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Journal of Veterinary Behavior 10 (2015) 513e524
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Journal of Veterinary Behavior
journal homepage: www.journalvetbehavior.com
Canine Review
Canis sensitivus: Affiliation and dogs’ sensitivity to others’ behavior
as the basis for synchronization with humans?
Charlotte Duranton a, b, *, Florence Gaunet a
a
b
Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille Université, UMR 7290, Marseille, France
AVA Association, Cuy-Saint-Fiacre, France
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 30 January 2015
Received in revised form
5 August 2015
Accepted 18 August 2015
Available online 5 September 2015
One widely studied phenomenon in behavioral sciences is the ability of 2 individuals to behave in a
synchronous way, which has links with affiliative relationships and an adaptive role in increasing fitness.
Behavioral synchrony is found in various social species, but has been very little studied at the interspecific level. The unique relationship of humans and dogs deserves to be studied from this perspective.
This article reviews present knowledge about dogs’ sensitivity to other dogs’ and humans’ behaviors. The
conclusions are that (1) dogs are sensitive to other dogs’ and humans’ direct behavior, and adjust their
own behaviors accordingly; (2) dogs use some information from third-party interactions, and adjust their
behavioral response according to the outcome of the interactions; and (3) some recent data suggest that
dogs are sensitive to humans’ emotional cues, that they show social referencing toward humans, and
emphasize the strong affiliative bond between dogs and their owners. This finding suggests that dogs can
be considered as an appropriate biological model to study interspecies synchronization with humans. We
propose that dogs could mirror at least their owners during day-to-day situations and encourage further
research in this field.
Ó 2015 Elsevier Inc. All rights reserved.
Keywords:
domestic dog
behavioral synchronization
behavioral mimicry
dog-human synchronization
dog-human affiliation
Introduction
Being synchronized1 with other individuals can be defined by 3
complementary characteristics, 3 types of synchrony. First, the
temporal aspect of synchronization (also called temporal synchrony), is defined as switching actions at the same time
(Dostálková and Spinka,
2007; Lakin et al., 2003). The actions/activities/events can be identical or different (i.e., if all individuals in a
group switch from inactivity to activity, even if they are performing
different actionsdone switching from resting to scratching itself,
another from resting to yawning, and the third from resting to
standing up and moving), but the important feature is the timing.
* Address for reprint requests and correspondence: Duranton Charlotte, Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille Université, UMR 7290, 3 place
Victor Hugo, CS 80249, Bât. 9, Case D, 13331 Marseille Cedex 03, France, Tel: þ33 4
13 55 09 60; Fax: þ33 4 13 55 09 65.
E-mail address: charlotte.duranton@cegetel.net (C. Duranton).
1
In this review, we chose to focus only on nonconscious synchronization. Indeed,
conscious synchronization is a full field of study, leading to more complex phenomena such as cooperation, but we did not review it.
http://dx.doi.org/10.1016/j.jveb.2015.08.008
1558-7878/Ó 2015 Elsevier Inc. All rights reserved.
Second, the behavioral aspect of synchronization, often called activity synchrony, is defined as performing the same behaviors as
others in a short lap of time. This type of synchronization is also
often called behavioral matching, allelomimicry or nonconscious
behavioral mimicry in the literature (Chartrand and Barg, 1999;
Chartrand and Lakin, 2013; Gautrais et al., 2007; Lakin et al.,
2003; Louwerse et al., 2012). Third, the local aspect of synchronization, named local synchrony, is defined as being in the same place
at the same time (Bertram, 1980; King and Cowlishaw, 2009). These
aspects are often combined together and/or cited under the name of
synchronization in a broad sense (for each temporal/behavioral/
local synchrony alone or combined together), as suggested by
Louwerse et al. (2012), and we chose to do the same in the following
parts of the present review.
Synchronization is widespread among live beings and has
various adaptive values. Indeed, being synchronized with others
increases the fitness of offspring by decreasing the pressure of
predation (Yasaka et al., 2003), increases the chances of survival of
each member by avoiding predators (Conradt and Roper, 2000;
Fernandez et al., 2003), increases foraging efficiency (King and
Cowlishaw, 2009; Stone et al., 2003), and increases social
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cohesion among individuals (Gautrais et al., 2007; Rook and
Penning, 1991). Animals in pairs also benefit from behavioring in
a synchronous way. Synchrony helps to maintain pair bonds between partners (Lakin et al., 2003), which has direct benefits on the
pairs’ behaviors, for example, by increasing the efficiency of antipredation strategies such as vigilance in pademelons (Pays et al.,
2007; 2008), of a huddle in penguins (Ancel et al., 2009), and of
arrival in migratory birds (Gunnarsson et al., 2004). Does synchronization also occur between 2 individuals from different species? Surprisingly, this question has been very little studied. To our
knowledge, only one study has investigated the existence of interspecific synchronization as a main topic, focusing on activity synchrony between humans and capuchin monkeys (Cebus capucinus),
with the latter interacting more with people who did behaviorally
synchronize with them (Paukner et al., 2009). The lack of studies on
activity synchrony between individuals from different species could
be due to methodological and observational issues. Indeed, it is
possible that interspecific synchronization mainly occurs between
stable group members, or at least needs the 2 protagonists to
regularly interact. These situations are not very common.
One situation in which individuals from different species form a
stable group does exist and is easily observable: humans sharing
their daily life with dogs (Canis familiaris). The 2 main hypotheses
proposed to explain the special relationship between domestic
dogs and their human caregivers are the effects of a highly ancient
domestication (Hare et al., 2002; 2010; Vilá et al., 1997) and the
effects of dogs’ history of life (Wynne et al., 2008), the 2 being not
mutually exclusive (Udell and Wynne, 2010). Anecdotes report that
dogs sleep when humans sleep and are active when they are active.
Pet (Hart, 1995; Serpell, 1995, 1996; White et al., 2010) or working
(Gaunet and Milliet, 2010) dogs are known to form strong affiliative
bonds with humans. In humans, it is known that synchronization
and affiliation are positively correlated (Cheng and Chartrand,
2003; Lakin et al., 2003), but the ability of dogs to synchronize
their behavior with human behavior has not been studied to date.
The aim of this review is to discuss some prerequisites in dogs
leading to synchronization with humans: that is attention or
sensitivity to others’ behaviors and the ability to adjust their own
behavior accordingly to what they perceive (e.g., as found in
humans and fish, Chartrand and Bargh, 1999; Dijksterhuis and van
Knippenberg, 1998; Pitcher, 1979). We do so by examining dogs’
behavioral reactions to their conspecifics’ direct behavior, to
humans’ direct behavior, to dogs’ and humans’ indirect behaviors,
and finally by focusing on more direct evidence supporting our
hypothesis. Behaving in congruence with each other is yet an
essential aspect of human-dog interactions and relationships. We
review the following data about why dogs would show high levels
of synchronization with humans (see Figure 1 for a schematic
overview), more specifically with their owners.
Synchronization with humans could arise from dogs’
sensitivity to conspecifics’ direct behaviors
Evidence of the ability of dogs to adjust their behavior to that of
other dogs
The first step in this review is to consider the ability of dogs to
observe and use the behaviors of their conspecifics. In various
observed spontaneous dyadic interactions, dogs “adjust their
communicative behavior according to the behaviors of other individuals,” that is, they change their behavior so that it fits to
another individual’s behavior. For example, if a dog receives
agonistic behaviors from another dog, it is likely to display visual
communicative signals that will lead to a decrease in the other’s
agonistic signals (Gazzano et al., 2010). Dogs also adjust their
behavior according to their familiarity with the congener encountered: they emit twice as many communicative signals, such as
freezing and looking elsewhere, when meeting an unfamiliar dog
than a familiar one (Mariti et al., 2010).
Sensitivity to another dog’s behavior also leads to more complex
phenomena such as “social learning” (i.e., learning from conspecifics). For instance, “observational learning” is the ability of an
individual to learn to display a behavior faster if that individual has
previously seen a skilled individual (i.e., a skilled demonstrator)
performing it, than if there was no demonstrator, or after seeing a
“naïve” demonstrator (not skilled at performing the task) (Slabbert
and Rasa, 1997). This is highly adaptive, since it helps an individual
to acquire a strategy to achieve a goal or to decrease the costs of
nonsocial learning such as trial-and-error (Kubinyi et al., 2009).
Dogs learn from observing conspecifics from puppyhood. Indeed,
German shepherd pups, from observing their skilled mother,
learned to locate and retrieve a bag of narcotics faster than puppies
that did not observe this behavior (Slabbert and Rasa, 1997). This
ability is also found in adult dogs, and has been tested in various
situations. For instance, dogs learn to find hidden food by observing
a conspecific: they performed faster in finding a hidden treat after
seeing a skilled demonstrator dog going to the location (Heberlein
and Turner, 2009; Range and Virányi, 2013). They further adjusted
their behavior on the information they obtained after interacting
with the demonstrator conspecific (Heberlein and Turner, 2009):
they searched for food with more motivation and perseverance if
the demonstrator dog had found food than if it did not. This last
point thus shows that dogs are not only sensitive to their conspecifics’ behaviors they also adjust their own behaviors accordingly.
The ability to adjust to other dogs’ behaviors is also evidenced by
“sensitivity to the attentional state of conspecifics.” Dogs were found
to be sensitive to the direction of visual attention of other dogs
during dyadic play between dog partners (Horowitz, 2009). Indeed, if
a dog was not looking at its partner, the other dog moved and
changed its behavior to attract its attention (see Figures 2 and 3). In
addition, they displayed more play signals when the other dog was
pausing in the play session. Dogs thus produce communicative cues
in a flexible way when interacting with a partner (Horowitz, 2009).
Dogs also adjust their behavior to others in more artificial settings.
For example, a dog’s ability to coordinate with a partner (i.e., to
spatially and temporally adjust their behaviors) was studied during
attempts to solve a complex cognitive task and obtain a food reward.
If their partner was delayed, the dogs waited and inhibited their own
behavior until the partner was about to start the task (Ostoji
c and
Clayton, 2013). This is striking evidence that dogs tune their own
behavior to that of others in a flexible way.
Evidence of the ability of dogs to synchronize with other dogs
This topic has not been widely studied in recent canine studies.
However, dogs have been identified as an allelomimetic species for
some time. Vogel et al. (1950) wrote: “it is fairly obvious that this
[mutual mimicry] must occur in some of the highly coordinated
group activities of vertebrates” (p.121), “in a highly allelomimetic
species such as dog” (p.123). This statement shows that the extent
to which dogs synchronize their behaviors with others has never
been directly tested, as the ability of dogs to synchronize with
others was merely assumed to exist. We think that this assumption
and the late development of the study of dog cognition to which
belongs dog-others synchronization, may be an explanation for the
lack of recent studies in this field. Synchronization of behaviors in
dogs was mentioned by Scott and Fuller (1965, p.63), and synchronized switches of activities was assumed: the authors
described puppies howling together, and both puppies and adult
dogs sleeping, getting up, sitting and lying down, walking, and
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515
Figure 1. Dogs’ sensitivity to behaviors of other dogs as the basis for synchronization with humans. Arguments for considering that dogs show high levels of synchronization with
humans and would be a relevant biological model to study interspecific behavioral synchronization.
running at the same time (see Figure 4). More precisely, they
described (p.106) synchronized behaviors as emerging very early in
various breeds such as Basenji, beagle, cocker spaniel, Sheltie, and
fox terrier: “At first the members of a litter are quite independent in
their activities [.]. Between 3 and 4 weeks of age they begin to
follow each other around, and by 5 weeks we often see puppies
rushing toward the gate of their pen as a group. [.] By 7 weeks the
puppies have begun the group attacks [.] which are a combination
of allelomimetic and agonistic behavior”. Scott and Fuller (1965,
p.74) indeed stated “allelomimetic behavior is a basic part of the
social life of dogs.” The authors proposed that the main function of
behavioral synchronization in dogs is to provide safety, because all
group members can act together in emergencies (Scott and Fuller,
1965, p.75). To behave in a synchronous way, dogs maintain close
contact with one another (Scott and McGray, 1967) not only using
vision but also hearing and touch (Scott and Fuller, 1965, p74). In a
task consisting of running in pairs, without competition between
the individuals, mutual mimicry was observed in 2 different studies
with a tendency to synchronize the pace of running between the 2
dogs (Scott and Marston, 1950a; Scott and McGray, 1967), but no
effect of the familiarity of the congener was evidenced (Scott and
Marston, 1950b). In a recent study, dogs have been observed to
synchronize their behavior according to their familiarity. Indeed,
free-ranging dogs were locally synchronized: follower dogs presented more local proximity with the usual leaders than with other
followers (Bonanni et al., 2010). The authors proposed that dogs
showed more synchrony with individuals they considered as their
favorite social partners. Thus, it appears that dogs show more local
synchrony with congeners with which they have a higher degree of
affiliation. Finally, even if more research in this field is needed, dogs
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Figure 3. In play context, dogs adjust their production of play signals (e.g., play bow,
“chase me,” open mouth, bowed head) according to their partner’s direction of
attention. Dogs performed more play signals toward attentive recipients (black
component of bar) than towards inattentive ones (gray component). Adapted from
Horowitz et al. (2009).
Figure 2. Dogs adjust their behaviors to other dogs. During a dyadic play session, when
a dog stops looking at its playmate (A), the other one reorients itself (B), produces
attention-getting signals such as play-signal behaviors (C) to incite its partner to go
back to play. Adapted from Horowitz (2009).
do appear to show behavioral synchronization with others dogs.
We thus propose that their skills for intraspecific synchronization
could be one of the phenomena underlying their ability to synchronize their behavior with that of human beings.
This is the first prerequisite showing that dogs are a good
candidate species for interspecific synchronization with humans.
Synchronization with humans could arise from dogs’
sensitivity to humans’ direct behaviors
Dogs are sensitive to communicative cues from humans
Dogs are one of the very first species to live in such a close
cohabitation with humans (Vilá et al., 1997; Virányi et al., 2004).
First, dogs are sensitive to human behavior and use it to develop
new behaviors via direct observation and learning (Kubinyi et al.,
2003a). For example, when alone, dogs were not good at detouring a V-shaped fence to obtain a toy or food reward, but they
learned to go around the fence by watching a human demonstrator,
using the information gained by observation (Pongrácz et al., 2001).
Kubinyi et al. (2003a) also found that dogs used a new path to come
back home after seeing their owner using it, and they managed to
anticipate it when walking with their owner more than 50% of the
time. Dogs are also capable of learning from a human demonstrator
in manipulative tasks. When confronted with a box to open to
obtain a ball, they performed better after seeing their owner performing the task, and used the same strategy (Kubinyi et al., 2003b).
Second, dogs are skilled at using or understanding human
communicative cues. The ability of dogs to follow human deictic
cues (e.g., arm pointing) to find hidden food has been widely
studied using the so-called 2-way object-choice task. The dog is
facing a human demonstrator who is standing between 2 containers (one baited with food, the other not). The demonstrator
shows a container to the dog by pointing at it, and the dog is then
allowed to go and choose one container. Dogs have been found to
succeed (i.e., choosing the container indicated) in this task with
proximal or distal pointing or even cross-pointing and pointing
when more than 2 containers were present (Lakatos et al., 2012;
Miklósi and Soproni, 2006; Soproni et al., 2002). Moreover, dogs
also follow human gaze (head plus eyes) with good scores and
better performances if the gaze cue is given in repetitive consecutive manner compared to single continuous manner (Agnetta et al.,
2000; Kaminski et al., 2012; Téglás et al., 2012). There are indications that this sensitivity is learned in everyday life or in trials,
because a barely visible gesture, such as eye direction only, is poorly
used (McKinley and Sambrook, 2000). In working dogs, Lit et al.
(2011) evaluated the effect of humans’ beliefs and nonconscious
gestures on working dog outcomes. Lit et al. tested drug and
explosive detection dog-handler teams in different conditions,
including some in which the owner was misled with false information about the location of the marker: dogs made more mistakes
(i.e., indicating the wrong place) when the handler believed the
marker was in that place, even if he did not talk to the dog or
intentionally communicate with it (Lit et al., 2011). Thus, dogs
appear to be sensitive to slight communicative cues from humans,
even when these are unconsciously produced.
C. Duranton, F. Gaunet / Journal of Veterinary Behavior 10 (2015) 513e524
517
Figure 4. Example of behavioral synchronization among adult dogs. Barking and howling together (A) or lying together (B). Adapted from Scott and Fuller (1965).
Dogs adjust their behaviors according to human behaviors
Dogs are sensitive to humans’ body postures: they behave in
different ways depending on them. First, they are sensitive to the
direct behavior of a person toward them. For instance, Millot (1994)
used childlike dummies and presented them to the dogs. The
dummy was either in an affiliative posture (kneeling, with the head
tilted toward the shoulder, right hand extended with the palm
upward) or in an agonistic posture (kneeling, trunk and head forward, and right hand in a threatening position). The dogs’ reactions
were more positive (e.g., affiliative behavior such as tail wagging,
showing interest in the dummy) in the first condition than in the
second. Reactions of dogs to positive or friendly and negative or
threatening postures have also been investigated when they are
confronted with adult humans, in the so-called approach paradigm
(see Figure 5). In one study, an unfamiliar human approached a dog
in different ways, switching from one attitude to another, while the
}ri
dog’s behavioral response was recorded. Barrera et al. (2010), Gyo
et al. (2010), and Vas et al. (2005) found that the dogs’ behavioral
reactions varied according to the threatening or friendly
approaching human. Dogs were more likely to avoid the person,
avert their gaze, and vocalize, and less likely to exhibit contactseeking behaviors with the threatening approach than with the
friendly approach. Finally, the dogs adjusted their behavior from
passive or friendly to aggressive or avoiding, and the reverse, according to switches in the human’s behavior (see also Gácsi et al.,
2013; Vas et al., 2008). Dogs also flexibly change their behaviors
according to a human’s behavior when facing an unsolvable
problem-solving task. One study reported that they looked back
more often at their owners if he/she had previously encouraged
them than if the owner remained silent (Horn et al., 2012).
Second, it appears that dogs discriminate the direction of visual
attention in humans, that is, body direction, and the orientation of
the head and eyes (i.e., gaze). When asked by their owners to lie
down, dogs behaved in different ways depending on context
(Schwab and Huber, 2006). When the dogs were being watched by
the owner, they stayed in the commanded position more often and
for longer than in other situations (e.g., owner reading a book,
watching TV, and so forth). In another obedience context, dogs
were confronted with a visible piece of food, and were told to
leave it by their owners (Call et al., 2003). The dogs approached
food in a more indirect way and took less food when the experimenter was facing them, compared with when she was turning
her back or absorbed in some activity. When the dogs were facing
two humans, one turning away from them and the other facing
them and were then allowed to beg for food, they preferentially
begged for food from the person facing them (Gácsi et al., 2004;
Virányi et al., 2004). In another context using play (object-
fetching game), dogs had to bring the toy back to the front of the
human: they reoriented their own position if the human was
turning his back to the dog (Gácsi et al., 2004). Dogs also
discriminate their owner talking to a third party and not paying
attention to them (i.e., they obey their owner less) compared with
directly talking to them or talking away from the dog toward an
empty space (Virányi et al., 2004). Furthermore, when dogs were
involved in a referential communicative task toward their owners,
they positioned themselves in the optimal location to attract their
owners’ attention, taking into account their line of gaze (Gaunet
and Deputte, 2011; cf. also Kaminski et al., 2009 for sensitivity to
the visual perspective of humans, but see Gaunet and El Massioui,
2014). These results show the flexibility of dogs’ behaviors and
their ability to adjust them to the direction of attention in humans
(see also Savalli et al., 2014). However, there are limits to this
sensitivity. Indeed, Gaunet (2008, 2010) found that whereas guide
dogs performed more audible mouth licks toward their blind
owners than pet dogs toward their sighted owners to obtain food,
Figure 5. Dogs adjust their behavior to direct human cues. In the so-called approach
paradigm, dogs adjust their behavior from passive or friendly to aggressive or avoiding
according to the switch in human behavior from friendly (A) to threatening (B)
approach. Adapted from Vas et al. (2005).
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the 2 groups did not differ when they asked for a toy. These results
suggest that dogs’ ability to adjust a toy-directed behavior might
be tuned to early experience with humans bcause it is likely to be
sighted families that raise guide dogs.
Finally, this sensitivity to human’s communicative cues in dogs
extends to another area: sensitivity to emotional cues in humans.
This sensitivity is essential in interactions between individuals,
enabling them to behave in the appropriate way in accordance
with the visible emotional cues the partner is displaying (Ekman
and Frisen, 1975). Even if this is a new research field in dog science, there are studies with evidence that dogs are sensitive to
cues signalling emotions in humans. Dogs are sensitive to
emotional global body posture and adjust their behavior accordingly (Vas et al., 2005; Custance and Mayer, 2012). They are also
sensitive to different emotional tones of voice, such as gentle (high
pitched) versus harsh (low pitched) voice (Ruffman and MorrisTrainor, 2011; Scheider et al., 2011). Finally, they are also able to
focus on the face, and discriminate different human expressions,
such as smiling faces from blank expressions (Nagasawa et al.,
2011), sadness versus happiness (Morisaki et al., 2009), happiness versus disgust (Buttelmann and Tomasello, 2013), or happiness versus anger (Müller et al., 2015). According to these authors,
this ability to discriminate human facial expressions is adaptive,
because it helps dogs to adjust to humans. In another study, dogs
were exposed to human faces expressing joy, fear, anger, or disgust
(Deputte and Doll, 2011). Adult dogs, but not younger ones,
responded more to anger (by avoiding the face) and fear (by
paying more attention to the face). The dogs could have learned to
adjust their behavior according to human emotions by repeated
exposure to them.
These data add consistent evidence that dogs are sensitive to
direct behaviors in humans, which is one of the prerequisites
leading to dogs’ ability to synchronize with humans beings.
Synchronization with humans could arise from dog’s
sensitivity to third-party interactions
Dogs are efficient at adjusting their behaviors to the direct
behaviors of both conspecifics and humans. We also must consider
the sensitivity of dogs to indirect behaviors, that is, third-party
interactions, as an essential prerequisite to dog-human synchronization. Sensitivity to indirect behaviors is defined as the ability
to get information from the interaction of 2 individuals (thirdparty interaction), and then to behave with the protagonists according to the outcome of the interaction (also known as
eavesdropping).
Sensitivity of dogs to human third-party interactions
The issue of the sensitivity of dogs to indirect human behavioral
cues during third-party interactions has been explored in the
foraging context. In a first experiment, after dogs were informed
that 1 of 2 pots could contain food, they were faced with 2 humans
interacting together: one called the other and only showed him/her
1 of 2 containers (the baited one) by pointing or gazing at it
(Kaminski et al., 2012dexperiment 3). Then the dogs were
released. They did not choose the indicated baited container more
than the nonbaited one. Thus, in this study, dogs did not gain information from a third-party interaction between humans about a
food location, or at least did not use it or behave accordingly.
In other studies, Marshall-Pescini et al. (2011) and Kundey et al.
(2011) tested dogs’ ability to eavesdrop in a food-sharing task. An
observer dog watched 2 humans (the donors) interacting with a
third (the demonstrator). The demonstrator requested food from
the donors. The mean donor did not allow the requester to have the
food (e.g., by removing the food, or saying “no” in a firm voice and
flicked her hand away), and the friendly donor gave the food to the
requester. The dogs were then allowed to go and choose a donor:
they first approached and interacted more with the friendly donor
rather than with the mean one in both studies (see Figures 6 and 7).
The authors concluded that dogs distinguished the roles of the
participants, and then used the information to behave accordingly.
When Nitzschner et al. (2014) replicated this protocol, the results
were not convergent. Moreover, the authors added a condition:
after the dog observed the interactions, the friendly and mean
donors switched their places (without the dog seeing it). Surprisingly, the dogs did not choose the friendly donor, but preferred the
side where the positive interaction occurred. The authors thus
concluded that there is no support for eavesdropping in dogs when
observing humans sharing food. Interpreted more parsimoniously,
dogs would have chosen the side emphasized during the positive
interaction. In a last study, dogs observed 2 donors behaving in the
same way (i.e., giving food to the person asking) but with the
requester reacting in a positive manner to one (eating the food and
speaking in a positive tone) and in negative manner to the other
(not eating the food and speaking in a negative tone) (Freidin et al.,
2013). The dogs more often chose the donor obtaining the positive
interaction. The authors concluded that the dogs were able to
eavesdrop from the interaction.
Thus, given the variability of the protocols and results presented
previously, replications and deeper analyses of the tasks and processes involved will clarify the conditions of fulfillment of dogs’
sensitivity to human third-party interactions.
Sensitivity of dogs to interspecific third-party interactions
Sensitivity of dogs to conspecific third-party interactions
Dogs are sensitive to the behavior of conspecifics from early
ages, and third-party interactions are found among littermates.
Indeed, when 2 puppies play-fight together, a third often intervenes
in the interaction, that is, approaches the dyad and physically interferes, by targeting (e.g., jumping on, biting at, or mounting) the
loser (Ward et al., 2009). The authors of this study proposed that
puppies behave in a specific way toward the loser by doing what
the winning puppy is doing. Sensitivity to third-party interactions is
also found in adult dogs. During a conflict between 2 individuals,
dogs display reconciliation behaviors toward the loser, that is, exchanges of friendly behaviors shortly after the aggressive conflict
(Cools et al., 2008). This shows that dogs recognize the outcome and
individual roles of conspecifics in various third-party situations
(e.g., play, contest), and adjust their own behavior in an appropriate
way, even if more studies in this field are clearly needed.
To our knowledge, only 3 studies have investigated the ability of
dogs to evaluate indirect behaviors in interspecific interactions. In
one study, dogs observed 2 experimenters interacting with a
demonstrator dog (Nitzschner et al., 2012). One behaved in a
friendly way with the dog (e.g., displaying play signals, talking
nicely to the dog, petting the dog), and the other ignored the dog
(e.g., walked by without looking at or talking to it). First, the dogs
vocalized, scratched, and jumped on the separation barrier more
often during the observation phase of the friendly interaction than
during the other interaction. Then, when allowed to interact with
the experimenters, they did not show any behavioral difference
toward one or the other. The authors concluded that the dogs
distinguished the different types of dog-human interactions and
gained information but did not then use it for their own behavior.
They proposed 2 hypotheses to explain this failure to use the information. First, the ignoring situation could have been interpreted
C. Duranton, F. Gaunet / Journal of Veterinary Behavior 10 (2015) 513e524
519
Figure 7. Eavesdropping in dogs. Dogs observed a third-party interaction (experimental group: 1 human requester, and 2 human donors; control group: 2 donors, no
requester). In the experimental group, the dogs spent more time interacting with the
generous donor (45%) than with the selfish one (2%); in the control group, no effect was
found. The dogs spent significantly more time interacting with the friendly donor in
the experimental group than in the control group. *P < 0.05. Adapted from MarshallPescini et al. (2011).
Figure 6. Dogs gain information from observing third-party interactions. After
observing a human demonstrator asking for food and (A) receiving it from the friendly
donor (left) but (B) not receiving it from the selfish donor (right), the dog preferred to
interact with the friendly donor (C). Adapted from Marshall-Pescini et al. (2011) and
Kundey et al. (2011).
by the observing dog as a walking activity and considered to be as
positive as the friendly interaction. Second, the situation was quite
neutral, as no play, contest, or foraging was involved, and it could be
that the dogs did not consider the information gained or perceived
as relevant for themselves. This logic is in agreement with another
study where, in a more natural setting, dogs gained information
from interactions between humans and dogs (Rooney and
Bradshaw, 2006). The dogs were spectators of interspecific
competitions between a human and a dog. The 2 protagonists were
competing for an object, either in a playful way (the human presented play signals before the interaction) or in a contesting way
(the human did not produce play signals before the interaction).
Then the spectator dog was allowed to go and interact with the 2
protagonists. The dogs more often and more readily approached the
winner, whether the human or the dog won the tug-play game.
Conversely, the dogs approached both participants more slowly
when the interaction was similar to a real contest. Thus, the dogs
not only distinguish between the behaviors of 2 interacting partners, even when they were not involved in the interaction, they also
discriminated between different contexts (play/contest) and tuned
their behaviors according to the outcome of the interspecific
interaction. Finally, Range et al (2009) showed that dogs were
sensitive to third-party interspecific interactions in an obedience
context. Indeed, 2 dogs (the subject and a partner) had to perform a
command (give the paw). If the subject received no food, the authors found that the dog would stop obeying the command earlier if
he could see the partner dog receiving food, than he would have
when alone. The authors concluded that dogs were sensitive to the
outcome of the interspecific interaction and behaved accordingly.
Dogs are thus sensitive to third-party interactions between
others dogs, other humans, and even between dogs and humans.
These are consistent findings, enabling us to propose that dogs have
one more prerequisite leading to the ability to synchronize their
behaviors with those of humans.
Direct evidence supporting the existence of dog-human
synchronization
This review provides evidence for dogs’ sensitivity to human
behavioral cues and shows how skilled they are at using human
behaviors. They are able to distinguish human behaviors when they
are directed toward them, and also when directed toward other
humans. We hypothesize that these skills may underlie dogs’ ability
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C. Duranton, F. Gaunet / Journal of Veterinary Behavior 10 (2015) 513e524
to adjust their behavior to human behavior (Ostoji
c and Clayton,
2013).
It is well known that dogs are strongly affiliated with humans
and even more strongly with their owners (Horn et al., 2013). In
addition, synchronization between human individuals is positively
correlated with rapport (Chartrand and van Baaren, 2009). Indeed,
high rapport and liking between individuals have been found to be
linked to a greater tendency to behavioral synchronization
(Chartrand and van Baaren, 2009). In one study, when a person
interacted with another human presented as a peer, he/she more
often exhibited behavioral synchronization (such as tapping a foot,
or touching the face) than with a confederate presented as a supervisor (Cheng and Chartrand, 2003). In another study, if 2 human
individuals had a common affiliation goal, an increase in synchronization between them was observed, compared to when there was
none (Lakin and Chartrand, 2003). This phenomenon is also found
in many other species. Indeed, the more 2 wild bottlenose dolphins
(Tursiops aduncus) engaged in affiliative behaviors, the more they
exhibited synchronous pair-swimming behaviors (e.g., type of activity, direction of swim, breathing episodes; Sakai et al., 2010). A
similar facilitating role of affiliation on synchronized breathing
behavior was also found in long-finned pilot whales (Senigaglia
et al., 2012). In Tonkean macaques (Macaca tonkeana), affiliative
relationships play an essential role in collective movements:
indeed, it was observed that an individual joined the movement of
collective departure depending on the departure of its strongly
affiliated mates (Sueur et al., 2009).
At group level, dogs more readily follow a leader toward whom
they show affiliative behavior than other individuals (Bonanni et al.,
2010). Dogs and their owners develop strong affiliative bonds (Horn
et al. 2013; White et al., 2010). Because dogs are sensitive to human
behavioral cues, and adjust their behavior in an appropriate
manner, it appears plausible that a phenomenon such as synchronization could exist between dogs and humans. Very few studies
have investigated this question in dogs, and it was not the main
focus of the studies involved. For example, Millot et al. (1988)
studied the factors influencing dog-child interactions. They found
that when the child presented more affiliative behaviors, it
increased the tendency among the dogs to present affiliative behaviors too. But the authors did not investigate whether there was
actual behavioral synchronization between the 2 partners. To our
knowledge, only 1 recent study has investigated synchronization
between human and dogs, observing interactions in terms of timing
patterns (Kerepesi et al., 2005). These authors analyzed a cooperative situation between an owner and his/her dog (the owner asked
the dog to help him to build a tower). The results showed that the
behaviors of both dog and owner were organized into temporal
patterns, with communicative behavior units and action units. The
authors proposed that dog-human interactions could be much
more organized in time than previously thought (Kerepesi et al.,
2005). Gaunet et al. (2014) also provided evidence that dogowner dyads in the street presented an adaptive synchronized
and silent walk, indicating synchronous behaviors between the
members of dyads and highlighting a specific bond (Hart, 1995).
Thus, we propose that behavioral synchronization could indeed
exist between dogs and humans during daily interactions.
Two further fields of study in dogs may support our hypothesis.
First, the existence of dog-human yawning contagion, that is,
yawning in dogs triggered by seeing a human yawning (JolyMascheroni et al., 2008). It is proposed to be linked to the capacity for empathy of a given species (Romero et al., 2013; Silva and De
Sousa, 2011), but a more parsimonious consideration of yawning
contagion as a case of activity synchrony between humans and dogs
has been suggested, whereby dogs are considered as “social chameleons” (Yoon and Tennie, 2010). Moreover, it has been proposed
that dog-human contagious yawning depends on the emotional
connection between individuals (Joly-Mascheroni et al., 2008; Silva
et al., 2012), and dogs were observed to be more sensitive to their
owner’s yawns compared to those of an unfamiliar human (Romero
et al., 2013; Silva et al., 2012). These authors proposed that this
reflects the existence of an affiliation-dependent activity synchrony
between dogs and humans. Yet recent studies have shown that an
actual mimicry of human yawns and the processes at plays are not
so clear-cut (Harr et al., 2009; O’Hara and Reeve, 2011). If
confirmed, the existence of dog-human contagious yawning would
thus be a clear case of dog-human synchronization and is essential
to take into account. Finally, recent studies have shown that dogs
were sensitive to their owners’ emotional cues. When the owner
was stressed, the behaviors of dogs were affected in a cognitive
task, suggesting an emotional contagion (Sümegi et al., 2014).
When listening to a human infant crying, dogs reacted in the same
way as humans: their cortisol level increased, and their behaviors
were affected (Yong and Ruffman, 2014). For the authors, these
findings evidence the potential existence of dog-human emotional
contagion. Custance and Mayer (2012) also found that when confronted with a human crying, dogs interacted more with him/her
than if the person was just talking or humming. The authors proposed a parsimonious interpretation of emotional contagion between human and dogs, coupled with a learning history with dogs
rewarded for approaching their sad owners. Even if still not fully
explained and demonstrated, these observations of dog-human
yawning and emotional contagion could add important evidence
supporting our hypothesis.
The second field of study potentially supporting our hypotheses
is led by Merola and colleagues and focuses on social referencing in
dogs. “Social referencing” is the process by which an individual,
when confronted with an unknown stimulus or event, seeks and
gains information from another individual and uses it to guide its
own behavior (Merola et al., 2012a, b). Social referencing involves 2
different components: the subject alternating gaze from the individual to the object or event, and the subject’s behavioral adjustment based on the information received from the informant (see
Merola et al., 2012a for more details). In a recent study, the authors found that dogs chose an object according to the cues of their
owner’s visible emotional reaction (Merola et al., 2013b). When
confronted with two identical toys, the dogs preferentially chose
the toy eliciting a positive visible emotional reaction in their owner.
In their other studies, the authors confronted dogs with an unfamiliar stimulus (a fan with green plastic ribbons on it). Then they
observed the dog’s behaviors according to its owner’s reaction
(Merola et al., 2012a, b) or to a stranger’s reaction (Merola et al.,
2012b). The authors found that whatever the degree of familiarity
with the person, when dogs were faced with the novel object, they
cast gaze alternations between the object and the human. The
humans were then told to behave either in a positive way towards
the object (happy voice and facial expression, then approaching the
object), or in a negative way (fearful voice and facial expression,
then moving away from the object). When the human informant
was the owner, dogs in the negative group showed more static
behaviors than dogs from the positive group, and they used the
space in opposite manners, mirroring their owner’s movements.
The dogs in the positive group indeed moved closer to the fan,
whereas in the negative group, they spent more time as far as
possible from the fan (Merola et al., 2012a) (see Figure 8). These
dogs where thus strongly influenced by their owners’ behaviors
toward the new object, because they mirrored their owners’ reactions. When the informant human was a stranger there were
fewer differences between the negative and positive groups, suggesting that the relational bond was essential for the dog to synchronize its behavior on that of the human (Merola et al., 2012b).
C. Duranton, F. Gaunet / Journal of Veterinary Behavior 10 (2015) 513e524
521
Figure 8. Social referencing paradigm between dogs and their owners. When confronted with a strange object, the behavioral responses of the dogs [approaching (A) or
avoiding (B) the new object] varied according to their owners’ reactions [curious (A) or
fearful (B)]. Adapted from Merola et al. (2012a; b).
But in another study, the authors found that pet dogsdbut not
water rescue-trained dogsdused strangers as informants in a social
referencing context (Merola et al., 2013a). All these results show
that, even if still not yet extensively studied in interspecific context,
social referencing occurs between dogs and humans, and dogs
synchronize their behavioral reaction with humans’ one in an
adaptive manner, at least when confronted with an unknown
object.
Finally, a study recently found that when confronted with a
problem-solving task in which dogs were released to open a box
after watching their owner doing itdthe owner staying
silentdinterestingly, the dogs exhibited an automatic tendency to
imitate their owners, even when it was counterproductive (Range
et al., 2010) (see Figure 9 for more details about the
proceduredA, B, C, and resultsdD). This one study adds a further
argument in favor of our hypothesis that dogs synchronize their
activity with their owners’ one.
To get additional insight into possible behavioral synchronization by dogs, we propose to consider another natural situation
experienced by dog-owner dyads: encounters with unfamiliar
persons, for example, when going to the vet, or when walking dogs
in public areas. Indeed, owners need to manage their dogs in a safe
way when they meet very different types of unfamiliar people:
children, elderly persons, or people afraid of dogs (Gaunet, 2012).
These situations are known to cause agonistic reactions in dogs
toward humans, and most bites in public areas involve people who
are unfamiliar to the dogs (Cornelissen and Hopster, 2010). This is
why dogs’ reactions toward an unfamiliar person have been
extensively studied, with the so-called approach paradigm
(described above). But so far, to our knowledge, only the effect of
various behaviors by strangers has been investigated (e.g., Vas,
}ri et al., 2010). In natet al., 2005; 2008; Ortolani et al., 2009; Gyo
ural circumstances, when owners encounter a stranger, it is not
easy to ask the stranger to behave in a specific way to avoid
agonistic reactions from the dog. As a consequence, owners are
often seen calling back their dogs, changing their path, or trying to
hold their dogs back to prevent them from reacting toward the
Figure 9. Automatic imitation is present in dogs in a problem-solving task. The procedure is detailed on apparatus (A), pre-training (B), no command test (C). Results are
displayed in (D): the dogs more readily adopted the same action as that demonstrated
by their owner. Adapted from Range et al. (2010).
stranger. In these circumstances, owners are often stressed, and/or
behave in a quite harsh way toward their dogs. This could induce
negative associations for the dogs, creating a vicious circle leading
to agonistic reactions of the dogs toward the unfamiliar person.
Thus, to be more realistic, and considering the research reviewed
here, we propose that further research studies should focus on the
effect of the owner’s behavior, and on the way it could influence
dogs’ behavioral responses when faced with an unfamiliar person,
by way of observational learning, emotional contagion, and/or
behavioral synchronization. What appears essential is to establish
the extent to which the owners’ reactions during such encounters
influence their dogs’ behavioral responses. In other words, does a
stressed, avoiding reaction by the owner, or conversely a happy,
relaxed reaction, affect the dog’s behavior? To our knowledge, only
one study has discussed this potential influence. Neessen (2013)
tested the influence of a supportive owner versus a passive owner
when the dogs met a new person. The author found that when the
522
C. Duranton, F. Gaunet / Journal of Veterinary Behavior 10 (2015) 513e524
owners gave active support to their dogs (i.e., by talking calmly to
them and petting them), it reduced the agonistic behaviors toward
an approaching unfamiliar person, but these results have not yet
been published (Neessen, 2013).
Thus, we recommend that further studies should investigate
these aspects as a paradigm for studying synchronization between
human and dogs. From the current review, we can suggest that
owners’ reactions do influence dogs’ behaviors toward an unfamiliar human. We hypothesize that dogs synchronize their
behavior with their owners’ behavior toward the stranger. We also
hypothesize that the type of relationship between the dog and its
handler could play a role in this behavioral synchronization (e.g.,
caretakers with shelter dogs; different members of the family with
pet dogs; various dog professionals with pet and working dogs). A
key step will thus be to design experiments testing these specific
hypotheses in an approach paradigm, varying owner behaviors to
observe the consequences on response in the dogs. Further research
in this field will give more understanding about dog-human interactions. From a practical viewpoint, it will provide key information on how the owner can influence and manage his/her dog in
daily situations such as meeting an unknown person who wants to
chat or to pet the dog, or who is wearing unusual clothes or
behaving unusually. Ultimately, if behavioral synchronization is
present between the owner and his/her dog, if dogs do indeed
mirror their owners, it could enable us to provide scientific data for
dog trainers and dog owners, and to propose advice on how to
behave to reduce stress and agonistic behaviors in dogs in these
situations, by considering or acting on the owner’s nonverbal
behavior.
Acknowledgments
The authors gratefully acknowledge Marion Montaigne for her
drawings. We thank Prescott Breeden, Séverine Belkhir, and Dr.
Thierry Bedossa for reading the article and their helpful suggestions
on it. This work was funded by Association Nationale de la
Recherche et de la Technologie, Association Aide aux Vieux Animaux, the Centre National de la Recherche Scientifique, and AixMarseille Université. The idea for the article was conceived by Dr.
Florence Gaunet and Charlotte Duranton (PhD). The review was
written, by both Dr. Florence Gaunet and Charlotte Duranton.
Conflict of interest
The authors declare no conflict of interest.
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