Applied Animal Behaviour Science 81 (2003) 229–244
Clever hounds: social cognition in the
domestic dog (Canis familiaris)
Jonathan J. Cooper*, Clare Ashton, Sarah Bishop,
Rebecca West, Daniel S. Mills, Robert J. Young1
Animal Behaviour, Cognition and Welfare Research Group, Department of Biological Sciences,
University of Lincoln, Riseholme Park, Riseholme, Lincoln LN2 2LG, UK
Abstract
This paper reviews the reasons why domestic dogs make good models to investigate cognitive
processes related to social living and describes experimental approaches that can be adopted to
investigate such processes in dogs. Domestic dogs are suitable models for investigating social
cognition skills for three broad reasons. First, dogs originated from wolves, social animals that
engage in a number of co-operative behaviours, such as hunting and that may have evolved cognitive
abilities that help them predict and interpret the actions of other animals. Second, during domestication dogs are likely to have been selected for mental adaptations for their roles in human society
such as herding or companionship. Third, domestic dogs live in a human world and ‘‘enculturation’’
may facilitate the development of relevant mental skills in dogs. Studies of social cognition in
animals commonly use experimental paradigms originally developed for pre-verbal human infants.
Preferential gaze, for example, can be used as a measure of attention or ‘‘surprise’’ in studies using
expectancy violation. This approach has been used to demonstrate simple numerical competence in
dogs. Dogs also readily use both conspecific and human social signals (e.g. looking or pointing) as
information sources to locate hidden rewards such as food or favourite toys. Such abilities make dogs
particularly good models for investigating perspective-taking tasks, where animals are required to
discriminate between apparently knowledgeable and apparently ignorant informants.
# 2003 Elsevier Science B.V. All rights reserved.
Keywords: Domestic dog; Canine; Social cognition; Counting; Theory of mind; Perspective taking
*
Corresponding author.
E-mail address: jcooper@lincoln.ac.uk (J.J. Cooper).
URL: http://www.lincoln.ac.uk/lsa/staffcvs/jjcooper.htm
1
Present address: Department of Post-Graduate Studies in Zoology, Pontifı́cia Universidade Católica de
Minas Gerais, Av. Dom José Gaspar 500, Coração Eucarı́stico, 30535-610 Belo Horizonte, Minas Gerais, Brazil.
0168-1591/03/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved.
doi:10.1016/S0168-1591(02)00284-8
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1. Introduction: the study of social cognition
The contemporary experimental paradigms used for the study of social cognition and its
relationship with animal behaviour can be traced to the work of Humphrey (1976) and
Premack and Woodruff (1978). In ‘‘The social function of intellect’’, Humphrey argued that
the primary driving forces in the evolution of human intelligence were those challenges
related to the social environment, and in particular, interaction with individuals of the same
species rather than those associated with the physical environment. This argument extends to
the evolution of animal cognition, since the social environment contains more complex
challenges than the physical environment and, consequently, highly social animals are likely
to have evolved mental processing abilities to help them predict and exploit the actions of
others (Byrne and Whiten, 1990; Dunbar, 1992). Premack and Woodruff (1978) discussed
‘‘theory of mind’’ or the attribution of mental states (such as beliefs or desires) to others. They
described this mental ability as both a mechanism for animals to predict the actions of others
and a means for cognitive scientists to investigate cognitive processes in non-human animals.
The ability to take the perspective of others has recently received much interest amongst
comparative and evolutionary psychologists and applied to deceit and exploitation or
‘‘Machiavellian Intelligence’’ (Byrne and Whiten, 1988; Whiten and Byrne, 1997) as well
as co-operation in social animals. Byrne and Whiten (1988) report that, after primates, dogs
are the most commonly reported species to engage in apparent tactical deception. The study
of social cognition is not, however, limited to interpreting and understanding the actions of
others and a wide range of mental representational abilities which would be useful to social
animals, are known to have evolved in humans and may have evolved in other social species.
These include: the ability to count or numerical competence; certain forms of social learning;
and the communication of abstract information between individuals through language.
Studies of social cognition have tended to concentrate on humans and closely related
non-human primates (e.g. Povinelli et al., 1997; Heyes, 1998; Call and Tomasello, 1999).
However, if social intelligence has functional benefits to social animals then it seems
reasonable to postulate their existence in a wider range of species (Held et al., 2001a).
2. Development of social skills in the dog
Broadly, there are three reasons why we might predict that domestic dogs possess the
capacity for social cognitive skills. First, they originate from wolves, a species that forms
stable social bands and engages in co-operative behaviour such as hunting (Mech, 1970;
Frank, 1980); second, because some individuals may have been selected for such abilities
during domestication and breed selection (Coppinger and Coppinger, 2001); and third,
because they commonly live in a human social environment that may facilitate the
development of such skills.
2.1. Ancestral influences from the wolf
There has been considerable debate amongst anthropologists and biologists about the
ancestry of the domestic dog and the process of its domestication, though it is generally
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231
accepted that the majority of dogs evolved from wolves (Canis lupis); albeit over different
time periods across the world and involving a number of sub-species of wolf (Fox, 1978;
Clutton-Brock, 1995; Vila et al., 1997). Wolves commonly live in tightly knit groups or
packs, consisting of related individuals of varying age, and with clear dominance
hierarchies amongst males and females (Mech, 1970). Packs engage in co-operative
hunting, involving the co-ordinated tracking, chasing, catching and killing of prey (Mech,
1970; Fox, 1971). Wolves may, therefore, benefit functionally from the ability to predict
the behaviour of other wolves or their prey (Frank and Frank, 1982; Gagnon and Dore,
1994). The wolf also forms strong stable bonds between individuals and therefore
meets another important criterion underlying the selective advantage of social cognitive
skills. The majority of species, in which some form of social cognition has been claimed
form relatively long-lived stable social groups. These include humans and other apes
(e.g. Povinelli et al., 1990; Tomasello et al., 1997), dolphins (e.g. Tschudin, 2001), parrots
(Pepperberg, 1994) and pigs (Held et al., 2000, 2001b).
2.2. Effects of domestication and breed diversification
Domestic dogs have undergone two selective processes related to their association with
human societies. The first is domestication, which involves biological and cultural changes
in both the domestic animal and the domesticators (Clutton-Brock, 1995). The second is
breed diversification where dogs have been selected for specific traits to suit specific roles
in human society (Coppinger and Schneider, 1995). Both these processes may have
involved selection for social intelligence (by accident or design) in dogs.
A process commonly seen in domesticated species is neotenisation, which means the
process whereby juvenile characteristics are retained into adulthood. It has been suggested
that this is a general effect of domestication (Fox, 1968), since sub-adults exhibit greater
behavioural plasticity and may be more manageable as a result in the domestic environment (Hediger, 1938). The mechanism by which neotenisation is achieved is uncertain
(Price, 1984), but there is evidence for its occurrence in the dog at both the physical and
behavioural level (Ginsburg and Schotte, 1978; Frank and Frank, 1982; Coppinger and
Coppinger, 2001). It has also been suggested that humans exhibit many features comparable to a neotenised wild ape species (Bolk, 1926) and Gould (1978) has argued that this
may be adaptive for humans by increasing their capacity to learn. Thus, it may be that
through neoteny both humans and dogs retain and develop a range of cognitive processes
into adulthood, which are not retained in their phylogenetic relatives.
Frank (1980) has argued that the domestication of the dog has selected against cognitive
processes, which may exist in the wolf. Experimental support for this is weak, as it is based
on limited samples with different developmental backgrounds. Behavioural changes are
notoriously difficult to track over evolutionary time-scales as they leave little direct
evidence in the form of fossil records. Behavioural changes may nevertheless be inferred
from changes in anatomical features such as the skull. Domestic dogs have a smaller
cranial capacity and consequently smaller brain size than the wolf (Wayne, 1986;
Coppinger and Schneider, 1995), which would appear to support Frank’s hypothesis. A
smaller brain does not, however, necessarily preclude cognitive abilities in animals and the
social aspects of cognition in mammals are more closely related to the size and complexity
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of the neocortex size rather than whole brain size (Kruska, 1988; Dunbar, 1992). Wolves
have a relatively large neocortex, which in carnivores is only exceeded by lions and hyenas
(Dunbar and Bever, 1998) and thus have a large area of the brain devoted to processing
cognitive information. No such comparative data have, however, been calculated for dogs,
either using fossil records, or comparing breeds and it would be worthwhile to do so to
relate changes in brain size during domestication and breed selection to the changing roles
of dogs in human society.
In addition to indirect selection, there may have been direct selection for social skills to
suit the needs of people and dogs, such as companionship and trainability. Dogs/wolves
have co-existed with humans for millennia as, for example, scavengers of human refuse or
as food resources themselves, but the actual use of dogs in work such as co-operative
hunting appears to be a relatively recent development (Clutton-Brock, 1995). In the later
diversification of breeds, dogs have been artificially selected for specific tasks such as
hunting or herding, which involve co-operation with humans or other dogs (McConnell and
Bayliss, 1985; Slabbert and Rasa, 1997). Social cognitive skills, such as observational
learning, would be useful in traditional roles for dogs (Slabbert and Rasa, 1997) and are
potentially advantageous in some of the new roles for dogs in human society such as
guiding the blind (Naderi et al., 2001). Without further study of, for example, breed
differences in brain morphology or task completion in rigorous experimental paradigms it
is perhaps unwise to comment further on the role of selection of behavioural traits in the
development of social skills in dogs.
2.3. Effects of lifetime developmental experience
There is considerable anecdotal evidence for the expression of social intelligence by
dogs within the context of the human–animal relationship (Byrne and Whiten, 1988). More
recently, Topal et al. (1997, 1998) have investigated the influence of the type of attachment
between people and their pet dogs on the dog’s behaviour, including problem-solving
abilities. They found that dogs performed better at solving novel problems in the presence
of their owners than in the presence of strangers or when isolated, even when their owners
had no actual knowledge of the task to be solved (Topal et al., 1998). During these tests they
noted frequent glancing toward the owner as if the dog was monitoring the owner’s
behaviour or even soliciting help with the task. Topal et al. (1997) argue that the formation
of strong social bonds are important in the behavioural development of the dog, resulting in a
form of imprinting which can be seen both in situations where dogs are naturally protective
of family members, and in the enthusiasm with which dogs greet familiar people.
Evaluating the significance of enculturation in the domestic environment on social
cognition is extremely difficult. Animals with close associations with humans will have
plenty of opportunity to learn to use our behaviour, both intentional and unintentional, to
predict future events as a result of simple learned contingencies. However, exposure to the
human world may also facilitate the development of the more complex social cognitive
skills. If exposure to the human environment itself is an important factor in the expression
of these skills, then it becomes difficult to compare the findings of laboratory studies
involving enculturated animals with those of their wild cousins (Heyes, 1993; Povinelli,
1994). In other words, wild animals may only rarely use their potential cognitive abilities to
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233
solve problems, as most challenges in the natural environment could be solved by other
means such as species-specific responses, trial and error learning or observational learning.
The effects of exposure to our culture on dogs’ behavioural development and of breeding
and other selective pressures on their cognitive abilities are both important areas for future
investigation, but first it is important to establish reliable methodologies for testing for
these abilities in dogs. We review some of our own experiences in the following section.
3. Experimental methodologies to investigate cognitive processes in dogs
One of the principal difficulties with investigating mental representation in animals is
finding irrefutable evidence that they have used a cognitive process to change their
behaviour (that is, differentiating simple associative learning from true cognitive learning).
In humans this is partly solved by language, as we can articulate how we solved problems,
or our feelings at the time. In dogs, as in many other species, changes due to mental
representation can only be inferred from changes in behaviour. Behaviourists recognised at
an early stage that the majority of such changes in behaviour need only be explained by the
re-enforcing properties of the consequences of the behaviour’s action on the environment,
and that there was no need to infer unmeasurable changes in mental state as an intervening
variable. In the face of this logical argument, comparative psychologists have often limited
themselves to the tools employed by developmental psychologists to investigate cognitive
processes in pre-verbal infants (Piaget, 1952). These tools have, however, proved exceedingly powerful. For example, expectancy violation is used to investigate the ability to hold
mental information and use it to predict future events. This approach can be used to
investigate object permanence, or the ability to maintain a representation of an object when
it is not in view in animals and pre-verbal infants (Hauser, 2000).
3.1. Expectancy violation
An example of expectancy violation in animals was reported by Tinkelpaugh (1928) in
an experiment similar to the cup and ball illusion. In this experiment, a food item was
shown to a rhesus monkey, then covered by an upside-down cup. At the same time similar
cups were placed upside down but not covering food. If rewarded by receiving whatever
was underneath the cup, the monkey rapidly learned to indicate the food-covering cup even
if the positions of the cups were changed or briefly hidden from view by a screen. In itself,
this is quite impressive, but the monkey may have only formed a simple association that
lifting the appropriate cup leads to a food reward, rather than a mental concept of what lies
beneath each cup. If, however, the food item was highly prized (e.g. item of fruit) and was
secretly exchanged for a less desirable food item after it was covered (e.g. swap fruit for
lettuce), Tinkelpaugh described the monkey’s response as ‘‘surprised and angry’’ when the
lettuce leaf was revealed in the place of the fruit. As Hauser (2000) argues, it is not possible
to verify these interpretations of the monkey’s feelings, but the study seems to demonstrate
that the monkey detected a violation of an expectation based on a stored memory. These
behavioural changes are, however, difficult to objectively measure and quantify. Hence,
psychologists have developed additional tools in their armoury that may quantify the
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degree of surprise. One such tool is gaze duration, as we tend to look for longer at situations
that differ from our expectations.
Gaze duration and expectancy violation have been used to investigate numerical
competence in pre-verbal children (Wynn, 1992). Five-month-old infants were trained
to gaze at a screen behind which objects (Mickey Mouse dolls) were placed. Once the
screens were removed there were either the same or a different number of dolls as they had
seen placed. For example, two dolls may have been placed behind the screen, but upon
screen removal there were either one, two or three dolls in view. Wynn (1992) found that
infants would stare for longer at the dolls’ location if there were one more or one less than
should be expected. Thus, infants appeared to have some degree of numerical competence
or representation of number of objects even though they could not report the difference
with words or place semantic labels to what they have seen.
Numerical competence would be a valuable skill for both social and non-social animals,
for example in predator or prey detection, or estimation of the number of animals in rival
groups (McComb et al., 1994). In principle, a concept of number of predators could be
adaptive for prey species particularly those that are preyed upon by co-operative hunters.
Similarly co-operative hunters, when co-ordinating an attack would benefit from a concept
of where and how many of their fellows there were even when not all of the pack are in
view. A concept of number can take a number of forms (Hauser, 2000). At its simplest, this
could be just an ability to judge relative numerousness (i.e. X is greater than Y). More
complex processes may include some reference to mental representation of number such as
subitising (i.e. assigning an exact numerical tag to a small quantity of items) and estimation
(i.e. the process of approximating when the array contains six or more items). Finally,
counting itself implies some rather complex representational information. For example,
using a label (e.g. two) to indicate the number of objects and recognising that this label is
independent of the objects it applies to (i.e. two bananas is the same number as two apples
or even the same number as 2 days, a concept you cannot physically see or touch).
These latter processes are difficult to demonstrate without language (Pepperberg, 1994),
but some forms of numerical competency may be investigated using Wynn’s methods in
non-verbal animals. This has been done by Hauser (2000), who found that rhesus monkeys
appeared to be able to add up to three eggplants (aubergines), but no more. Similar studies
have been conducted by our own group in domestic dogs (West and Young, 2002). In this
experiment, pet dogs were tested using large bone-shaped biscuits instead of dolls. During
training, single biscuits were placed behind an opaque screen. The screen was then
removed to reveal the same biscuit as had been placed (Fig. 1A–C). Once each dog had
attained a stable gaze duration (approximately 6 s between screen removal and looking
away), they were presented with three simple calculations: 1 þ 1 ¼ 2 (correct), 1 þ 1 ¼ 1
(incorrect), 1 þ 1 ¼ 3 (incorrect) and gaze duration was recorded from videos from the
time of screen removal to the time of looking away (preferential looking method). With
expected outcomes (i.e. 1 þ 1 ¼ 2), dogs spent the same amount of time looking at the
result of the calculation as they did upon the presentation of a single biscuit (Table 1).
When the result was unexpected (i.e. 1 þ 1 ¼ 1 or 1 þ 1 ¼ 3) dogs spent significantly
longer looking at the outcome of the calculation than they did with a single biscuit control.
These results show that dogs gazed for longer if there were either more or fewer biscuits
than they expected. The dogs may have been solving this task by actual counting or simple
J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
235
Fig. 1. Preferential gaze in the dog as used by West and Young (2002). (A) Three bone-shaped biscuits have
been placed behind the screen. (B) The screen is removed and the time taken between screen removal and the
dog’s looking away (C) recorded. Photos courtesy of Rebecca West, De Montfort University.
arithmetic, though there is little evidence to support this conclusion from their overt
behaviour. They did not, for example, appear to linger on each biscuit then move on.
Alternatively, the results may be interpreted as a simple form of object permanence or
delayed matching to sample, which at least shows a representation of object not in view,
though not representing this as a number of objects. This interpretation may be fair except
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J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
Table 1
Preferential looking times (s) for dogs in three tests
Bones
Dog
1
2
3
4
5
6
7
8
9
10
11
Mean
Control 1
(one bone)
Test 1
(two bones)
Control 2
(one bone)
Test 2
(one bone)
Control 3
(one bone)
Test 3
(three bones)
5.69
5.53
4.62
4.97
6.60
6.24
5.03
4.73
11.03
5.25
9.71
5.28
6.69
5.03
3.76
7.96
6.68
4.48
5.26
11.63
4.52
11.75
6.72
6.84
3.38
4.14
6.62
5.12
5.34
5.41
9.38
4.38
9.57
8.19
8.15
4.50
4.56
9.41
5.94
5.61
6.75
15.59
5.59
11.94
5.12
5.29
–
–
–
–
–
–
9.57
4.25
8.81
6.72
6.88
–
–
–
–
–
–
13.07
4.79
11.4
6.31
6.64
6.08
7.84**
6.61
8.57*
In the first test (n ¼ 11) two bones were placed behind screen and both remained when screen was removed
(1 þ 1 ¼ 2). In the second test (n ¼ 11) two bones were placed behind screen and only one remained when the
screen was removed (1 þ 1 ¼ 1) and in the third test (n ¼ 5) two bones were placed behind the screen but three
were present when the screen was removed (1 þ 1 ¼ 3). Before each test there was a control where a single bone
was placed behind the screen, which was still there when the screen was removed. Dogs gazed for longer when
the number of bones differed from their ‘‘expectation’’. Data from West and Young (2002).
*
P < 0:05.
**
P < 0:001.
that the dogs never actually saw the biscuits in their precise locations behind the screen, but
rather the placing of the biscuits. Consequently, they would have had to transfer observed
information involving movement to a position behind the screen to location information
once the screen was removed, rather than actually having seen where the bones were
placed. This transfer of information implies, at the very least, some concept of number of
objects, though it would not be fair to infer anymore than simple subitising of number. It
may therefore be that dogs only represent numbers of objects as ‘‘one’’, ‘‘two’’, and ‘‘lots’’.
Preferential looking technique may be extended to larger numbers, though in rhesus
monkeys, the technique has only been used successfully up to four, which may represent
a limitation on the animal’s numerical competence or a limitation of the technique
(Hauser, 2000).
3.2. Mental state attribution
Other important tools for investigating cognitive processes are problem-solving paradigms involving the acquisition or expression of novel, behavioural responses. The aim of
such paradigms is to be able to eliminate simpler or more parsimonious explanations of
apparent problem-solving ability, which may be based on evolutionary rules of thumb, trial
and error learning or prior experience. This positivist, scientific requirement to ascribe the
most parsimonious explanation of observed events is just as important today as in the time
J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
237
of Lloyd-Morgan and has recently been reviewed by, amongst others, Dawkins (1993) and
Heyes (1994).
Such approaches can also be used to investigate object permanence in animals. One
example is selective search behaviour for objects out of view (Gagnon and Dore, 1994) but
a more interesting paradigm for investigating social cognition is based on perspective
taking. An example of such a paradigm is the false believe task originally created by
Wimmer and Perner (1983) and modified by Baron-Cohen et al. (1985), who called it the
‘‘Sally-Anne’’ task. In Wimmer and Perner’s original method two children see an
experimenter place a toy in a location A. One child leaves the room and the experimenter
moves the toy to another location B. The remaining child is asked to indicate where the
absent child would look for the toy on their return. A child able to take the perspective of
others would indicate location A, as they will realise that the other child has not seen the toy
being moved. A child unable to take the perspective of others would indicate location B. As
children age, they shift from consistently choosing the box in which the object is actually
located to indicating the box in which the object was originally placed (Wimmer and
Perner, 1983). Co-incidentally children with impaired social skills perform poorly on this
task (Baron-Cohen et al., 1985; Pilowsky et al., 2000). This task, however, involves fairly
sophisticated linguistic abilities, which may explain why younger children perform poorly.
A non-verbal form of this location change task involving marking the locations has been
developed by Call and Tomasello (1999) for use with pre-verbal humans and animals,
which was successfully completed by most 5-year-old children, some 4-year olds, but not
by orang-utans or chimpanzees.
An alternative approach to investigating perspective taking is the Knower:Guesser
paradigm that has been developed by Povinelli and colleagues and originally involving
chimpanzees (e.g. Povinelli et al., 1990, 1997; Povinelli and Eddy, 1996). In this paradigm,
the ability to distinguish between an apparently knowledgeable social cue (the Knower)
and an apparently ignorant social cue (the Guesser) is used to demonstrate that animals can
see the world from the perspective of others. Povinelli’s group developed two methods to
investigate this ability using non-human primates as test species and humans as the Knower
and the Guesser.
3.2.1. Choice of target when begging
The first method is based on food soliciting (begging) from a human provider/helper
(Povinelli and Eddy, 1996). The chimps are first trained to solicit food from a human
provider, and then they are asked to discriminate between an apparently knowledgeable
provider and an apparently unknowledgeable provider with, for example, a blindfold over
their eyes. As a control for presence of blindfold alone, they are also offered choices
between provider with blindfold over eyes and providers with blindfold over mouth or over
hair. In this paradigm, three out of four chimpanzees consistently preferred to beg from the
provider that could see, whereas no rhesus monkeys made this discrimination (Povinelli
and Eddy, 1996). This approach has been adapted for dogs by our own group using a range
of vision obstructers including blindfolds over eyes, buckets on heads and books obscuring
eyes (Bishop and Young, in press). Overall, dogs preferred to solicit food from a human
who could see the reward, or whose eyes the dog could clearly see (Table 2), though this
finding was strongest when vision was obscured by a book (Friedmann test; P < 0:01).
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Table 2
Number of times (out of 10) each dog begged from the ‘‘seeing’’ person in each experimental condition
Dog
A
B
C
D
E
F
G
H
I
J
Total
Blind 1
Blind 2
7
5
7
8
8
7
6
4
5
7
8
7
7
7
8
6
5
5
8
4
64
65
Blind 3
8
8
9a
6
7
7
2
4
8
6
65
Bucket
6
7
8
6
7
7
5
7
9a
7
69
Hands
Book
6
5
8
5
8
5
4
7
7
6
8
9a
10a
5
8
9a
7
8
10a
8
61
82
Total (%)
43
41
49
37
46
41
29
35
47
38
(72)
(68)
(82)
(62)
(77)
(68)
(48)
(58)
(78)
(64)
406 (68)
Blind 1: blindfold over eyes versus no blindfold; Blind 2: blindfold over eyes versus blindfold on forehead;
Blind 3: blindfold over eyes versus blindfold on chin; Bucket: bucket on head versus bucket in hand; Hands:
hands over eyes versus hands over ears; Book: book over eyes versus book in hand. Data from Bishop and Young
(in press).
a
Preferences of 9 or 10 out of 10 are better than would be expected by chance from binomial distribution.
This finding suggests that, at least in this begging paradigm, prior experience may play a
major role since the blindfold and bucket options were novel to the dogs, but they are likely
to have had prior experience of people reading books and learned not to beg from people
engaged in these activities.
3.2.2. Use of demonstrators
The second method used to investigate perspective taking is based on using human
demonstrators as cues to locating hidden food (Povinelli et al., 1990; Heyes, 1993). Chimps
are first trained to use humans as indicators of the location of food, for example pointing at
food that has been provisioned behind one of the number of screens. The chimps are then
tested with two human indicators, one of whom knows the location of the food (saw where
the food had been placed) and one who does not (e.g. was out of the experimental room
when the food was placed or had a paper bag over his/her head). Again chimpanzees chose
the locations indicated by Knowers in preference to locations indicated by Guessers. This
study, therefore, suggests that the chimps were capable of taking the perspective of the
demonstrators and acting sensibly on that information (Povinelli et al., 1990).
Whilst these experiments provide compelling evidence for perspective taking in
non-human animals, the interpretation of the work has been criticised (Heyes, 1993,
1994). The specific criticism is that the chimps could have learnt to use the demonstrators
as discriminatory cues without understanding the different states of knowledge of the
demonstrators. The chimps could have made a simple association between the person in the
room, their signal and the location of food, without actually appreciating that they are
likely to be more knowledgeable about the test situation because they have actually seen
what happened. Certainly, the chimps were tested often enough to have the opportunity to
make these simple associations. Another problem is that there may also have been subtle
J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
239
distinctions between the two demonstrators at the time of the discriminating task, e.g. the
Knower pointed more confidently than the Guesser. The chimps may have used these subtle
cues as the discriminator with no reflection on previous events.
A potential solution to this has been developed by Held et al. (2001a) using trained
conspecifics as the demonstrators. Their chosen test species was the domestic pig (Sus
scrofa). They first showed that pigs could use other pigs as information sources when
locating food (Held et al., 2000). For example, a pig that had not seen the location of baiting
would follow another pig that had seen the baiting to the correct location. Unfortunately,
when they allowed pigs to choose between demonstrator pigs that had seen a food-baiting
event and demonstrator pigs that had not, 12 out of 13 test pigs avoided both of the
demonstrators’ choices due to agonistic confrontations when two pigs went to the same
food location (Held et al., 2001b). Only one pig consistently followed others and this pig
did prefer to follow Knowers in 21 out of 24 trials, suggesting some appreciation of the
difference in information held by the two informants.
Domestic dogs may provide an alternative model for investigating these perspectivetaking paradigms: firstly, because they are relatively easy to train to locate rewards, and
secondly, because they live so closely with people. Hidden food location protocols have
been used to investigate a wide range of learning processes in dogs including spatial
memory (Gagnon and Dore, 1992, 1994; Fiset et al., 2000) and the response to human
(Hare et al., 1998; Miklosi et al., 1998; McKinley and Sambrook, 2000; Soproni et al.,
2001; Pongracz et al., 2002) and conspecific social cues (Hare and Tomasello, 1999).
Interestingly, in these experiments dogs appear to be better than chimpanzees at using
social cues (such as pointing) to locate food (Povinelli et al., 1997, 1999; Tomasello et al.,
1997). For example, Miklosi et al. (2000) found that dogs could use human signals such as
pointing, orientation and even just glancing at a location to influence the target choice of
dogs. They also took considerably less training than primates to learn these associations
(Povinelli et al., 1999). Thus, social signals appear to be more powerful than non-social
cues for domestic dogs.
Tests for the ability to use others as information sources, based on the methodologies
developed by, e.g. Povinelli et al. (1990) and modified by Held et al. (2001a) have been
attempted using dogs by our group (Ashton and Cooper, unpublished data; West,
unpublished data). In the first of these studies, Ashton and Cooper trained nine dogs to
locate food that had been placed behind one of the four screens. All dogs selected
successfully learnt this task when they had seen the baiting of the target with a latency
to reach food of approximately 7 s and a rate of 1 error or incorrect choice every 10 tests
(0.1 errors per test). They were then ‘‘blinded’’ by placing a blanket over their start box
(Fig. 2A). When ‘‘blinded’’, the dogs made more mistakes during food-locating tasks (1.5
errors per test) and took longer to locate food (an average latency of 15 s to reach baited
target) than when they had seen the act of baiting. Next, ‘‘blind’’ dogs were allowed to use a
dog that had seen the baiting as an information source. Under these circumstances ‘‘blind’’
dogs followed the ‘‘informed forager’’ to the baited target, such that they found the food
faster (5 s) and with fewer mistakes (0.2 errors per test) than if they had been on their own.
It was, however, not clear if they were using their conspecific as an information source
or just following it, then responding to the food, when they came across it. This issue was
not resolved in the Knower:Guesser paradigm, when blind test dogs were required to
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J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
Fig. 2. Knower:Guesser paradigm as used by Ashton and Cooper (unpublished data). (A) ‘‘Blind’’ dogs in
covered start box were found to follow demonstrator dogs able to see the baiting of food targets behind screens.
(B) Demonstrator dogs housed in either the covered or the uncovered side start boxes are trained to seek food in
specific target locations behind screens and act as information sources to test dog in covered, central start box.
Photo courtesy of Jonathan Cooper, University of Lincoln.
discriminate between a dog that had seen where food was provisioned and a dog that had
not, even though both had been trained to fixed locations (Fig. 2B). In the test situation,
dogs appeared to be more interested in positive social interaction than locating food as
they always followed another dog, but did not discriminate between apparently informed
and uninformed dogs. Species-specific limitations, such as avoidance in pigs and social
interaction in dogs, may therefore limit the usefulness of this methodology when using
groups of animals released into a test arena.
An alternative approach is to use human demonstrators as simple discriminative stimuli.
We modified Povinelli et al.’s (1990) protocol using a larger sample of dogs for a small
number of trials each, rather than repeatedly testing the same test individuals (West,
unpublished data). The dogs had a choice of three baited target locations, and two human
indicators. Each dog was present in the room when the targets were baited, but could not
see the bait location itself. It could, however, see one human (the Knower) in a position
where they would have been able to see where food had been placed. The second
demonstrator (the Guesser) was outside the room when the location was baited but
returned to the room in order to indicate a non-baited location prior to the dog being
released. Fifteen dogs were tested six times, which represented one trial each of each
demonstrator–target combination. No dog chose the target that was not indicated by either
demonstrator. In the first trial of the six, they did discriminate between the two demonstrators with 14 dogs choosing the Knower’s direction (Table 3; P < 0:001), but in
subsequent trials there was no preference with dogs performing no better than what
would be expected by chance (P > 0:05).
This experiment has two findings of particular note. First, the preference for the Knower
in the first trial suggests that the dogs had transferred knowledge from previous situations
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J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
Table 3
Results of Knower:Guesser paradigm using humans as discriminative cues for 15 dogs (one of which only
completed three trials)
ID
Test 1
Test 2
Test 3
Test 4
Test 5
Test 6
Total (K)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
K
K
K
K
K
K
K
G
K
K
K
K
K
K
K
K
G
K
G
K
G
G
K
G
K
K
K
G
G
K
K
K
K
K
K
K
G
G
K
K
G
G
G
G
K
K
K
G
G
K
K
K
K
K
G
–
K
K
K
G
K
G
K
G
G
G
G
K
K
K
–
G
G
K
K
G
G
K
G
K
G
K
K
K
K
–
K
K
G
G
5
3
5
2
5
3
3
4
5
5
2
4
3
3
4
Percent
14/15
93
8/15
53
9/15
60
10/14
71
7/14
50
8/14
57
56/90
64
Given a choice between a target indicated by the person who had remained in the room during baiting (K), a
target indicated by a person who had not been in the room during baiting (G), or a target indicated by neither
person (N), dogs always chose either K or G. In the first trial, dogs had a preference for the Knower’s target
(P < 0:001), but in subsequent trials no such preference was evident.
(e.g. the home) about the reliability of present and absent people as information sources.
The high proportion of successful responses in the first trial also overcomes the criticism
put forward by Heyes (1994) of Povinelli et al.’s (1990) work, that the animals may form a
rapid association between the alternative cues and the rewards they indicate, such that the
preferences may be explained as simple associative learning rather than explicit problem
solving. The second interesting finding is that the dogs subsequently did not persist with
using the perspective-taking rule. In fact, the population appeared to be following no
consistent rule, although individuals may have used different rules. This points to the
value of using novel tests when investigating cognitive functions in animals. Having
successfully solved the food-locating task when the only discriminatory cue was the signal
of the demonstrator, the dogs may fail subsequent tests as they are attempting to apply
information they have learnt from previous trials. This may, for example, involve a return to
a previously rewarded location, or the use of a previous demonstrator (in the experiment the
demonstrator and location were controlled for in the experimental design). If dogs react to
test situations in this way (i.e. ‘‘on first trial transfer information from other situations: in
subsequent tests apply what you have learnt about the current test situation’’), then this not
only demonstrates the danger that repeated testing leads to simple conditioned responses
(Heyes, 1994), but also suggests that higher cognitive abilities are most likely to be used in
novel situations. If this is the case, then investigating these processes may be most practical
in species with a large, readily accessible test population such as pet dogs.
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J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
4. Recommendations for studying social cognition in domestic dogs
In summary, the domestic dog appears to make a good model species for the
investigation of cognitive processes, particularly those related to social function. Dogs
may have inherited the capacity for certain social skills from their social living,
co-operatively hunting ancestors. This may have been enhanced by artificial selection under
domestication for co-operative skills or the tendency to form close social ties with humans. A
number of methodologies may be adopted from studies of pre-verbal humans and apes to
investigate the social skills in dogs. However, rather than simply taking methods off the shelf
and substituting dogs, the species-specific behavioural repertoires need to be considered.
There has been some success in investigating both dog’s expectancies and their ability to
transfer information between situations to solve new problems. Dogs give preference to
social cues (other dogs and humans) over abstract non-social cues as information sources
about reward location, and appear to have less difficulty than primates in using social cues
for this purpose. Domestic dogs, however, only show the ability to distinguish between
knowledgeable and unknowledgeable people (and not other dogs) when faced with a choice.
Previous studies with dogs lead to the general recommendation that, where possible, single
trial experiments should be used to investigate transfer of knowledge. This rules out the
possibility of a conditioned response over successive trials, and animals may be more likely to
use transfer of knowledge from another situation (i.e. thinking) when exposed to a new
problem.
Acknowledgements
We would like to thank Melissa Albentosa for comments on this manuscript and Susanne
Held, Mike Mendl and Adam Miklosi for discussions relating to this review and the
development of methodologies for work with dogs. We also thank The Universities
Federation for Animal Welfare for funding Clare Ashton’s Vacation Scholarship, De
Montfort University for supporting Rebecca West’s graduate studies, Andrea Ferguson and
Sue McKinley for help on experimental trials and Colin Riches and University of Lincoln
Animal Care Unit staff for help with caring for dogs.
References
Baron-Cohen, S., Leslie, A.M., Frith, U., 1985. Does the autistic child have a theory of mind? Cognition 21,
37–46.
Bishop, S., Young, R.J. Do domestic dogs understand the importance of eye contact with humans? Anim. Cogn.,
in press.
Bolk, L., 1926. Das Problem der Menschwerdung. Gustav Fischer, Jena.
Byrne, R.W., Whiten, A., 1988. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in
Monkeys, Apes and Humans. Clarendon Press, Oxford.
Byrne, R.W., Whiten, A., 1990. Tactical deception in primates, the 1990 database. Primate Rep. 27, 1–101.
Call, J., Tomasello, M., 1999. A non-verbal false belief task: the performance of children and great apes. Child
Dev. 70, 381–395.
J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
243
Clutton-Brock, J., 1995. Origins of dog domestication and early history. In: Serpell, J. (Ed.), The Domestic Dog:
its Evolution, Behaviour and Interactions with People. Cambridge University Press, Cambridge, pp. 7–20.
Coppinger, R., Coppinger, L., 2001. Dogs. Scribner, New York.
Coppinger, R., Schneider, R., 1995. Evolution of working dogs. In: Serpell, J. (Ed.), The Domestic Dog: its
Evolution, Behaviour and Interactions with People. Cambridge University Press, Cambridge, pp. 21–47.
Dawkins, M.S., 1993. Through our eyes only the search for animal consciousness. Skectrum Fulcrum,
Oxford.
Dunbar, R.I.M., 1992. Neocortex size as a constraint on group-size in primates. J. Hum. Evol. 22, 469–493.
Dunbar, R.I.M., Bever, J., 1998. Neocortex size predicts group size in carnivores and some insectivores.
Ethology 104, 695–708.
Fiset, S., Beaulieu, C., Gagnon, S., 2000. Spatial encoding of hidden objects in dogs (Canis familiaris). J.
Comp. Psychol. 114, 315–324.
Fox, M.W., 1968. The influence of domestication upon behaviour of animals. In: Fox, M.W. (Ed.), Abnormal
Behavior in Animals. Saunders, Philadelphia, pp. 64–76.
Fox, M.W., 1971. Behaviour of Wolves, Dogs and Related Canids. Jonathan Cape, London.
Fox, M.W., 1978. The Dog: its Domestication and Behavior. Garland Press, New York.
Frank, H., 1980. Evolution of canine information processing under conditions of natural and artificial selection.
Z. Tierpsychol. 59, 389–399.
Frank, H., Frank, M.G., 1982. On the effects of domestication on canine social development and behavior. Appl.
Anim. Ethol. 8, 507–525.
Gagnon, S., Dore, F.Y., 1992. Search in various breeds of adult dogs (Canis familiaris): object permanence and
olfactory cues. J. Comp. Psychol. 106, 58–68.
Gagnon, S., Dore, F.Y., 1994. Cross-sectional study of object permanence in domestic puppies (Canis
familiaris). J. Comp. Psychol. 108, 220–232.
Ginsburg, B.E., Schotte, C.S., 1978. Genetic differences determining the capacities for social behavior in wolves
and dogs. Behav. Genet. 8, 94.
Gould, S.J., 1978. Ever Since Darwin: Reflections in Natural History. Penguin, Hammondsworth.
Hare, B., Tomasello, M., 1999. Domestic dogs (Canis familiaris) use human and conspecific social cues to
locate hidden food. J. Comp. Psychol. 113, 173–177.
Hare, B., Call, J., Tomasello, M., 1998. Communication of food location between human and dog (Canis
familiaris). Evol. Commun. 2, 137–159.
Hauser, M., 2000. Wild Minds: What Animals Really Think. Allen Page, London.
Hediger, H., 1938. Tierpsychologie und Haustierforschung. Z. Tierpsycol. 2, 29–46.
Held, S., Mendl, M., Devereux, C., Byrne, R., 2000. Social tactics in pigs in a competitive foraging task: the
‘‘informed forager’’ paradigm. Anim. Behav. 59, 569–576.
Held, S., Mendl, M., Devereux, C., Byrne, R., 2001a. Studies in social cognition: from primates to pigs. Anim.
Welfare 10, S209–S217.
Held, S., Mendl, M., Devereux, C., Byrne, R., 2001b. Behaviour of domestic pigs in a visual perspective taking
task. Behaviour 138, 1337–1354.
Heyes, C.M., 1993. Anecdotes, training, trapping and triangulating: do animals attribute mental states. Anim.
Behav. 46, 177–188.
Heyes, C.M., 1994. Social cognition in primates. In: Mackintosh, N.J. (Ed.), Animal Learning and Cognition.
Academic Press, London, pp. 281–305.
Heyes, C.M., 1998. Theory of mind in non-human primates. Behav. Brain Sci. 21, 101–114.
Humphrey, N.K., 1976. The social function of intellect. In: Bateson, P.P.G., Hinde, R.A. (Eds.), Growing Points
in Ethology. Cambridge University Press, Cambridge, pp. 303–317.
Kruska, D., 1988. Mammalian domestication and its effects on brain structure and behaviour. In: Jerison, H.J.,
Jerison, I. (Eds.), Intelligence and Evolutionary Biology. Springer, Berlin, pp. 211–250.
McComb, K., Packer, C., Pusey, A., 1994. Roaring and numerical assessment in contests between groups of
female lions (Panthera leo). Anim. Behav. 47, 379–387.
McConnell, P.C., Bayliss, J.R., 1985. Interspecific communication in cooperative hunting herding: acoustic and
visual signs from human shepherds and herding dogs. Z. Tierpsychol. 67, 302–328.
McKinley, J., Sambrook, T.D., 2000. Use of human-given cues by domestic dogs (Canis familiaris) and horses
(Equus caballus). Anim. Cogn. 3, 13–22.
244
J.J. Cooper et al. / Applied Animal Behaviour Science 81 (2003) 229–244
Mech, L.D., 1970. The Wolf: The Behavior and Ecology of an Endangered Species. Natural History Press, New
York.
Miklosi, A., Polgardi, R., Topal, J., Csanyi, V., 1998. Use of experimenter given cues in dogs. Anim. Cogn. 1,
113–121.
Miklosi, A., Polgardi, R., Topal, J., Csanyi, V., 2000. Intentional behaviour in dog–human communication: an
experimental analysis of ‘‘showing’’ behaviour in the dog. Anim. Cogn. 3, 159–168.
Naderi, S., Miklosi, A., Doka, A., Csanyi, V., 2001. Co-operative interactions between blind persons and their
dogs. Appl. Anim. Behav. Sci. 74, 59–80.
Pepperberg, I., 1994. Numerical competence in an African grey parrot. J. Comp. Psychol. 108, 36–44.
Piaget, J., 1952. The Origins of Intelligence in Children. International University Press, New York.
Pilowsky, T., Yirmiya, N., Arbelle, S., Mozes, T., 2000. Theory of mind abilities of children with schizophrenia,
children with autism, and normally developing children. Schizophr. Res. 42, 145–155.
Pongracz, P., Miklosi, A., Kubinyi, E., Gurobi, K., Topal, J., Csanyi, V., 2002. Social learning in dogs: the effect
of a human demonstrator on the performance of dogs in a detour task. Anim. Behav. 62, 1109–1117.
Povinelli, D.J., 1994. Comparative studies of animal mental state attribution: a reply to Heyes. Anim. Behav. 48,
239–241.
Povinelli, D.J., Eddy, T.J., 1996. What young chimpanzees know about seeing. Monogr. Soc. Res. Child Dev. 61,
247.
Povinelli, D.J., Nelson, K.E., Boysen, S.T., 1990. Inferences about guessing and knowing in chimpanzees (Pans
trogodytes). J. Comp. Psychol. 105, 318–325.
Povinelli, D.J., Reaux, J.E., Bierschwale, D.T., Allain, A.D., Simon, B.B., 1997. Exploitation of pointing as a
referential gesture in young children, but not adolescent chimpanzees. Cogn. Dev. 12, 423–461.
Povinelli, D.J., Bierschwale, D.T., Cech, C.G., 1999. Comprehension of seeing as a referential act in young
children, but not juvenile chimpanzees. Br. J. Dev. Psychol. 17, 37–60.
Premack, D., Woodruff, G., 1978. Does the chimpanzee have a theory of mind? Behav. Brain Sci. 4, 515–526.
Price, E.O., 1984. Behavioral aspects of animal domestication. Q. Rev. Biol. 59, 1–32.
Slabbert, J.M., Rasa, O.A.E., 1997. Observational learning of an acquired maternal behaviour pattern by
working dog pups: an alternative training technique. Appl. Anim. Behav. Sci. 53, 309–316.
Soproni, K., Miklosi, A., Topal, J., Csanyi, V., 2001. Comprehension of human communicative signs in pet dogs.
J. Comp. Psychol. 115, 122–126.
Tinkelpaugh, O.L., 1928. An experimental study of representative factors in monkeys. J. Comp. Psychol. 8, 197–
238.
Tomasello, M., Call, J., Gluckman, A., 1997. Comprehension of novel communicative signs by apes and human
children. Child Dev. 68, 1067–1080.
Topal, J., Miklosi, A., Csanyi, V., 1997. Dog–human relationship affects problem solving behaviour in dogs.
Anthrozoos 10, 214–224.
Topal, J., Miklosi, A., Csanyi, V., Doka, A., 1998. Attachment behaviour in dogs (Canis familiaris): a new
application of Ainsworth’s (1969) strange situation test. J. Comp. Psychol. 112, 219–229.
Tschudin, A.J.-P.C., 2001. Mind-reading mammals? Attribution of belief tasks with dolphins. Anim. Welfare 10,
S119–S127.
Vila, C., Savolainen, P., Maldonado, J.E., Amorim, I.R., Rice, J.E., Homeycutt, R.L., Crandall, K.A., Lundeberg,
J., Wayne, R.K., 1997. Multiple and ancient origins of the domestic dog. Science 276, 1687–1689.
Wayne, R.K., 1986. Cranial morphology of domestic and wild canids: the influence of development on
morphological change. Evolution 40, 243–261.
West, R., Young, R.J., 2002. Do domestic dogs show any evidence of being able to count? Anim. Cogn. 5, 183–
186.
Whiten, A., Byrne, R.W., 1997. Machiavellian Intelligence. II. Cambridge University Press, Cambridge.
Wimmer, H., Perner, J., 1983. Beliefs about beliefs: representation and constraining function of wrong beliefs in
young children’s understanding of deception. Cognition 13, 103–128.
Wynn, K., 1992. Addition and subtraction by human infants. Nature 358, 749–750.