar
that provides important information that the dogs can use.
However, another possibility that must be considered is that the
difference in behaviour of dogs in the experimental versus ghost
control groups is simply due to different patterns of attention being
given to the donors during the observation phase. It may be that the
presence of the beggar increased the salience of the donor’s cues by
focusing the dog’s attention. This is unlikely, since dogs in both the
experimental and ghost control groups showed a similar preference for looking at the generous donor, and it was only in the
gestures group, despite the beggar being present, that dogs showed
equal attention to the generous and selfish donors. Thus, attention
to the donors does not seem to have been affected by the presence/
absence of the beggar.
As highlighted by Bonnie & Earley (2007), social eavesdropping
studies do not always control for the possibility that the preference
for a specific individual is due to the outcome of an interaction with
a social partner rather than having seen them manifest certain
behaviours during that interaction, which would have been equally
attractive had they been manifested without the presence of the
social partner. This may of course be difficult to achieve when
working with animals that cannot be asked to reproduce specific
**
60
**
50
% Trial time
40
**
30
20
10
0
Experimental
Ghost control
Voice
Gestures
Group
Figure 3. Mean percentage and SE of time spent interacting with the generous (dark grey) and selfish (light grey) donors during the test phase for each group. **P < 0.01.
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experimental group, where the actors combined voice and gestures
to convey the generous versus selfish acts, showed the strongest
preference for the generous donor (significantly more so than dogs
in the voice group), suggesting that the more communicative cues
available to the dogs, the better their discriminatory abilities.
Previous studies have shown that dogs are capable of obtaining
information through third-party interactions in a conflict situation
between conspecific (Cools et al. 2008) and that dogs are also
capable of flexibly choosing with whom to interact depending on
the outcome of a playful versus competitive interaction between
a human and a dog (Rooney & Bradshaw 2006). In the latter study,
dogs preferred either the winner or the loser depending on the
context, without showing a bias towards the human or dog. Thus
humans and dogs were ‘treated alike’ and chosen based solely on
their role in the interaction. Kundey et al. (2010) went a step
further, showing that dogs can also evaluate humans based on
observing a competitive interaction over a food resource.
However, it is not altogether clear from Kundey et al’s. (2010)
study whether in fact dogs evaluated the interaction between
actors and recipients, or simply chose the generous person (or
avoided the possessive one) based on the specific behaviours
exhibited towards the food resource (as opposed to the behaviours
exhibited towards the recipient). In fact, in all the cases in which
dogs discriminated between actors they saw a large bone either
being withdrawn from the attempted grasp of the recipient or being
ignored by the previous handler. Given the absence of a control
condition in which the exact same behaviours were manifested but
no recipient was present, it cannot be excluded that dogs simply
avoided the person manipulating the food in a possessive manner, or
chose the person who placed food on the ground and then no longer
showed interest in it. Although the results of that study are interesting, since they show that dogs are capable of discriminating
between different human behaviours towards a food resource, it
may not necessarily involve an understanding of a third-party
interaction. Potential support for this argument also comes from the
fact that, in our study, where food was not visible and thus dogs had
to evaluate the situation based on the behaviours directed towards
the beggar, they seemed to find it difficult to discriminate between
the actors’ generous versus selfish intent when this was expressed
with gestures alone, whereas in Kundey et al’s. (2010) study the
gestures directed towards the food were easily understood even
when accompanied by almost no social cues.
Our results raise a number of interesting questions concerning
both the complexity and the potential origins of dogs’ ability to
understand human communicative intent. One argument is that
humans differ from other species in their ability to evaluate others
socially because we are capable of forming a reputation about other
individuals based on a number of different parameters, thus showing
an abstract social-reasoning skill which can be applied in many
contexts. This is considered very different from the ‘domain-specific’
ability of eavesdropping in the context of mate selection or fighting
shown in other species (Subiaul et al. 2008). Although still in its
infancy, studies on eavesdropping in dogs so far seem to suggest that
they are capable of judging a human’s social attractiveness in at least
three different contexts (playful or competitive: Rooney & Bradshaw
2006; Kundey et al. (2010); resource sharing: current study) showing
a certain degree of flexibility. It may be that dogs learn about human
social cues exhibited directly towards them, and towards others, and
are capable of abstracting knowledge from these situations to assess
their partners’ potential value (Call 2001).
As to the origins of dogs’ ability to understand human
communicative intent, dogs, like their wolf, Canis lupus, ancestor,
could be considered a cooperative species (although see CluttonBrock 2009, for definitions of different forms of cooperation), but
reports of cooperation in feral populations are relatively rare
(Pal 2005; Cafazzo 2007; Bonanni et al. 2010) and there are few
experimental studies investigating this topic directly. The ability to
assess a human being’s generosity in a food-sharing context might
be a direct transfer of the ability to assess other dogs’ food-sharing
tendencies; however, no studies have investigated this issue, nor is
there any evidence that more tolerant dogs in a food-sharing
context are preferentially chosen as social/cooperative partners
(a link that has been shown in chimpanzees: Melis et al. 2006a, b).
Alternatively, assessing another individual’s generosity in
a food-sharing context may be a specialized skill that dogs have
developed in relation to humans, as part of the changes brought
about by the domestication process (Hare et al. 2002; Miklósi et al.,
2003; Hare & Tomasello 2005; Gacsi et al. 2009) and further
enhanced by the experience of frequent encounters with unknown
humans, a peculiarity that is thought to increase the importance of
reliance on indirect as opposed to direct reputation formation
(Bshary & Grutter 2006; Subiaul et al. 2008). The requirement to
interact frequently with conspecific and heterospecific strangers is
a trait that dogs share with humans and that may have had a crucial
role in shaping this species’ cognitive and communicative abilities.
Studies conducted to understand dogs’ (direct and indirect)
assessment of human and conspecific partners are still too scarce to
make firm conclusions; however, it may be that given the importance humans have for dogs’ survival, the latter have evolved
a sensitivity to specific human features, allowing them to
discriminate between potentially useful and harmful social partners, both directly and indirectly. It is, none the less, important to
note that, given a dog’s preference for multiple communicative
cues (voice and gestures) to detect the generous versus selfish
stance of the donors, it is likely that indirect assessment of human
generosity is substantially mediated by a learned component. Only
once dogs are capable of understanding our species’ behavioural
outputs in different contexts can they abstract social knowledge
from these situations (Call 2001).
Acknowledgments
This research was supported by doctoral and postdoctoral funds
from the University of Milan to C.P. and S.M.-P. We are grateful to all
dogs and owners for participating as volunteers. We thank Marco
Colombetti for drawing Fig. 1 and Simona Cafazzo, Roberto
Bonanni, Zsofi Viranyi, Frederike Range and Juliane Kaminski for
comments on the manuscript. We also thank the editor and two
anonymous referees for helpful suggestions and comments.
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APPENDIX
BREEDS OF PARTICIPATING DOGS
One Alaskan malamute, one Australian collie, two basenjis, four
beagles, one Belgian shepherd, one bichon bolognese, two bichon
frises, one border collie, one borzoi, four boxers, one Brittany
spaniel, two cocker spaniels, one corso, one Czechoslovakian
wolfdog, one doberman, two drahtar, two German shepherds, four
golden retrievers, one Jack Russell terrier, one Ibizan podenco, three
Irish setters, seven labrador retrievers, one miniature schnauzer,
one miniature poodle, two pinchers, one Portuguese water dog,
two pugs, one rottweiler, two Scottish collies, two shiba inu, one
standard poodle, two Siberian huskies, one terranova, two Yorkshire terriers, two vizla, one weimaraner, three whippets.
Please cite this article in press as: Marshall-Pescini, S., et al., Social eavesdropping in the domestic dog, Animal Behaviour (2011), doi:10.1016/
j.anbehav.2011.02.029