HOMEWORK #1

So for your homework, find a recent scientific article (no more than 10 years old) that supplies evidence for dogs having better communication with humans than wolves do! Please post the article citation and a brief two paragraph (at least 800 words) summary of how the evidence shows that dogs have some abilities that wolves do not. Then post an illustrative video (can be from YouTube!) showing dogs using their communication skills with humans.

(MY ARTICLE IS POSTED IN THE OTHER FILE)

For this homework assignment, we will continue to examine the differences between “tame” behavior and domestication.

For example, the domesticated foxes of Dr. Belayev’s experiment were friendly towards humans whereas the fearful/control line was not. Scientists have compared wild foxes with the domesticated foxes and find they differ on a number of communicative behaviors. That is, that they get more information from humans and establish a two-way communication with them.

The same argument applies for wild wolves versus domesticated dogs. Through the action of selection (whether as a by-product of selection on stress levels or cognition or not) dogs have very different behaviors than wolves. The primary differences lie in human-dog communication.

Bonus –  compare them with research on Dr. Belayev’s foxes!

https://youtu.be/GNf2vLhifiU

Hint:

For your evidence please use scientific articles (i.e., not the NYT or Scientific American) from the primary literature such as Nature, Animal Behavior, PLOS, etc. Use this format below for your citation (PLEASE do not just post a link without a citation).

Example citation:

Francois, A. 2016. Insight into dog and wolf behavior: dogs gaze longer at humans during communication. Animal Behavior 131:12-16.

For this article, I would write a two paragraph summary about how the article above provides evidence that dog gazes are different from wolf gazes and it affects communication in the following ways…etc.

A comparison between wolves, Canis lupus, and dogs, Canis familiaris,
in showing behaviour towards humans

Marianne T. E. Heberlein a, c, *, Dennis C. Turner a, d, Friederike Range b, c, Zs!ofia Vir!anyi b, c
a Animal Behavior, Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
b Messerli Research Institute, University of Veterinary Medicine Vienna, Medical University of Vienna and University of Vienna, Vienna, Austria
c Wolf Science Center, Ernstbrunn, Austria
d Institute for Applied Ethology and Animal Psychology (I.E.A.P./I.E.T.), Horgen, Switzerland

a r t i c l e i n f o

Article history:
Received 2 March 2016
Initial acceptance 14 April 2016
Final acceptance 11 August 2016
Available online 1 November 2016
MS. number: 16-00184R

Keywords:
Canis familiaris
Canis lupus
cognition
dog
gaze alternation
imperative pointing
referential communication
showing
wolf

Both human and nonhuman primates use imperative pointing to request a desired object from another
individual. Gaze alternation often accompanies such pointing gestures, and in species that have no hands
this can in itself function as imperative pointing. Dogs have exceptional skills in communicating with
humans. The early development of these skills is suggested to have been facilitated by domestication.
Adult wolves socialized with humans can use human-provided information to find food in various sit-
uations, but it is unclear whether they would use gaze alternation to show their human partner a target
location they cannot reach on their own. In our experiment, we tested wolves and dogs in a task where
they could indicate an out-of-reach food location to one of two human partners. One partner reacted in a
cooperative way and gave the food hidden in the indicated location to the subject whereas the other
responded in a competitive way and ate the food herself. Our results suggest that wolves, as well as dogs,
use ‘showing’ behaviours to indicate a food location to a human partner, and that both can adjust their
communication to the cooperativeness of their human partners, showing more indicating signals in the
presence of the cooperative partner than in the presence of the competitive one. We conclude that
wolves and dogs, both kept in packs under the same conditions, can use humans as cooperative partners,
and point imperatively in order to receive a desired out-of-reach object. It seems that intensive social-
ization with humans enables both wolves and dogs to communicate cooperatively about a food location
with humans, most probably relying on skills that evolved to promote social coordination within their
packs.

© 2016 The Authors. Published by Elsevier Ltd on behalf of The Association for the Study of Animal
Behaviour. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/

licenses/by-nc-nd/4.0/).

At about 12 months of age, children start to point in order to
communicate with their caregivers (Bates, Camaioni, & Volterra,
1975; Blake, O’Rourke, & Borzellino, 1994). Children use declara-
tive pointing when they want an adult to share attention/feelings
with them about an interesting event or object, and they use
imperative pointing when they want an adult to do something for
them, such as giving them a desired object (Bates et al., 1975;
Camaioni, 1993). Imperative pointing has been described not only
in humans, but also in captive chimpanzees, Pan troglodytes (e.g.
Leavens & Hopkins, 1998; Leavens, Hopkins, & Bard, 1996; Leavens,
Hopkins, & Thomas, 2004), orang-utans, Pongo pygmaeus, gorillas,

Gorilla gorilla, and bonobos, Pan paniscus (for review see Leavens &
Hopkins, 1999) when interacting with humans. In most cases,
pointing occurred towards objects or food items that were out of
reach of the animals but that could be reached by the familiar
humans with whom the animals were interacting. Therefore, it is
usually assumed that the animals point in order to get their human
partners to give these desired objects to them. Pointing in children
(e.g. Bruinsma, Koegel, & Kern Koegel, 2004) as well as in
nonhuman primates is often accompanied by gaze alternation (e.g.
Anderson, Kuwahata, & Fujita, 2007; Leavens & Hopkins, 1998).
Accordingly, it has been argued that in species that have no hands,
gaze alternation and other behaviours combining attention-
attracting and directional components can have a similar function
as pointing (Harding & Golinkoff, 1979; Leavens & Hopkins, 1998;
Leavens, Russell, & Hopkins, 2005). For instance, various studies
have shown that dogs readily alternate their gaze between the

* Correspondence: M. T. E. Heberlein, Animal Behavior, Department of Evolu-
tionary Biology and Environmental Studies, University of Zurich, Winter-
thurerstrasse 190, 8057 Zurich, Switzerland.

E-mail address: marianne.heberlein@ieu.uzh.ch (M. T. E. Heberlein).

Contents lists available at ScienceDirect

Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

http://dx.doi.org/10.1016/j.anbehav.2016.09.023
0003-3472/© 2016 The Authors. Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour. This is an open access article under the CC BY-NC-
ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Animal Behaviour 122 (2016) 59e66

Delta:1_surname

Delta:1_surname

http://creativecommons.org/licenses/by-nc-nd/4.0/

http://creativecommons.org/licenses/by-nc-nd/4.0/

mailto:marianne.heberlein@ieu.uzh.ch

http://crossmark.crossref.org/dialog/?doi=10.1016/j.anbehav.2016.09.023&domain=pdf

www.sciencedirect.com/science/journal/00033472

http://www.elsevier.com/locate/anbehav

http://dx.doi.org/10.1016/j.anbehav.2016.09.023

http://creativecommons.org/licenses/by-nc-nd/4.0/

http://dx.doi.org/10.1016/j.anbehav.2016.09.023

http://dx.doi.org/10.1016/j.anbehav.2016.09.023

reward location and humans when a desired food item or toy is out
of their reach (Marshall-Pescini, Passalacqua, Barnard, Valsecchi, &
Prato Previde, 2009; Mikl!osi, Pongr!acz, Lakatos, Top!al, & Cs!anyi,
2005; Passalacqua et al., 2011; Vir!anyi, Top!al, Mikl!osi, & Cs!anyi,
2006).

Dogs have also proved to be exceptionally skilled in communi-
cation with humans in several other paradigms, including reading
human communicative gestures such as pointing and gaze cues
(Mikl!osi, Polg!ardi, Top!al, & Cs!anyi, 1998; T!egl!as, Gergely, Kup!an,
Mikl!osi, & Top!al, 2012), or taking humans’ attentional states into
account (G!acsi, Mikl!osi, Varga, Top!al, & Cs!anyi, 2004; Vir!anyi, Top!al,
G!acsi, Mikl!osi, & Cs!anyi, 2004). Dogs were the first animals to be
domesticated, and as such, have shared a common environment
with humans for more than 10 000 years (Freedman et al., 2014;
Pang et al., 2009; Savolainen, Zhang, Luo, Lundeberg, & Leitner,
2002), for a longer time than any other species. Based on these
findings, it has been suggested that the domestication of dogs has
facilitated their cooperation and communication with humans
(Cooper et al., 2003; Hare, Brown, Williamson, & Tomasello, 2002;
Mikl!osi et al., 2003). This hypothesis is supported by comparative
studies showing that, at the age of 3e4 months, dogs outperform
hand-raised wolves in following human pointing in object choice
tasks (G!acsi et al., 2009; Hare & Tomasello, 2005; Mikl!osi et al.,
2003; Mikl!osi, Top!al, & Cs!anyi, 2004; Vir!anyi et al., 2008). At an
adult age, however, hand-raised wolves can also use human-
provided information, showing that domestication might have
affected the speed of development of such skills rather than the
skills themselves (G!acsi et al., 2009; Udell, Dorey, & Wynne, 2008;
Vir!anyi et al., 2008). Therefore, it is crucial to compare wolves and
dogs that are raised and kept under identical conditions in order to
exclude the interpretation that differential experience, rather than
differences in genetic predisposition, explains their behavioural
differences.

Besides the pointing studies, it has been shown that hand-
raised, captive wolves can also adjust their behaviour to the
attentional state of humans to a certain extent, as they beg for food
preferentially from a human who is oriented towards them rather
than from someone whose back is turned to them (Udell, Dorey, &
Wynne, 2011). Moreover, wolves can follow human gaze into
distant space by the age of 14 weeks (Range & Vir!anyi, 2011) and
can find hidden food based on a human demonstration in a local
enhancement task (Range & Vir!anyi, 2013). Therefore, it seems that
wolves have the necessary social attentiveness and can (or at least
can learn to) benefit from information provided by humans (Range
& Vir!anyi, 2015). Accordingly, since extensive individual socializ-
ation by humans seems to lead to social competences in wolves
comparable to those of dogs, it is difficult to assess whether and in
what way domestication has impacted these skills in dogs. Even
less is known about the origins of dogehuman communication in
the opposite direction: when dogs/wolves provide information to
humans, for example, during ‘showing’.

Mikl!osi, Polg!ardi, Top!al, and Cs!anyi (2000) defined ‘showing’ as
a communicative behaviour consisting of a directional component
referring to an external target and an attention-getting component
that attracts the receiver’s attention to the sender. In their experi-
ment, the behaviour of the dogs was recorded after they had
observed the hiding of a piece of food or a favourite toy in a place
that they could not access themselves. Mikl!osi et al. (2000) found
that after the hiding, when both reward and owner were present at
the same time the dogs looked more frequently at their owner and
the baited location than when only the hidden target or the owner
was in the room. Importantly, gaze alternation between the target
location and owner occurred only when both the reward and the
owner were present. Nor did the dogs show gaze alternation be-
tween an empty food location and the owner, or between the door

(through which the owner had left) and the target location.
Consequently, Mikl!osi et al. (2000) argued that dogs, similarly to
other animal species, might be able to engage in functionally
referential communication. It can still be questioned, however, to
what extent the sophisticated use of gaze alternation and other
showing behaviours reflects the association that dogs (and poten-
tially human-raised wolves) have formed during life-long experi-
ences involving food and their owners, for example, a dog may have
the learned expectation that if food is out of reach the human
present will give it to the dog. In order to exclude this simple
explanation, we improved the showing paradigm by testing the
animals with two familiar partners playing either a cooperative or a
competitive role during the experiment. If showing behaviours
reflect the communicative intention of the subjects, they should
occur more often with the cooperative partner than with the
competitive one, despite the fact that both partners have regularly
worked with the subjects and are therefore already associated with
donating food to a similar extent before the test starts.

To date, only one study has addressed the question of whether
wolves show humans where an out-of-reach food item can be
found. Kubinyi, Vir!anyi, and Mikl!osi (2007) mentioned an unpub-
lished study by Vir!anyi, Gasci et al. (2006), Vir!anyi, Topal et al.
(2006) comparing the showing behaviour of 1-year-old wolves
and dogs using the paradigm developed by Mikl!osi et al. (2000).
They reported that both wolves and dogs indicated a food location
to a human partner by alternating their gaze between the food
location and the human. However, the wolves did so less often than
the dogs. These results may suggest that domestication has facili-
tated the development of this kind of communication with a hu-
man partner in dogs. Alternatively, however, in this previous study
the dogs and wolves might have gathered different experiences
with humans in such situations by the age of testing (1 year), since
the dogs were kept as pets whereas the wolves, at the age of 2e4
months, were moved back to the farm where they were born.
Therefore, currently no data are available that compare the
showing behaviour of dogs and wolves raised and kept under
identical conditions.

Using a modified version of Mikl!osi et al. (2000) paradigm in the
present study, we investigated whether identically raised and kept
adult wolves and dogs exhibit similar showing behaviour in the
presence of food and a human. Importantly, we compared whether
wolves and dogs differentiated between a cooperative and a
competitive human partner in their showing behaviour in order to
exclude the interpretation that their behaviour reflects a general
foodehuman association. The domestication hypothesis as out-
lined above would suggest that dogs outperform wolves. Alterna-
tively, however, we may hypothesize that wolves have the
necessary social attentiveness and can therefore communicate with
humans in a similar way to dogs if they are raised and kept close to
humans, predicting that wolves and dogs perform in a similar way.

METHODS

We tested 13 (male/female: 7/6) adult dogs and eight (male/
female: 5/3) adult timber wolves in this experiment. The subjects
were between 1.5 and 3.5 years of age when being tested (dogs:
mean ¼ 2.35 years; wolves: mean ¼ 2.33 years). All subjects that
participated in this study were born in captive facilities (all the dogs
arrived from four different shelters in Hungary, three wolves came
from a zoo in Austria, one from Switzerland and four from the
U.S.A.). All dog and wolf puppies were separated from their
mothers within the first 10 days of life and were hand-raised and
socialized in the same way at the Wolf Science Center (WSC). For
details see Range and Vir!anyi (2014). The subjects grew up in peer
groups with 20e24 h of daily contact with humans in their first 5

M. T. E. Heberlein et al. / Animal Behaviour 122 (2016) 59e6660

months, when they were then introduced to packs of older animals
(founded by four dogs and three wolves, respectively). At the time
of this study, the dogs lived in four packs, and the wolves in two
different packs, in large enclosures (2000e8000 m2) at the Game
Park Ernstbrunn, Austria, where they remained after participating
in this study. According to their dietary needs, the dogs were fed
every day with dry food or meat mixed with dry food, while the
wolves were fed every third day with carcasses. Water was avail-
able for all subjects ad libitum. Since puppyhood, all subjects had
participated regularly in different cognitive behavioural tests and
had been trained on a daily basis. The training consisted of obedi-
ence training, including commands such as sit, down, roll over, or
touch, and was conducted either in the test building or in the test
enclosure in physical separation from the pack. Accordingly, the
subjects were used to being separated from their pack to work with
familiar humans.

General Experimental Set-up

The experiment took place at the Wolf Science Center in a large
test room (9 ” 5.37 m and 2.56 m high at the lowest point). On
three sides of the test room three boxes (plastic flower pots, 10 cm
in diameter) were hanging on a chain from the ceiling close to the
wall. The boxes served as hiding places during the experiment. The
chain was used to adjust the height of the boxes so that the humans
could take out a piece of food and the wolves were unable to reach
them when jumping up. To ensure a relaxed test environment,
three persons who were familiar to the wolves and dogs were
involved in this experiment (hand raisers or trainers with almost
daily contact, who had regularly rewarded them with food during
various interactions and tasks). The experimenter hid the food for
the subjects. The other two persons were assigned the roles of
‘cooperative partner’, who always rewarded the subjects, and
‘competitive partner’, who always ate the food herself/himself.

The whole experiment extended over at least 3 days (Fig. 1). On
the first day, each animal started with a prefeeding session fol-
lowed by its first training session. After a break of at least 3 min a
second training session was conducted, followed by a preference
test in order to check whether the subjects differentiated between
the cooperative and competitive partners. On the second day, each
subject again had a prefeeding session, followed by a training
session and a preference test. If in the preference test a subject
reached the criterion of choosing the cooperative partner in at least
three out of four trials, the animal received its first test session.
Subjects that did not reach that criterion in the preference test

received an additional preference test after a break of at least 3 min.
If the subject still did not reach the criterion, the procedure of the
second day was repeated, after a break of at least 24 h. On the third
test day, when an animal had been successful on day 2, it started
again with a preference test, in which it had to reach the same
criterion, followed by a second test session. In cases where an an-
imal did not reach the criterion in the preference test, that animal
repeated the third day after a break of at least 24 h. (Details of the
prefeeding, training, preference test and test sessions are given
below.) Between the training and test sessions, all three humans
involved in the test went on working with the subjects in accor-
dance with the every day routines of the WSC, that is, regardless of
their role in the experiment. Therefore, outside the test situation
the humans were all associated with food to a similar extent.

Prefeeding
The prefeeding phase aimed at teaching the subjects that the

three boxes could contain food and that humans (exemplified by
the experimenter) could provide them with this out-of-reach
reward. All subjects already had experience with this procedure
since they had participated in another test using the same equip-
ment and baiting procedure. During the prefeeding, the experi-
menter first showed a piece of sausage to the animal and then put it
into one of the boxes, while making sure that the animal paid
attention to the hiding procedure by calling the animal’s name if it
did not watch what she was doing. Then she baited the second and
third boxes in the same way. The order of baiting the boxes was
randomized across subjects and within subjects and across trials.
After the baiting, the experimenter stood in the middle of the test
room and addressed the animal, asking it to show her the food. If
the animal looked at any of the boxes, the experimenter went there
and rewarded the animal with its content. Then she addressed the
animal again until all three boxes were empty. If the animal looked
at an empty food location the experimenter verbally responded
that the food location was empty without approaching the box, and
asked the animal to show another one. If, however, an animal
insisted and repeatedly indicated the same empty food location, the
experimenter went there and presented the empty box to the an-
imal by showing an empty hand after reaching into the box. If an
animal did not look at the boxes when being asked, the experi-
menter approached a box randomly and touched the box waiting
until the animal looked at it. Then she provided the reward.

Training
The prefeeding phase was followed by a training session on both

days 1 and 2, in which the subjects were introduced to the roles of
the other two humans participating in this test. In the case of the
wolves, two female humans played these roles, while in the case of
the dogs, a female and a male took them on. These two human
partners had been chosen so that they were of similar age, and had
both worked with the animal in the same situations to the same
intensity and thus had a similar relationship with it. One of the two
persons was assigned the role of the cooperative partner who al-
ways rewarded the subjects, whereas the other one, the competi-
tive partner, always ate the food herself/himself. The role
assignment to one person or the other was semirandomized so that
a certain person was the cooperative partner for half of the male
and half of the female subjects, while for the other half that person
was the competitive partner.

During the training, the subjects were held on a leash by the
experimenter on one side of the test room. Approximately 3 m
away from the animal, a bowl with six pieces of sausage was placed
in the middle of the test room. On the opposite side of the bowl, in
the two corners of the test room, the two partners were waiting
(their positions were counterbalanced across subjects). In a

Day 1 Day 2 Day 3

Prefeeding Prefeeding
Preference test (test
criterion: 3 out of 4

)

Training (3 × 2)

Test (2 × 2)

Training (3 × 2)
Test (2 × 2)

Break (at least 3 min)

Training (3 × 2)

Preference test

Preference test (test
criterion: 3 out of 4)

Figure 1. Experimental procedure.

M. T. E. Heberlein et al. / Animal Behaviour 122 (2016) 59e66 61

predetermined order, the two partners went to the bowl three
times each, called the animal’s name, took a piece of sausage out,
and either ate it or gave it to the animal. For half of the subjects, the
cooperative partner started; for the others, the competitive partner
approached the bowl first. The cooperative partner always went to
the subject, holding the sausage in her/his hand and offered it to the
animal. The competitive partner, however, demonstratively ate the
sausage, making sure that the animal observed the action, then
went to the animal and presented her/his empty hand. In this way,
both partners appeared and could be associated with food to the
same extent.

Preference test
The preference test was conducted to assess whether the ani-

mals learned the role of the two partners in a context different from
our showing test. During the preference test, the subject was held
by the experimenter by its collar on one side of the test room, while
on the opposite side the two partners were waiting 3 m apart, at an
equal distance (4e5 m) from the animal. Both partners presented
simultaneously a piece of sausage on their open palm to the animal.
At that moment the experimenter released the subject to make a
choice. If it went to the cooperative partner, it was allowed to eat
the sausage; but if it went to the competitive partner, the person ate
the sausage herself/himself just before the subject would have
reached it. After each choice, the experimenter called the subject
back. A total of four trials were conducted. The positions of the
cooperative and competitive partners were predetermined and
semirandomized with the stipulation that neither of them
remained on the same side more than twice in a row.

Test
While the two partners were absent, the experimenter pre-

sented a piece of sausage to the subject and hid it in one of the
three potential food locations. Subsequently, she left the test
room through the door, behind which the two partners were
waiting (Fig. 2). Afterwards, one of the two partners, who did not
know in which of the three boxes the experimenter had hidden
the food, entered, closed the door and sat down on a chair
equidistant to the three hiding places. The partner was passive
but observed the subject attentively for 1 min. After this, she/he
stood up and went to the box that she/he thought the subject had
indicated during that minute. If she/he found the sausage and
was the cooperative partner, she/he gave it to the subject; if she/
he was the competitive partner, she/he ate the sausage. If the
subject had indicated an empty box, the partner showed the

empty box after checking it. Following this, the partner left the
test room. The subjects were tested twice with the cooperative
partner and twice with the competitive partner, with the stipu-
lation that the same partner did not show up consecutively in the
first two trials.

Behavioural Coding

The experiment was videotaped with a digital video camera
(Sony HDR-CX320). From the video recordings of the test sessions,
during the 1 min when the partner was passive, we analysed how
often a subject looked at the food location or at an empty box, for
how long and how often it watched the human partner, how often a
subject went to a human partner and for how long it was in close
proximity to her/him (within reaching distance of the partner’s
hand). Furthermore, we counted how often gaze alternation
occurred between one of the boxes and the partner. Gaze alterna-
tion was defined as looking at the partner’s face and then directly
(continuous head movement without interruption) to one of the
boxes or vice versa. Additionally, we analysed other showing be-
haviours including: (1) going to the partner (close proximity) and
looking at her/him, followed by going to one of the three boxes and
looking at it; (2) going to the partner (close proximity), touching
her/him with the nose or looking at her/him (not necessarily with
eye contact) and then looking at one of the three boxes; (3) looking
at the partner (into the face from any distance) and then going to
one of the boxes and looking at that.

For the statistical analysis we pooled these behaviours with gaze
alternations. These results are reported as ‘showing behaviours’.

Of the videos, 27% were analysed by a second coder who was
blind to the test condition, the hiding location and the purpose of
the test, and interobserver reliability was tested by calculating
Spearman’s rank correlations. Correlations (rho) were generally
high: frequency looking at partner: 0.81; time looking at partner:
0.75; frequency of looking at the food location: 0.81; frequency of
looking at an empty location: 0.78; frequency of going to the hu-
man partner: 0.80; time spent in close proximity to human part-
ner: 0.76; showing behaviour: food location: 0.75; empty location:
0.75.

Statistical Analysis

We calculated generalized linear mixed-effects models to
investigate the influence of the cooperativeness of the partner,
species, test day and the sex of the test subject on the occurrence
and frequency of different behaviours. The individual and the trial
were included in the model as random factors. For analyses of
whether or not showing behaviour occurred, a model with
binomial distributions was calculated. For analyses of the fre-
quencies, models with Poisson distributions were used. Durations
were analysed with a linear mixed-effect model using the same
fixed and random factors as described above. To get a normal
distribution of the residuals, we used a square-root trans-
formation for the duration of looking at the partner and a log
transformation for the duration of being in close proximity to the
partner. The analyses were done with the program R 2.15.2 (R
Core Team, 2012).

Ethical Note

No special permission for use of subjects (wolves and dogs) in
such sociocognitive studies is required in Austria (Tierversuchsge-
setz 2012 e TVG 2012). The relevant committee that allows
research without special permissions regarding animals is the

D

5
.3

7
m

9 m

Figure 2. Outline of the test room. The potential food locations hanging from the
ceiling are marked with stars, and the circle marks the position of a chair. The humans
enter and leave the room through a door (D).

M. T. E. Heberlein et al. / Animal Behaviour 122 (2016) 59e6662

Tierversuchskommission am Bundesministerium für Wissenschaft
und Forschung (Austria).

RESULTS

Showing Behaviour

The likelihood that a subject showed the food location to the
human partner during the test was influenced by the role of the
partner (GLMM: F1,141 ¼7.730, P ¼ 0.006) with more subjects
showing the food location to the cooperative than to the compet-
itive partner (Fig. 3). This result was the same for both species
(GLMM: species)partner: F1,139 ¼ 1.42, P ¼ 0.24), and this differ-
ence was obvious on both test days (GLMM: partner)test day:
F1,140 ¼ 1.85, P ¼ 0.18). Still, overall the subjects were more likely to
indicate the food location during the first than during the second
day (GLMM: F1,144 ¼ 9.350, P ¼ 0.003). Furthermore, in general, the
likelihood of showing the food location to the human partner, in-
dependent of her/his cooperativeness, was not influenced by sex or
species (GLMM: sex: F1,18 ¼ 0.37, P ¼ 0.55; species: F1,19 ¼ 0.59,
P ¼ 0.45). The likelihood that a subject indicated an empty food
location was not affected by the partner’s role (GLMM: F1,143 ¼ 0.68,
P ¼ 0.40) or by species, test day, or sex (GLMM: species: F1,19 ¼ 0.90,
P ¼ 0.40; day: F1,145 ¼ 1.82, P ¼ 0.20; sex: F1,18 ¼ 1.13, P ¼ 0.30).

Looking at a Potential Food Location

Analysing the number of looks to the location where the food
was hidden, we found that the subjects looked more often at the
food location on the first test day than on the second (GLMM:
F1,144 ¼ 5.850, P ¼ 0.020). Furthermore, we found a tendency for a
difference between wolves and dogs (GLMM: F1,19 ¼ 4.130,
P ¼ 0.060) with wolves looking more often at the food location than
the dogs. However, we found no influence of the role of the partner
present during the test (GLMM: F1,143 ¼ 0.79, P ¼ 0.38), and this did
not differ between the two species (GLMM: species)partner:
F1,142 ¼ 2.51, P ¼ 0.12), or test days (GLMM: day)partner:
F1,141 ¼ 0.43, P ¼ 0.51). Furthermore, sex of the subjects did not
influence the number of looks to the food location (GLMM:
F1,18 ¼ 0.31, P ¼ 0.58).

When analysing the number of looks to an empty food location,
we found a species difference (GLMM: F1,19 ¼ 5.250, P ¼ 0.030),
whereby wolves looked more often at an empty food location than
dogs. However, the role of the human partner did not influence this
behaviour (GLMM: partner: F1,143 ¼ 0.02, P ¼ 0.90), either in wolves

or in dogs (GLMM: partner)species: F1,142 ¼ 1.20, P ¼ 0.27).
Furthermore, for both wolves and dogs, we found a tendency to
look more often at an empty food location during the first than
during the second test day (GLMM: F1,145 ¼ 3.240, P ¼ 0.070), but
we found no influence of sex of the subject (GLMM: F1,18 ¼ 0.09,
P ¼ 0.77).

In line with the previous results, wolves in general looked more
often at any potential food location than dogs (GLMM: F1,19 ¼ 7.010,
P ¼ 0.016), and all subjects did so more on the first than on the
second test day (GLMM: F1,144 ¼ 9.390, P ¼ 0.003). However, we
found no influence of sex of subject or partner present on the fre-
quency of looking at a potential food location (GLMM: human
partner: F1,143 ¼ 0.52, P ¼ 0.47; sex: F1,18 ¼ 0.29, P ¼ 0.60).

Contact with Human Partner

Regarding contact with the human partners, we found that the
dogs looked more often, and for longer, at the human’s face than
the wolves (frequency: GLMM: F1,19 ¼ 4.670, P ¼ 0.040; duration:
LME: F1,19 ¼ 10.300, P ¼ 0.005) and the dogs also went more often
to their human partner than the wolves (GLMM: F1,18 ¼ 15.800,
P < 0.001). However, we found no influence of the role of the partner, sex of subject or test day on any of these variables (fre- quency of looking at human: frequency: GLMM: partner: F1,143 ¼ 0.37, P ¼ 0.54; sex: F1,18 ¼ 2.75, P ¼ 0.11; test day: F1,144 ¼ 2.51, P ¼ 0.12; duration of looking at human: LME: partner: F1,141 ¼ 2.96, P ¼ 0.09; sex: F1,18 ¼ 1.84, P ¼ 0.19; test day: F1,143 ¼ 2.08, P ¼ 0.15; going to partner: GLMM: partner: F1,140 ¼ 1.85, P ¼ 0.20; test day: F1,2 ¼ 0.13, P ¼ 0.80; sex: F1,17 ¼ 2.45, P ¼ 0.10).

Moreover, analysing how long a subject was in close contact
with the human partner (if this behaviour occurred), we found an
interaction between species and partner (LME: F1,92 ¼ 4.220,
P ¼ 0.040; Fig. 4). When the cooperative partner was present, we
found no difference between wolves and dogs (LME: F1,23 ¼ 1.92,
P ¼ 0.20). However, when tested with the competitive partner,
wolves spent less time with the human than dogs did (LME:
F1,17 ¼ 5.510, P ¼ 0.030). Neither test day nor sex of subject influ-
enced the time the subject spent next to the human partner (LME:
test day: F1,2 ¼ 0.21, P ¼ 0.69; sex: F1,15 ¼ 1.97, P ¼ 0.18).

Pe
rc

en
ta

ge
o

f i
nd

iv
id

ua
ls

e
xp

re
ss

in
g

sh
ow

in
g

be
ha

vi
ou

r (
%

)

7

0

60

50

40

30

20

10

0

Dog Wolf

Competitive
Cooperative

Figure 3. Percentage of subjects engaging in showing behaviour in the presence of the
cooperative and the competitive partner.

50
40
30
20
10
0
Competitive
Cooperative

D
u

ra
ti

o
n

i
n

c
lo

se
c

o
n

ta
ct

w
it

h
h

u
m

an
p

ar
tn

er
(

s)

Dog Wolf

Figure 4. Time the subjects spent in close proximity to the human partner, if they did
so. The top, middle and lower horizontal lines show the 75th, 50th and 25th per-
centiles, respectively. The whiskers mark the main body of the data, and the circles the
outliers.

M. T. E. Heberlein et al. / Animal Behaviour 122 (2016) 59e66 63

DISCUSSION

Our results demonstrate that the showing behaviour to human
partners of both wolves and dogs was very similar. Dogs and wolves
not only showed the food location to their human partners similarly
often but they also adjusted their showing behaviour to the coop-
erativeness of their human partner to the same degree from the
first test day, in being more likely to show the food location in the
presence of the cooperative partner than in the presence of the
competitive partner. Importantly, wolves and dogs differentiated
between the two different partners only in their showing behav-
iour but not in the likelihood of simply looking at a food or empty
location.

Vir!anyi, Gasci et al. (2006), Vir!anyi, Topal et al. (2006) showed
that wolves indicate a food location in a similar paradigm, but they
found that wolves did so less than dogs. The difference between the
two studies seems to result from the different performance of the
dogs tested in the two studies. In our study all subjects were hand-
raised, and therefore intensively socialized with humans but the
dogs as well as the wolves were integrated into packs at the age of
4e5 months, where they mainly interacted with conspecifics. In
contrast, in the previous study, while the wolves were integrated
into packs at the age of 2e4 months, the dogs were kept as pets
until the study was conducted at the age of 1 year. Interestingly, our
pack dogs showed fewer gaze alternations and other food-
indicating signals than pet dogs that had been tested with the
same set-up by the same experimenter (Heberlein, Turner, &
Vir!anyi, 2016). This difference is comparable to the difference be-
tween the wolves and dogs described by Vir!anyi, Gasci et al. (2006),
Vir!anyi, Topal et al. (2006); see Kubinyi et al. (2007), suggesting
that the differences in showing behaviour between wolves and
dogs may not originate from domestication but rather from their
different experiences, which seem to affect the showing behaviour
of dogs in a similar way.

Dogs and wolves adjusted their showing behaviour to the
cooperativeness of the partner, with more food-indicating signals
in the presence of the cooperative partner than with the compet-
itive partner. Differentiating between cooperative and competitive
individuals has been demonstrated also in ravens, Corvus corax,
where the birds adjusted their caching behaviour to their previous
experiences with the human participants and prevented only the
competitive human from finding their caches (Bugnyar, Schwab,
Schloegl, Kotrschal, & Heinrich, 2007). Importantly, however, only
the showing behaviour of the subjects was adjusted to the role of
the human partner; looking at the food location (without looking at
or contacting the partner) did not depend on the cooperativeness of
the human partner. The same results have been found in pet dogs,
where it is argued that looking at the food location in itself is not a
signal intended to communicate the food location to the human
partner (Heberlein et al., 2016).

Both human partners had a similar relationship with the sub-
jects and were associated to a similar extent with food before the
experiment started. Moreover, outside the test situation both
partners continued to reward the subjects to a similar extent. Only
in the context of the experiment did the subjects experience that
one person (the cooperative partner) gave them food, while the
other person (the competitive partner) ate the food herself/himself.
During the training this included getting food ‘for free’ from the
cooperative partner, while during the preference test the subjects
got the food when choosing to go to the cooperative partner but not
when going to the competitive one. Therefore, the subjects might
have associated food with the cooperative partner more than with
the competitive partner, but we can exclude that a food association
with the two partners was learned in the context of showing
behaviour. Except during prefeeding, showing behaviour itself was

not specifically reinforced during any step of the experiment.
Importantly, during prefeeding a third person, who was not one of
the later partners, reinforced the subjects’ behaviour, looking at the
food location (not necessarily showing, but this might be involved).
Therefore, the subjects might have learned to associate getting food
with looking at the food location, and showing the location to a
human partner, but this learning process was not linked to either of
their two later partners. During the actual test, if an animal engaged
in showing behaviour right before the test was over, the coopera-
tive partner would have rewarded it some seconds later, which
might have allowed reinforcement of showing behaviour and
consequent associative learning. The chance of such reinforcement,
however, was low since in most cases the animals indicated the
food location near the beginning of the test. Even if associative
learning had influenced the occurrence of showing behaviour, it
could not fully explain the observed differentiation between the
two partners, since the animals differentiated between them from
the beginning onwards and therefore proved to be flexible in the
use of showing behaviour. However, this flexibility was somewhat
limited in comparison to that of pet dogs tested in the same way,
which not only showed a food location more often to the cooper-
ative partner than to the competitive partner, but also showed an
empty food location more often to the competitive than to the
cooperative partner, in a way that could mislead the competitive
partner searching for the food. In the current experiment, we found
no such misleading behaviours, either in the dogs or in the wolves.
This difference between the two studies can potentially be
explained by the fact that we tested the wolves and dogs with two
familiar humans who had close working relationships with the
subjects, while in the pet dog study either two completely unfa-
miliar persons were used or a somewhat familiar person (known
from joint walks) played the role of the competitive partner and an
unfamiliar one was the cooperative partner. The lack of a working
relationship between the competitive partner and the pet dogs may
explain the higher propensity to show an empty food location. Such
active interactions have also been found to influence other be-
haviours (e.g. attention) of dogs towards familiar persons (Horn,
Range, & Huber, 2013).

While in this study the showing behaviour of dogs and wolves
was rather comparable, we also found some characteristic differ-
ences in the behaviour of the two species. First of all, independent
of the human partner present, the wolves looked more often at the
three food hiding places than the dogs, whereas the dogs looked at
the humans and approached them more often than the wolves. This
might reflect a higher food motivation in wolves than in dogs.
Mikl!osi et al. (2003) proposed that higher attraction of wolves to
food resources may also partly explain why wolves look at their
human partners later and less often in an unsolvable task than dogs.
Independently from this difference, both wolves and dogs looked
more often at any food location and displayed more showing
behaviour on the first test day than on the second. This might
indicate that the general arousal and/or motivation of the subjects
induced by the novel test situation decreased from the first to the
second test day. One reason for this might be that the subjects did
not get rewarded immediately when indicating a food location but
had to wait for a minute for the human partner to stand up and to
go to one of the food hiding places. Alternatively, we can exclude a
bad representation of the food location, since they are precise in
their showing behaviour. Furthermore, Fiset and Plourde (2013)
showed that dogs as well as grey wolves understand object
permanence at least in a visual displacement task.

In addition to their different food motivation, the different ga-
zing pattern of dogs and wolves (the dogs focusing less on food
locations but more on humans than the wolves) could also reflect a
difference in their human-directed behaviour. Mikl!osi et al. (2003,

M. T. E. Heberlein et al. / Animal Behaviour 122 (2016) 59e6664

2005) suggested that dogs might have been selected for higher
dependency on humans and, in particular, to look into their faces
more often in comparison to wolves, which allows for better
communication (Mikl!osi et al., 2003). This explanation is supported
by findings indicating that dogs remain attached to their owners
longer than wolves, who may have such a close bond to their hu-
man caretaker only at very young ages even after extensive human
socialization (Hall, Lord, Arnold, Wynne, & Udell, 2015; Top!al et al.,
2005). Top!al et al. (2005) found that young dogs but not young
wolves showed a preference for their owner over an unfamiliar
human, which does not imply, however, that the wolves do not
recognize their human caregivers. In contrast, Kubinyi et al. (2007)
described that in their greeting behaviour wolves show a prefer-
ence for their human raisers even in comparison to other familiar
humans. Rather, it has been argued that the preference of dogs for
their owner in the attachment study reflects a dependent rela-
tionship with her/him which has been suggested to be similar to
the mothereinfant bond in humans (Prato Previde, Custance,
Spiezio, & Sabatini, 2003; Top!al et al., 2005; Top!al, Mikl!osi,
Cs!anyi, & D!oka, 1998). Since the subjects had a close relationship
with both the cooperative and the competitive partner, the higher
dependency of dogs on them may also explain why in our experi-
ment the dogs not only looked at their human partners more often
than the wolves but also went to them more often and were less
discriminative regarding with whom they stayed in contact. The
wolves stayed for a shorter duration in close proximity to the
competitive partner than the dogs, whose lower selectivity may
indicate a stronger influence of their long-term relationship with
their trainer in comparison to wolves.

To sum up, in spite of potentially higher food motivation in
wolves and higher dependency on humans in dogs, both dogs and
wolves engage in showing behaviour to indicate a food location to a
cooperative but not to a competitive human partner. Based on this
flexibility, dogs as well as wolves appear to be able to engage in
functionally referential communication with humans. Importantly,
dogs and wolves raised under the same conditions and kept simi-
larly in packs in a game park setting do not differ in their showing
behaviour; but both use such behaviours less often than pet dogs
living in human families, suggesting that closeness to humans and
different experiences with them can strongly influence the
showing behaviour of dogs. Further research has to investigate
whether wolves with even more experience would communicate a
food location to their human partners as intensively as pet dogs if
they lived similarly close to humans.

Acknowledgments

We thank Marta Manser for her help, discussions and sugges-
tions for the manuscript. Furthermore, we thank all Wolf Science
Center team members for their help in conducting the experiments.
We also thank Linda Lüthi for coding videos for the interobserver
reliability test. F. R. was financially supported by Austrian Science
Fund (FWF) project P21244-B17 and project P24840, and by the
European Research Council under the European Union’s Seventh
Framework Programme (FP/2007-2013)/ERC Grant Agreement n.
[311870]’, while Z. V. has been funded by the Vienna Science and
Technology Fund (WWTF) through project CS11-026. We further
thank many private sponsors including Royal Canin for financial
support and the Game Park Ernstbrunn for hosting the Wolf Science
Center.

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• A comparison between wolves, Canis lupus, and dogs, Canis familiaris, in showing behaviour towards humans

Methods
General Experimental Set-up
Prefeeding
Training
Preference test
Test
Behavioural Coding
Statistical Analysis
Ethical Note
Results
Showing Behaviour
Looking at a Potential Food Location
Contact with Human Partner
Discussion
Acknowledgments
References