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Majid Beshkar
Animal Consciousness
Abstract: There are several types of behavioural evidence in favour
of the notion that many animal species experience at least some
simple levels of consciousness. Other than behavioural evidence,
there are a number of anatomical and physiological criteria that help
resolve the problem of animal consciousness, particularly when
addressing the problem in lower vertebrates and invertebrates.
In this paper, I review a number of such behavioural and brain-
based evidence in the case of mammals, birds, and some invertebrate
species. Cumulative evidence strongly suggests that consciousness, of
one form or another, is present in mammals and birds. Although
supportive evidence is less strong in the case of invertebrates, it is
more likely than not that they also experience some simple levels of
consciousness.
Keywords: Behaviour; Birds; Brain; Cephalopods; Communication;
Insects; Mammals; Mirror self-recognition; Tools
Introduction
So far, almost all scientific studies of consciousness have focused on
humans and other primates that share many common features in the
nervous system in terms of both anatomy and physiology. Although
this line of research has provided invaluable insight into the problem
of consciousness, using other animal species, such as lower
Journal of Consciousness Studies, 15, No. 3, 2008, pp. 5–33
Correspondence:Majid Beshkar, Tehran University of Medical Sciences, Tehran, Iran.Email: [email protected]
Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction
vertebrates and even invertebrates, as subjects of consciousness stud-
ies will open an entirely new window and shed more light on the prob-
lem. In this regard, a comparative approach to the problem of
consciousness might be as informative and helpful as in other areas of
biological sciences.
There is no generally agreed upon definition for the term ‘con-
sciousness’. However, there is general consensus that consciousness
comes in a variety of different levels. At one end of the spectrum lie
higher levels of consciousness, including ‘self-awareness’ — the
capability of an organism to be aware that it is awake and actually
experiencing specific mental event — and ‘meta-self-awareness’ —
the capability of an organism to be aware that it is self-aware (Morin,
2006). At the other end lie the lower levels of consciousness including
‘primary consciousness’ which refers to the presence of reportable
multimodal scenes composed of perceptual and motor events, and
‘fringe consciousness’ which refers to vague conscious experiences
that do not have sensory qualities like color, pitch or texture and lack
object identity, location in space, and sharp boundaries in time (Seth et
al., 2005).
A precise definition of consciousness is ideal but not possible with
our current knowledge of this enigmatic phenomenon. Everyone has a
rough idea of what is meant by consciousness, and as Crick and Koch
(1990, p. 624) believe ‘Until we understand the problem much better,
any attempt at a formal definition is likely to be either misleading or
overly restrictive, or both.’ Therefore, a practical definition of con-
sciousness seems to be sufficient for the purpose of this article.
Throughout this paper I use the term ‘consciousness’ in the context
described by Edelman (1989; 2003; 2004). He distinguishes two vari-
eties of consciousness, primary and higher-order consciousness.
Animals with primary consciousness can integrate perceptual and
motor events together with memory to construct a multimodal scene in
the present … On this basis, the animal may alter its behavior in an
adaptive fashion … Higher-order consciousness allows its possessors
to go beyond the limits of the remembered present of primary con-
sciousness. An individual’s past history, future plans, and conscious-
ness of being conscious all become accessible (Edelman, 2003, pp.
5521–22).
Until recently, nonhuman animals were not usually considered as
suitable subjects for consciousness studies because it was hard for
many researchers to believe that animals could experience any kind of
consciousness at all. However, several lines of behavioural and brain-
6 M. BESHKAR
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based evidence strongly suggest that many animal species might
experience at least some simple levels of consciousness.
Behavioural versatility is considered to be a strong line of evidence
in support of animal consciousness (Griffin & Speck, 2004; Griffin,
1998; 1995). If an animal adjusts its behaviour appropriately in
response to novel and unpredictable challenges, it seems more likely
that it is thinking consciously about its situation than when its
responses are uniform and stereotyped. One can argue that no matter
how versatile and ingenious an animal’s behaviour may be, it is quite
possible that it is accomplished unconsciously. However, conscious
thinking may be a more effective way to use a nervous system, render-
ing it unnecessary to store a vast library of detailed instructions as to
how an animal should behave under all possible contingencies,
whether the library is established by genetic instruction or individual
learning. Significant examples of goal-directed versatile behaviour
suggestive of conscious thinking include (i) creative tool-making and
tool-use, (ii) problem solving, and (iii) deceptive behaviours.
Another line of evidence in support of animal consciousness is the
capacity of mirror self-recognition which is considered to be an indi-
cator of self-awareness. Mirror self-recognition is usually explored in
animals by recording whether they touch a dye-marked area on visu-
ally inaccessible parts of their body while looking in a mirror or
inspect parts of their body while using the mirror’s reflection.
The ability of some animals to communicate semantic information
is considered to be a suggestive evidence of animal consciousness.
Griffin (1998, p. 4) argues that ‘interpretation of animal communica-
tion can provide fairly direct evidence about some of their thoughts
and feelings, just as human communicative behavior is our chief basis
for inferring what our human companions think and feel.’
There are several examples of semantic communication in animals,
including the well-studied alarm calls. When detecting a predator,
some animals give an alarm call that contains information about the
type of predator that has been detected. When this encoded informa-
tion is perceived by other animals that hear the alarm call, they imme-
diately take appropriate evasive actions. If an animal’s alarm calls are
all the same, except in loudness or frequency of repetition, no matter
what the animal is afraid of, it seems less likely that these signals are
expressing even simple conscious feelings than when such signals
also transmit information about the type of danger that is threatening.
However, there is clear evidence that alarm calls not only vary in
intensity and in how often they are repeated in accordance with the
ANIMAL CONSCIOUSNESS 7
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degree of danger or fear, but also convey specific information about
the type of danger or how hearers might escape it (Griffin, 1995).
Another line of strong evidence in support of animal consciousness
is the ability of many animals to form and recall such types of memory
that requires consciousness, generally referred to as explicit memory.
For example, the ability to remember unique personal experiences in
terms of their details (what), their locale (where) and temporal occur-
rence (when) is known as episodic memory and is thought to require
self-awareness and the ability to subjectively sense time (Dere et al.,
2006). It has long been held that explicit memory is unique to humans,
because it was accepted that animals lack consciousness. However,
this assumption is strongly challenged by relatively recent
behavioural evidence showing that various animal species indeed
show behavioural manifestations of different features of explicit
memory.
Another equally important behavioural index of consciousness is
the so called ‘commentary key’ paradigm developed by Weiskrantz
(1991; 1999) and Cowey and Stoerig (1995). Weiskrantz argues that
commentaries (or the lack of them) are critical measure of conscious-
ness because they provide the means by which we decide whether or
not a subject is conscious of an event. The commentary key method
allows an animal to make a behavioural comment on a previous
response. In this paradigm, animals have available two discrimination
responses and also a commentary key with which to step outside the
discrimination and report on the state of their knowledge or percep-
tion. The commentary key method is particularly remarkable because
it allows us to ask if the animals studied act in response to conscious
events differently than they do to comparable brain events that are
unconscious.
The above-mentioned behavioural indices mainly focus on those
kinds of conscious experiences that are associated with carrying out
complex cognitive tasks. In fact the search for consciousness in ani-
mals is frequently seen as the search for higher and higher cognitive
capacities in them. However, although these cognitive abilities are
remarkable, too much emphasis on the cognitive side of conscious-
ness may lead us to overlook other aspects that are equally important,
such as the interesting domain of animal emotions.
Current research provide convincing evidence that many animal
species experience at least some kinds of emotions such as fear, joy,
happiness, jealousy, rage, anger, sadness, despair, and grief (Bekoff,
2000). Since no great cognitive powers are needed to experience such
emotions as pain, fear or hunger ‘our search for animal consciousness
8 M. BESHKAR
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could fruitfully be extended to the realm of the emotions and therefore
potentially to a much wider range of animals than just the ones that are
outstandingly clever’ (Dawkins, 2000, p. 883).
The behavioural evidence discussed above, although very strong
and suggestive, should not be taken as exclusive measures of animal
consciousness. Since computers and robots can also produce outputs
that resemble conscious behaviours; and furthermore, since there are
many complex behaviours that can be performed unconsciously, it is
better to complement behavioural evidence with brain-based mea-
sures of consciousness.
As discussed in detail by Seth, Baars, and Edelman (2005), from
anatomical and physiological points of view, there are three main facts
that distinguish consciousness from other mental phenomena in
humans: (i) Conscious states are characterized by irregular,
low-amplitude, and fast electrical activity in the brain ranging from 12
to 70 Hz. On the other hand, unconscious states such as deep sleep,
vegetative states, epileptic loss of consciousness and general anesthe-
sia are all characterized by regular, high-amplitude, and slow voltages
at less than 4 Hz. (ii) Consciousness seems to be particularly associ-
ated with the thalamocortical system. (iii) Conscious states are associ-
ated with widespread brain activation; while, unconscious perception
involves local activation of the brain.
In this paper, I review suggestive evidence of animal consciousness
in both vertebrates and invertebrates. In the case of vertebrates, I
focus mainly on primates and birds because these animals have been
studied in more details in term of cognitive capacities. However, other
mammals such as rodents and elephants are also discussed here in
some detail. In the case of invertebrates, I focus on cephalopods and
insects and a relatively less-studied species, namely spiders.
1. Mammals
1.1. Explicit memory
There are many studies showing the ability of mammals to form and
retrieve different kinds of explicit memory. Here I review several
most significant cases of such studies.
Schwartz and colleagues have provided clear evidence that gorillas
demonstrate at least a limited capacity for episodic memory, that is, an
ability to retrieve events from the past. They have shown that King, a
western lowland gorilla, can remember aspects of an event that took
place up to 24 h earlier (Schwartz et al., 2004; 2002). These include
foods eaten, people who fed him, people who performed unusual
ANIMAL CONSCIOUSNESS 9
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events (e.g., playing a guitar), and objects witnessed (i.e., a Frisbee).
They reported King to be able to correctly identify a specific human
individual after a single exposure, when given a set of photographs to
choose among. In another experiment (Schwartz et al., 2005), they
also showed that King was able to recall three foods eaten and cor-
rectly sequence them in time; and furthermore, he was capable of
remembering where events took place.
Episodic memory is also present in mice and rats. In order to show
episodic memory in mice, Dere et al. (2005) designed an object explo-
ration task in which different versions of the novelty-preference para-
digm were combined to include (i) object recognition memory, (ii) the
memory for locations in which objects were explored, and (iii) the
temporal order memory for object presented at distinct time points.
They found that mice spent more time exploring two ‘old familiar’
objects relative to two ‘recent familiar’ objects, reflecting memory for
what and when and concomitantly directed more exploration at a spa-
tially displaced ‘old familiar’ object relative to a stationary ‘old famil-
iar’ object, reflecting memory for what and where. These results
strongly suggest that during a single test trial the mice were able to (i)
recognize previously explored objects (‘what’ aspect of episodic
memory), (ii) remember the location in which particular objects were
previously encountered (‘where’ aspect), and (iii) discriminate the
relative recency in which different objects were presented (‘when’
aspect).
Using a modification of the above-mentioned paradigm, Kart-Teke
et al. (2006) found that rats spent more time exploring an ‘old famil-
iar’ object relative to a ‘recent familiar’ object, suggesting that they
recognized objects previously explored during separate trials and
remembered their order of presentation. Concurrently, the rats
responded differentially to spatial object displacement dependent on
whether an ‘old familiar’ or ‘recent familiar’ object was shifted to a
location, where it was not encountered previously. These results pro-
vide strong evidence that the rats established an integrated memory
for ‘what’, ‘where’, and ‘when’.
Retrospective memory, which is considered to be an explicit form
of memory, has been demonstrated in dolphins. Mercado et al. (1998)
trained dolphins to execute specific behaviours, repeat behaviours
just performed, and emit a behaviour not performed most recently in
response to commands by the experimenter. During the test for retro-
spective memory, the animals were first required to show a relatively
novel response, and then asked to repeat that behaviour, while this
progression of commands was unexpected by the animals. The fact
10 M. BESHKAR
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that the dolphins were able to do so suggests that they indeed recol-
lected what their last response was, instead of just responding to a
command of the experimenter.
1.2. Mirror self-recognition
There are several accounts of the ability of mammals to recognize
themselves in mirrors or reflecting surfaces. For example, Lin et al.
(1992) have clearly demonstrated that chimpanzees are endowed with
the capacity of mirror self-recognition. They exposed chimpanzees to
mirrors and tested them for self-recognition and contingent move-
ment. They found that chimpanzees exhibited mirror-guided, mark-
directed behaviour and clear evidence of self-recognition. In the order
primates, this ability has been also observed in orangutans (Tobach et
al., 1997), gorillas (Shillito et al., 1999), and tamarins (Hauser et al.,
1995).
The capacity of mirror self-recognition is also present in non-pri-
mate mammals. Plotnik et al. (2006) exposed three Asian elephants to
a large mirror to investigate their responses. They applied visible
marks to the elephants’ heads to test whether they would pass the
‘mark test’ for mirror self-recognition in which an individual sponta-
neously uses a mirror to touch an otherwise imperceptible mark on its
own body. All the elephants in this study displayed behaviours consis-
tent with mirror self-recognition, such as bringing food to and eating
right in front of the mirror (a rare location for such activity), repeti-
tive, nonstereotypic trunk and body movements (both vertically and
horizontally) in front of the mirror, and rhythmic head movements in
and out of mirror view. Interestingly, these behaviours were not
observed in the absence of the mirror. They observed that the ele-
phants sometimes stuck their trunks into their mouths in front of the
mirror or slowly and methodically moved their trunks from the top of
the mirror surface downward. In one instance, one of the subjects put
her trunk tip into her mouth at the mirror, as if inspecting the interior
of her oral cavity, and in another instance, she used her trunk to pull
her ear slowly forward toward the mirror. One of the subjects also
passed the mark test and touched the mark on his head. Because these
behaviours were never observed in the absence of the mirror, they
indicate that this species has the capacity to recognize itself in a
mirror.
Reiss and Marino (2001) showed that dolphins also meet the crite-
ria for mirror self-recognition. They exposed two dolphins to
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reflective surfaces, and both demonstrated responses consistent with
the use of the mirror to investigate marked parts of the body.
1.3. Semantic communication
There are many examples of artificial communication systems that
have been taught to primates, by means of which the animals could
accurately and reliably report their experiences and convey semantic
information. This line of research was pioneered by Gardener and
Gardener (1969) with the chimpanzee Washoe who learned to use ges-
tures derived from the sign language of the human deaf to ask for
things or activities she wanted, answer simple questions, and identify
objects when shown their pictures. The original studies by the Gar-
deners have been extended and refined by several other investigators
during the past three decades (Fouts & Jensvold, 2002), and it is now
beyond question that apes can express simple desires and answer sim-
ple questions. Interestingly, some apes spontaneously use their
learned signaling systems to communicate with each other in the
absence of human companions, and a few have been observed to sign
to themselves when all alone.
Savage-Rumbaugh and Lewin (1994) have developed modified
computer keyboards by which apes communicate with human experi-
menters and with each other. By this type of communicative
behaviour the apes are able to identify familiar objects and persons
from their photographs, ask for things they want, including trips to
specified destinations, answer questions and request specific tools
needed for particular activities.
A clear example of semantic communication in animals is the use of
alarm calls by vervet monkeys in the wild (Griffin, 1995). These ani-
mals use acoustically distinct calls when they see three classes of dan-
gerous predators: leopards, eagles, and large snakes. Vervet monkeys
can escape from a leopard by climbing into a tree and out on the
smaller branches where the heavier leopard cannot reach them. But
this is just the wrong thing to do when threatened by an eagle that can
seize an exposed monkey on the outer branches. To escape from large
snakes, all the monkeys need to do is look around because they can
easily run away.
Seyfarth et al. (1980) conducted playback experiments showing
that vervet monkeys convey simple but semantic information by
means of their alarm calls. During the experiment, the three types of
alarm calls were played back from a hidden loudspeaker when no
predator was present, and when the monkey whose alarm calls were to
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be played back had moved out of sight in the general direction of the
loudspeaker. The result was that most of the vervet monkeys climbed
trees on hearing the leopard alarm call, rushed into thick bushes in
response to the eagle alarm, and stood up on their hind legs and looked
around on the ground when the snake alarm call was played back. One
may argue that consciousness is not necessary for, or in any way sug-
gested from, the fact that animals can communicate semantic informa-
tion because, for example, when a printer sends a signal to a computer
that there is no paper in it, the computer displays the right sort of reac-
tion without being conscious. In response to such arguments, it should
be noted that, in sharp contrast to such examples of machine commu-
nication, the above-mentioned examples of animal communication
are not stereotyped and show elements of versatility and flexibility. In
fact, there is evidence to believe that alarm calling is not a stereotyped
behaviour, because vervet monkeys occasionally withhold them
(Cheney & Seyfarth, 1990).
In the order primates, alarm calls have been also found in Diana
monkeys (Zuberbuhler, 2000), Campbell’s monkeys (Zuberbuhler,
2001), Patas monkeys (Enstam & Isbell, 2002), lemurs (Fichtel &
Kappeler, 2002), tarsiers (Gursky, 2003), sifakas (Fichtel, 2004),
baboons (Fischer et al., 2002), bonnet macaques (Ramakrishnan &
Coss, 2000), and Geoffroy’s marmosets (Searcy & Caine, 2003).
The capacity of semantic communication by means of alarm calls
has been also demonstrated in rodents. For example, it has been
shown that prairie dogs have alarm calls for four different species of
predator: hawk, human, coyote, and domestic dog (Placer &
Slobodchikoff, 2001; 2000). Interestingly, within the call type given
for humans, there is a considerable amount of variation that can be
ascribed to descriptors of body size, shape, and color of clothes
(Slobodchikoff et al., 1991). The escape responses of prairie dogs to
naturally occurring live predators differ depending upon the species
of predator; furthermore, playbacks of alarm calls that were elicited
originally by the live predators also produce the same escape
responses as the live predators themselves (Kiriazis & Slobodchikoff,
2006). The escape responses fell into two qualitatively different cate-
gories. When hawks and humans come into view, the escape response
is to run to the burrow and dive inside. When coyotes and domestic
dogs appear, the escape response typically is to run to the burrow and
stand at the lip of the burrow (for coyotes), or stand alert where forag-
ing (for domestic dogs).These responses to both the live predators and
to predator-elicited alarm calls imply that the alarm calls of prairie
ANIMAL CONSCIOUSNESS 13
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dogs contain meaningful information about the categories of preda-
tors that approach a colony of prairie dogs.
In the order Rodentia, alarm calls have been also found in many
other animal species including ground squirrels (Owings & Hennessy,
1984), tree squirrels (Greene & Meagher, 1998), marmots (Shriner,
1998), and the great gerbil (Randall et al., 2005).
There is compelling evidence that several other mammalian species
are also able to convey semantic information. For example, it has been
shown that suricates, which are small carnivorous mammals, use sev-
eral structurally distinct alarm calls for warning other group members
when predators are approaching. There is clear evidence that suricate
alarm calls contain semantic information not only about the predator
type but also about the level of urgency (Manser, 2001). Playback
experiments have indicated that call recipients are able to extract such
information when hearing a recorded call even in the absence of a
predator (Manser et al., 2001).
Dolphins have also demonstrated compelling capacities to under-
stand an artificial language and interpret untrained communicative
signs (Tschudin et al., 2001). There is clear evidence that dolphins are
capable of semantics (comprehending visual and auditory symbols as
‘words’) and syntax (understanding that changes in word order
change the meaning of a sentence) (Marino, 2004).
1.4. Tool manufacture and use
The evidence for creative tool-making and tool use is quite compel-
ling in mammals. For example, it has been observed that, in the wild,
chimpanzees often drink rainwater from the hollows of trees using
leaves as tools (Tonooka, 2001). They employ three different tech-
niques to make and use such tools to drink water. One is called ‘leaf
sponge’, where chimpanzees crumple leaves in their mouth, soak
them in a tree hollow with their hands, and suck the water from them.
The other technique is ‘leaf spoon’, where they use leaves like a
spoon, without crumpling them up, to scoop out the water. The third
technique is called ‘leaf folding’, where chimpanzees neatly fold
leaves while stuffing them into the mouth. The leaves are then soaked
in a tree hollow, and the water is sucked from the leaves when they are
removed.
There are several other accounts of tool manufacture and use by pri-
mates. Pruetz and Bertolani (2007) observed that chimpanzees make
different kind of pointed tools and use them during hunting in the
manner of a spear. Visalberghi and her colleagues (Visalberghi &
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Limongelli, 1994; Fragaszy & Visalberghi, 1989) conducted innova-
tive experiments in which a horizontal tube was presented to capuchin
monkeys, and the animals were then provided a tool (a stick) that
could be inserted into the tube to push out small pieces of candy. The
capuchins were also able to modify the tool (a stick with a small cross-
piece inserted at the end, which had to be removed for the tool to be
usable), to obtain the food reward. Westergaard (1988) observed that
lion-tailed macaques in captive social groups spontaneously manufac-
tured and used tools to extract syrup from an apparatus. In the case of
gorillas, there is also some evidence of spontaneous tool making and
use (Nakamichi, 1999; Fontaine et al., 1995).
There is also evidence of creative tool manufacture and use by
rodents such as mole rats. In the wild, naked mole-rats cooperatively
dig extensive (> 3 km) tunnels with their large, procumbent incisors in
search of food (bulbs and tubers). Shuster and Sherman (1998)
observed that captive individuals often placed a wood shaving or
tuber husk behind their incisor teeth and in front of their lips and
molar teeth while gnawing on substrates that yield fine particulate
debris. This artificial oral barrier blocked the digger’s mouth, trachea,
and esophagus and thus served to prevent choking or aspiration of
finely divided particulate debris. They observed that if the barrier
slipped out of position, the animal either readjusted it or looked for a
new one and continued gnawing, or else stopped excavating and left
the area. The mole-rats used these physical barriers when gnawing on
materials that were likely to be aspirated or to cause choking, but not
while gnawing on materials that usually crumbled into relatively large
chunks and did not produce fine debris. The use of husks and shavings
by naked mole-rats exemplifies an innovative behavioural response to
a novel challenge which is thought to require perceptual conscious-
ness. However, Shuster and Sherman argue that something even more
complex than perceptual consciousness might be present in naked
mole-rats because it seems that the animals understood the problem
they were solving and were not merely responding to oral irritation.
The latter would be the case if each excavator typically sought a husk
or shaving after having gotten particulate debris into its mouth (as
indicated, for example, by coughing, sneezing, or spitting). However,
the mole-rats always picked up a husk or shaving before commencing
to gnaw, suggesting that they had insight about the situation and
understood the problem.
There are other examples of tool use in rodents. For example, it has
been observed that a female pocket gopher clutch a stone in her
forepaws while digging, apparently to facilitate loosening and moving
ANIMAL CONSCIOUSNESS 15
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soil (Beck, 1980). Zimmerman (1952) frequently observed a captive
female harvest mouse prop an oat stalk against the side of an aquarium
and climb it to reach the wire mesh top.
Elephants are also able to use tools to achieve a goal. It has been
observed that, in the wild, fly switching with branches of trees or
shrubs is a common form of tool use in Asian elephants when fly
intensity is high. Hart et al. (2001) provided Asian elephants with
branches that were too long or bushy to be effectively used as switches
and observed that the animals modified branches to make them more
efficient for repelling flies.
1.5. Commentary key paradigm
Cowey and Stoerig (1995) developed and used a commentary key
method to test whether macaques with cortical blindness lose con-
scious visual perceptions of color and motion, which human subjects
with similar brain damage report losing.
Lesion studies demonstrate that macaques behave much like human
blindsight subjects when selected parts of the striate cortex are
removed. In order to find whether blindsighted macaques have also
lost visual conscious perceptions of color, motion, and texture, Cowey
and Stoerig used the commentary key paradigm, allowing the animals
to make a metacognitive comment about their discriminative
responses.
The commentary key is especially useful in the study of cortical
blindness, where humans can make accurate discriminations while
claiming that they do not actually see the discriminated targets con-
sciously. In the case of macaques, Cowey and Stoerig (1995) have
demonstrated that the animals can choose between two stimuli pre-
sented in their blind fields; but they cannot distinguish the chosen
stimulus from a blank trial in their intact visual field. As if monkeys
are saying, ‘we can discriminate between the two colours, but we do
not experience any difference between coloured and blank slides.’
These results imply that monkeys have conscious visual experiences
pretty much similar to humans.
1.6. Emotion
Seyfarth and Cheney (2003) reviewed the results of field experiments
on the natural vocalizations of vervet monkeys, diana monkeys,
baboons, and suricates, and found that vocalizations of these animals
not only provide others with semantic information, but also transfer
highly emotional information. In the case of elephants, there is also
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convincing evidence that they likely experience a range of emotions
such as joy, happiness, love, compassion, and respect (Poole, 1998).
Furthermore, laughter, as an affective nonspeech vocalization, has
been observed in several mammalian species, in particular monkeys
and great apes (Meyer et al., 2007). And finally, there is evidence that
rats can experience such emotions as joys (Panksepp & Burgdorf,
2003), and sheep can experience emotional states such as mood
(Greiveldinger et al., 2007).
1.7. Brain evidence
In the case of mammals, brain evidence in favor of the presence of
consciousness is quite compelling. All mammals have a highly devel-
oped thalamocortical system. Furthermore, in all mammalian species
studied so far, waking conscious state is associated with fast, irregu-
lar, and low-voltage electrical activity throughout the thalamocortical
system. In contrast, deep sleep shows slow, regular, and high-voltage
electrical activity. In fact, brain electrical activity during conscious
states is so similar in humans, monkeys, cats, dogs, and rats that these
species are routinely studied interchangeably to obtain a deeper
understanding of states of consciousness. (Baars, 2005)
2. Birds
2.1. Explicit memory
Different types of explicit memory have been described in various
species of birds. For example, Clayton and colleagues (Clayton et al.,
2003; 2001; Clayton & Dickinson, 1998) have provided strong evi-
dence that scrub jays are able to form memories for ‘what, where, and
when’ and thus exhibit all the objective attributes of episodic memory.
They first demonstrated that scrub jays can learn that a particular type
of preferred food (wax-moth larvae) become unpalatable 5 days after
the birds had stored them, but that peanuts, a less preferred food,
remain edible. The jays were trained to cache these two types of food
by burying them in sand in two different locations. When tested 4 days
after caching, and after the sand had been replaced to prevent odor
cues from affecting their choices, the jays were more likely to choose
the location they knew contained larvae. But after 5 days they usually
went where they had stored peanuts.
Zentall et al. (2001) have demonstrated that pigeons are also able to
remember specific details about their past experiences, a result consis-
tent with the notion that they have the capacity for forming episodic
memories. They chose the behaviour of pigeons as the characteristic
ANIMAL CONSCIOUSNESS 17
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of the prior event to be reported. Specifically, the behaviour to be
reported was whether the pigeon had recently pecked or had refrained
from pecking a response key. To teach them how to report their
behaviour, the pigeons were trained to choose the red comparison
stimulus if they had recently pecked an initial stimulus and to choose
the green comparison stimulus if they had recently refrained from
pecking the initial stimulus. The appropriate differential behaviour
(pecking or not pecking), which was signaled by the initial stimulus,
was required to produce the comparison stimuli. This phase of train-
ing is analogous to training the pigeons to answer the question, ‘What
did you just do?’ And the appropriate answer would be, ‘I just
pecked,’ if they chose the red comparison or ‘I just refrained from
pecking,’ if they chose the green comparison. In the second phase of
the experiment, the pigeons were exposed to a differential
autoshaping procedure designed to persuade them to peck at one stim-
ulus (a yellow response key that was always followed by food), and to
refrain from pecking another stimulus (a blue response key that was
never followed by food). With the autoshaping procedure, food fol-
lows presentation of a stimulus noncontingently but, in spite of the
fact that pecking is not required, pigeons typically peck at the stimu-
lus. Under these conditions, however, they almost never peck at a
stimulus that is never followed by reinforcement. After stable differ-
ences in pecking were established, test trials were introduced in which
a yellow or blue stimulus was followed by a choice between a red and
a green comparison. The presentation of red and green comparison
stimuli can be viewed as asking the unexpected question, ‘What did
you just do?’ In this study, Zentall and colleagues found that the
pigeons showed a significant tendency to choose the red comparison
stimulus after having pecked the yellow stimulus and to choose the
green comparison after having refrained from pecking the blue
stimulus.
There is also evidence showing that certain passerine birds store,
and then retrieve, numerous items of food in scattered locations.
These feats of memory can be astonishing. A Clark’s nutcracker may
prepare for winter by storing as many as 9000 caches of pine seeds,
which may be recovered several months later (Capaldi et al., 1999).
2.2. Semantic communication
A strong line of evidence for the communicative competence of birds
comes from the works of Irene Pepperberg on African grey parrots.
Pepperberg (1999; 1994; 1991) demonstrated that an African grey
18 M. BESHKAR
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parrot, named Alex, is not only able to imitate almost any human
words to communicate but also he understands the meanings of the
words he imitates. Pepperberg developed a special training method in
which two people talked in simple words, in Alex’s presence, about
objects in which he appeared to be interested. In this way, using social
encouragement rather than food reward, they induced him to enter
into the verbal exchanges. Alex learned to ask by spoken name for
things he liked to play with, and when queried, ‘what’s this?’ to accu-
rately say the object’s name. He later learned to answer simple ques-
tions about the color, shape, and number of objects and to answer
correctly in most cases when asked whether two things were the same
or different and if different whether in shape or colour. These commu-
nicative capabilities are not unique to Alex since Pepperberg obtained
comparable results with two other African grey parrots.
Chickadees, which are small common songbirds, produce two very
different alarm calls in response to predators: When flying raptors are
detected, chickadees produce a ‘seet’ alarm call; in response to a
perched or stationary predator, they produce a ‘chick-a-dee’alarm call
that is composed of several types of syllables. Whereas the ‘seet’
alarm call functions to warn of flying predators, the ‘chick-a-dee’
mobbing alarm call recruits other chickadees that harass, or mob, a
perched predator. Templeton et al. (2005) have shown that even subtle
variations in the ‘chick-a-dee’ mobbing calls transfer semantic infor-
mation about the size of a specific predator. Body size may be a good
predictor of risk for chickadees. Small predators (such as a northern
pygmy-owl) tend to be much more maneuverable than larger preda-
tors (such as a great horned owl) and likely pose a greater threat to
chickadees. Therefore, these vocal signals probably contain semantic
information about the degree of threat that a predator represents.
Other avian species with the ability to produce meaningful alarm
calls include white-browed scrubwrens (Platzen & Magrath, 2005),
hornbills (Rainey et al., 2004), and mallard ducklings (Miller &
Blaich, 1986).
2.3. Tool manufacture and use
In the wild, New Caledonian crows manufacture and use different
types of hook tools out of leaves and barks to probe for and prey on
invertebrates in crevices. The crows insert these hooks into cavities
and drag out prey that would otherwise be difficult or impossible to
dislodge (Hunt & Gray, 2003; Hunt, 2000a,b; 1996).
ANIMAL CONSCIOUSNESS 19
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Chappell and Kacelnik (2002) conducted experiments demonstrat-
ing that New Caledonian crows are able to choose appropriate tools,
from a range of tools available, to solve a novel problem, without
trial-and-error learning. They kept two New Caledonian crows in an
aviary where they spontaneously broke off twigs and used them to
probe into holes and crevices. When presented with a favourite food
placed in a horizontal transparent pipe open at only one end, the crows
readily inspected the position of the food in the pipe, from the side
(through the transparent walls of the pipe) and from the open end and
then picked up one of several sticks provided in the aviary, held it in
the bill and poked it into the open end of the pipe to drag out the food.
The food was placed at varying distances in the pipe, and sticks varied
widely in length. In most cases the crows successfully solved the
problem and obtained the food by choosing a stick that was just long
enough, or in a few cases longer than necessary, to reach the food.
In later experiments by Weir et al. (2002) the same two crows were
presented with food in a small bucket with a loop-shaped handle at its
top. This bucket was placed at the bottom of a transparent vertical pipe
where it could not be reached by the bird’s unaided bill. Two types of
wire were provided, one straight and the other bent to form a hook at
one end. It was much easier for the birds to obtain the food with the
hooked wire, although the male once accomplished this with a straight
wire. When only a straight wire was available, in nine out of ten trials
the female bent the straight wire to form a hook and used this success-
fully to obtain food.
Tool manufacture and use is not restricted to crows and there is evi-
dence that other avian species such as woodpecker finches also pos-
sess this capability (Tebbich et al., 2001).
2.4. Problem solving
The capacity to solve problems which seems to require higher-order
cognitive abilities have been described in several avian species. Hein-
rich (1995) investigated the degree to which hungry ravens could
understand and solve the totally novel problem presented by food sus-
pended from a string, when they had had no previous experience with
strings or string-like objects. After some time spent trying ineffective
ways to get the food, some of the ravens suddenly performed a com-
plex series of actions without any preliminary practice or reinforce-
ment. These consisted of standing on a horizontal pole from which the
food was suspended, grasping the string with the bill, pulling it up as
far as possible, then holding the string with one foot and repeating the
20 M. BESHKAR
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process five or six times until the food could be reached with the bill.
It was demonstrated long ago that birds can learn to pull strings to get
food, but this has always occurs after a long process of gradual learn-
ing effected by reinforcing each step in the process. But in Heinrich’s
experiments the ravens received no reinforcement until the whole
sequence was completed. Even more significant was a second phase
of this study. Almost every time a hungry raven succeeded in grasping
the food after the pull-and-hold procedure Heinrich frightened it so
that it flew off to another perch. Hungry ravens that have just obtained
a morsel of food ordinarily fly off with it held firmly in the bill; but the
birds that had just obtained food by the pull-and-hold procedure
dropped it before flying away. Other ravens that had obtained pieces
of food that one of their companions had pulled up did fly off with the
string still attached so that the food was pulled from their bills. There-
fore, it is plausible to suggest that the ravens not only solved the string
problem, but also understood the nature of the string and its attach-
ment to the food (Griffin, 1998).
Similarly, Pepperberg (2004) has demonstrated that grey parrots
are also able to solve the string problem. When encountered with the
problem, parrots understand that food can be retrieved by pulling
string, involving multiple pulls and the need to secure the pulled seg-
ment each time by stepping on it.
2.5. Deceptive behaviour
There are several examples of deceptive behaviours in avian species.
For example, a recent study in ravens (Bugnyar & Kotrschal, 2004)
demonstrates that these birds are capable of deliberately practicing
deception. A subordinate male first learned which of two sets of food
boxes was loaded. In the presence of a dominant male who would take
the food from him, the subordinate male then displayed diversionary
behaviour, leading the dominant male to the set of empty boxes and
then quickly returning to loaded boxes to retrieve the food while the
other bird was still distracted.
Furthermore, it has been observed that ravens try to withhold infor-
mation from conspecifics about their intentions when either caching
food or observing other ravens in order to raid their caches (Bugnyar
& Kotrschal, 2002). Those ravens who are caching food usually move
behind visual barriers to obstruct the view of those observing them,
while the latter watch from a distance and position themselves so as to
be as inconspicuous as possible to the cachers.
ANIMAL CONSCIOUSNESS 21
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2.6. Emotion
The body of evidence in favor of the presence of emotional feelings in
different members of avian species is not as strong as mammalian spe-
cies. However, there is convincing evidence that birds express emo-
tions in their songs (Bay, 1984), and that gees express grief in a way
that is pretty similar to grief in young children (Bekoff, 2000). Fur-
thermore, emotional fever, a rise in core body temperature as a result
of emotional feelings, has been recorded in fowls (Sufka & Hugues,
1991) and pigeons (Nomoto, 1996).
2.7. Brain evidence
The avian forebrain has many similarities, but also many differences
to that seen in the mammalian forebrain. However, the critical struc-
tures assumed to be necessary for consciousness in mammalian brains
(i.e., the thalamocortical system) have their homologous counterparts
in avian brains (Butler, Manger, Lindahl, & Arhem, 2005).
Like mammals, birds have a pallium, which is the dorsal part of the
telencephalon, the rostral division of the forebrain. In the pallium of
birds, a medially located hippocampal region and a laterally located
olfactory cortical region are present. In between lie two major struc-
tures, one called the Wulst, and the other called the dorsal ventricular
ridge. The Wulst and the anterior part of the dorsal ventricular ridge
(ADVR) have long been regarded as being homologous to mamma-
lian neocortex, a view supported by the evidence of similar
neurochemical traits and circuitry (Butler, 1994).
Further support for this homology comes from the fact that the
Wulst and ADVR of birds and the neocortex of mammals (with some
participation of the lateral amygdala) are clearly the sites where
highly complex cognitive behaviours are produced. Lesion and other
experiments have conclusively demonstrated the essential participa-
tion of these structures in some of these behaviours, including work-
ing memory-dependent tasks (Butler et al., 2005).
In addition to identifying anatomical structures in avian brains that
are analogous or homologous to the mammalian neocortex, it is criti-
cal to look for neurophysiological correlates of the mammalian con-
scious state. In this context, it is worth mentioning that waking avian
EEG patterns are similar to those of awake mammals. Furthermore,
slow wave electrical activity is present during sleep as well, although
the overall avian EEG pattern during sleep is noticeably different than
that of mammals (Edelman et al., 2005).
22 M. BESHKAR
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3. Bees and Spiders
3.1. Explicit memory
There is compelling evidence suggesting that bees are able to form
and recall quite complex memories about locations and recognize for-
aging areas in the past. Reinhard et al. (2006) trained marked bees to
visit two sugar feeders, each placed at a different outdoor location and
carrying a different scent. They then tested the ability of the bees to
recall these locations and fly to them, when the training scents were
blown into the hive, and the scents and food at the feeders were
removed. When trained on two feeder locations, each associated with
a different scent, the bees could correctly recall the location associated
with each scent.
Animals that forage from a nest face the problem of returning
repeatedly to specific places in the environment. Social insects, like
honeybees, must be able to move efficiently to and from a nest to for-
age. The potential foraging range of honeybees and other species of
bees is quite astonishing, approximately 10 to 15 km (Capaldi et al.,
1999). It is an extraordinary feat for animals to find a small nest from
such distances. Recent findings indicate that the memory used by bees
to navigate within the range of their orientation flights is very com-
plex and appears to allow bees to decide between at least two goals in
the field, and to steer towards the goals over considerable distances
(Menzel et al., 2006).
3.2. Semantic communication
The so-called ‘waggle dance’ of honeybees is a well-studied example
of insects’ capacity to communicate semantic information in the wild
(Griffin, 1995). By doing waggle runs, successful foragers can share
with other bees in their colony information about the direction and
distance to patches of flowers yielding nectar or pollen, and to water
sources as well as to other quite different things such as waxy sub-
stances that are used to seal gaps in the cavity where the colony is
located. The essential part of the waggle dance is a straight walking
over the vertical surface of the honeycomb during which the bee rocks
her body from side to side at a rate of about 13 per seconds. The dura-
tion and length of this straight waggle run is proportional to the dis-
tance to the source. Furthermore, the direction in which the dancer
moves during the waggle run conveys information about the direc-
tions her sisters must fly to reach the goal. The waggle dance also var-
ies in intensity; for example, a very desirable food source elicits
ANIMAL CONSCIOUSNESS 23
Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction
dozens of waggle runs, but less desirable goals are reported by only a
few dances.
In order to substantiate the notion that these waggle dances really
conveys semantic information, Gould (1976) devised an experiment
in which bees were tricked into performing waggle dances pointing in
an incorrect direction. The result was that most of the bees flew in the
direction indicated by the dances rather than to where the dancer had
actually gathered food. Another more conclusive experiment has
employed a model bee that simulates a live dancer closely enough that
some bees were recruited by its computer-controlled waggling move-
ments and simulated dance sounds. The great majority of these
recruits flew in the direction indicated by the model even though it had
never been anywhere near the goal (Michelsen et al., 1992).
3.3. Deceptive behaviour
Wilcox and Jackson (2002, 1998) have found extensive experimental
and observational evidence of complex cognition in jumping spiders
of the genus Portia, which often prey on web-building spiders. To
solve the challenge of preying on larger spiders, Portia must reach
fairly complex and suitable decisions about spatial relationships, tak-
ing long detours around obstacles to reach a favorable position even
when this necessitates losing visual contact with the goal. They
engage in a complex form of communicative exchanges with their
prey that include elements of deception. ‘They approach the web qui-
etly and set some of its threads into vibrations similar to the vibrations
used in the courtship of the web-builder. The Portia adjusts its own
vibratory signals in response to those of the web-builder in many sub-
tle ways, tending to emit a wide variety of vibratory signals but to
repeat those that attract the web-builder to the edge of the web’ (Grif-
fin & Speck, 2004, p. 13)
4. Cephalopods
4.1. Behavioural evidence
A number of behavioural studies suggest that the cephalopods possess
a rich cognitive capacity that might be considered as an indication of
consciousness. For example, there is ample evidence showing the
ability of the octopus to make discriminations between different
objects based on size, shape, and intensity (Wells & Young, 1972;
Young & Wells, 1969; Sutherland, 1969). Furthermore, cephalopods
have been shown to have highly developed attentional and memory
capacities. It has been demonstrated that octopus and cuttlefish
24 M. BESHKAR
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possess distinct capacities for short-term and long-term memory
(Agin et al., 1998; Fiorito & Chichery, 1995). In studies in which an
octopus was confronted with a maze containing obstacles that were
changed ad libidum by the researcher, the animal was able to remem-
ber these changes and readily navigate around these obstacles
(Moriyama & Gunji, 1997). These findings suggest that octopus
seems to consider the layout of the maze before proceeding. The
sophistication of the octopus’memory capabilities is also borne out by
its ability to solve problems through observational learning (not
merely through mimicry) which has been demonstrated reasonably
well (Fiorito & Scotto, 1992).
Researchers have documented evidence that cephalopods are aware
of their position, both within themselves and in larger space, including
having a working memory of foraging areas in the recent past
(Mather, 2007). Octopuses occupy a small home range for a period of
about a week and are central place foragers in the area, returning to a
sheltering home after short foraging trips. Returning to the central den
after these trips is clearly the result of spatial memory (Shettleworth,
1998) because octopuses do not retrace their outward paths. In addi-
tion, they make detours when they are displaced from these directions
(Mather, 1991). More interestingly, over a period of several days the
octopuses do not forage in areas they had recently covered, indicating
that they also had an episodic memory of where they had been.
4.2. Brain evidence
According to Edelman et al. (2005, p. 177):
in contrast to avian neuroanatomy, the organization of the cephalopod
nervous system presents an utterly unique set of problems for identify-
ing necessary structural correlates of systems underlying conscious-
ness. The search for structures in the cephalopod brain analogous to the
reentrant loops of the mammalian thalamocortical system will be par-
ticularly challenging. Where would they be?
Detailed anatomical and neurophysiological studies suggest that at
least some parts of the cephalopods brain serve a function similar to
that of the mammalian cortex. However, the anatomy of the
cephalopod brain is at this time not sufficiently characterized to iden-
tify functionally analogous structures with much confidence.
In contrast to weak anatomical evidence, perhaps the most sugges-
tive brain evidence in favor of precursor states of consciousness in at
least some members of the cephalopods is the demonstration in the
cuttlefish of EEG patterns, including event related potentials that look
ANIMAL CONSCIOUSNESS 25
Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction
quite similar to those in awake, conscious vertebrates (Bullock &
Budelmann, 1991).
Conclusion
Griffin and Speck (2004, p. 6) argues that ‘It is helpful to consider
questions about the content of an animal’s awareness in terms of the
probability of awareness, pA. If we have complete certainty that a
given animal has a particular conscious experience, then pA=1.0, and
pA=0 means that we know with certainty that it does not.’ Although
no single piece of evidence provides absolute proof of consciousness,
the accumulation of strongly suggestive evidence can serve to shift pA
upward. Demanding absolute perfection of evidence before reaching
even tentative conclusions would have seriously impeded progress in
almost every area of science, especially in the early stages of investi-
gation. Scientific investigation has often achieved substantial prog-
ress long before ideally convincing data became available, and in the
case of animal consciousness the accumulation of suggestive evi-
dence significantly increases the likelihood that some animals experi-
ence at least simple levels of consciousness (Griffin, 1998).
Regarding the evidence reviewed here, it is plausible to suggest that
the case for mammalian consciousness is quite compelling, and a little
less so for birds. As we go below this level to invertebrates, support-
ing evidence becomes increasingly less strong and more sketchy and
tenuous. However, there is still quite reasonable data to support the
notion that at least some invertebrate species such as octopuses and
bees experience simple levels of consciousness. It is noteworthy that
the lack of compelling evidence for invertebrates as compared to ver-
tebrates might be due to the fact that, in contrast to vertebrates, inver-
tebrates have been studied in less detail in terms of cognitive abilities.
The one functional property that I use to make a bridge between
consciousness and cognitive capacity is ‘flexibility’ or ‘versatility’.
One may cast doubt on the appropriateness of this criterion and ask
why consciousness should confer flexibility, and whether functions
other than consciousness (such as ‘learning’) might not also confer
versatility in the absence of consciousness. In response to such argu-
ments, it should be noted that there is convincing evidence showing
that animals can solve a novel problem spontaneously and without any
sort of trial-and-error learning. For example, consider the New Cal-
edonian crows of Chappell and Kacelnik (2002) (reviewed above)
that were able to select appropriate tools according to the needs of a
food-extraction task novel to them, without any training or experience
26 M. BESHKAR
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about the task. Another example is provided by the Heinrich’s experi-
ment in which some of ravens introduced to the food-on-string prob-
lem simply inspected the situation for a while, and then solved it
successfully on first try, without any trial-and-error (Heinrich, 1995).
At the end, it is noteworthy that in this paper I regarded sophisti-
cated types of cognitive capacities as evidence of animal conscious-
ness and, therefore, excluded from this review, those animals that lack
higher-order cognition. However, some influential neuroscientists go
beyond this frontier and believe that ‘…consciousness evolved for a
purpose other than sophisticated cognition and therefore can exist in
species without impressive cognitive capacity’ (Bjorn Merker, per-
sonal communication).
Acknowledgments
I am grateful to Drs. Colin Allen, Bjorn Merker, Matt Rossano, Daniel
Cohnitz, Manuel Bremer, and two anonymous reviewers for critical
reading of the manuscript and their insightful comments.
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