Animal Consciousness

29
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 2010 For personal use only -- not for reproduction

Transcript of Animal Consciousness

Page 1: Animal Consciousness

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

Page 2: Animal Consciousness

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-

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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

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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

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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

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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

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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

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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

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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

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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

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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).

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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

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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.

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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).

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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

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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

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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

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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.

References

Agin, V., Dickel, L., Chichery, R. & Chichery, M.P. (1998), ‘Evidence for a spe-cific short-term memory in the cuttlefish, Sepia’, Behavioral Processes, 43, pp.329–34.

Baars, B.J. (2005), ‘Subjective experience is probably not limited to humans: Theevidence from neurobiology and behavior’, Consciousness and Cognition, 14,pp. 7–21.

Bay J.C. (1984), ‘Expressions of emotion in birds’ song’, Science, 23, p. 53.Beck, B.B. (1980), Animal Tool Behavior: The Use and Manufacture of Tools by

Animals (New York: Garland).Bekoff, M. (2000), ‘Animal emotions: Exploring passionate natures’, Bioscience,

50, pp. 861–70.Bugnyar, T. & Kotrschal, K. (2002), ‘Observational learning and the raiding of

food caches in ravens, Corvus corax: Is it ‘‘tactical’’ deception?’, AnimalBehavior, 64, pp. 185–95.

Bugnyar, T. & Kotrschal, K. (2004), ‘Leading a conspecific away from food inravens (Corvus corax)?’ Animal Cognition, 7, pp. 69–76.

Bullock, T.H. & Budelmann, B.U. (1991), ‘Sensory evoked potentials inunanesthetized unrestrained cuttlefish: A new preparation for brain physiologyin cephalopods’ Journal of Comparative Physiology, 168, pp. 141–50.

Butler A.B., (1994), ‘The evolution of the dorsal pallium in the telencephalon ofamniotes: Cladistic analysis and a new hypothesis’, Brain Research Reviews,19, pp. 66–101.

Butler, A.B., Manger, P.R., Lindahl, B.I.B. & Arhem, P. (2005), ‘Evolution of theneural basis of consciousness: a bird-mammal comparison’, Bioessays, 27, pp.923–36.

Capaldi, E.A., Robinson, G.E. & Fahrbach, S.E. (1999), ‘Neuroethology of spatiallearning: the birds and the bees’, Annual Review of Psychology, 50, pp. 651–82.

ANIMAL CONSCIOUSNESS 27

Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction

Page 24: Animal Consciousness

Chapell, J.A. & Kacelnik, A. (2002), ‘Tool selectivity in a non-primate, the NewCaledonian crow (Corvus moneduloides)’ Animal Cognition, 5, pp. 71–78.

Cheney, D. L. & Seyfarth, R.M. (1990), How Monkeys See the World: Inside theMind of Other Species (Chicago: University of Chicago Press).

Clayton, N.S. & Dickinson, A. (1998), ‘Episodic-like memory during cacherecovery by scrub jays’, Nature, 398, pp. 272–4.

Clayton, N.S., Yu, K.S. & Dickinson, A. (2001), ‘Scrub jays (Aphelocomacoerulescens) form integrated memories of the multiple features of caching epi-sodes’, Journal of Experimental Psychology: Animal Behavior Processes, 27,pp. 17–29.

Clayton, N.S., Yu, K.S. & Dickinson, A. (2003), ‘Interacting cache memories: evi-dence for flexible memory use by western scrub-jays (Aphelocoma californica)’Journal of Experimental Psychology: Animal Behavior Processes, 29, pp. 14–22.

Cowey, A. & Stoerig, P. (1995), ‘Blindsight in monkeys’, Nature, 373, pp. 247–9.Crick, F. & Koch, C. (1990), ‘Towards a neurobiological theory of consciousness’,

Seminars in the Neurosciences, 2, pp. 263–75.Dawkins M.S. (2000), ‘Animal minds and animal emotions’, American Zoologist,

40, pp. 883–88Dere, E., Huston, J.P. & De Souza Silva, M. A. (2005), ‘Integrated memory for

objects, places and temporal order: Evidence for episodic-like memory inmice’, Neurobiology of Learning and Memory, 84, pp. 214–21.

Dere, E., Kart-Teke, E., Huston, J.P. & De Souza Silva, M.A. (2006), ‘The case forepisodic memory in animals’, Neuroscience and Biobehavioral Reviews, 30, pp.1206–24.

Edelman, G.M. (1989), The Remembered Present: A Biological Theory of Con-sciousness (NewYork: Basic Books).

Edelman, G.M. (2003), ‘Naturalizing consciousness: A theoretical framework’,Proceedings of the National Academy of Sciences of the United States of Amer-ica, 100, pp. 5520–24.

Edelman, G. M. (2004), Wider than the Sky: The Phenomenal Gift of Conscious-ness (Yale University Press).

Edelman, D.B., Baars, B.J. & Seth, A.K. (2005), ‘Identifying hallmarks of con-sciousness in non-mammalian species’, Consciousness and Cognition, 14, pp.169–87.

Enstam, K.L. & Isbell, L.A. (2002), ‘Comparison of responses to alarm calls bypatas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys inrelation to habitat structure’, American Journal of Physical Anthropology, 119,pp. 3–14.

Fichtel, C. (2004), ‘Reciprocal recognition of sifaka (Propithecus verreauxiverreauxi) and redfronted lemur (Eulemur fulvus rufus) alarm calls’, AnimalCognition, 7, pp. 45–52.

Fichtel, C. & Kappeler, P.M. (2002), ‘Referential alarm calls in lemurs’, Behav-ioral Ecology and Sociobiology, 51, pp. 267–75.

Fiorito, G.P. & Scotto, P. (1992), ‘Observational learning in Octopus vulgaris’, Sci-ence, 256, pp. 545–74.

Fiorito, G. & Chichery, R. (1995), ‘Lesions of the vertical lobe impair visual dis-crimination learning by observation in Octopus vulgaris’ Neuroscience Letters,192, pp. 117–20.

Fischer, J., Hammerschmidt, K., Cheney, D.L. & Seyfarth, R.M. (2002), ‘Acousticfeatures of male baboon loud calls: influences of context, age, and individual-ity’, Journal of Acoustical Society of America, 111, pp. 1465–74.

28 M. BESHKAR

Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction

Page 25: Animal Consciousness

Fontaine, B., Moisson, P.Y. & Wickings, E.J. (1995), ‘Observations of spontane-ous tool making and tool use in a captive group of western lowland gorillas(Gorilla gorilla gorilla)’, Folia Primatologica, 65, pp. 219–23.

Fouts, R.S. & Jensvold, M.L.A. (2002), ‘Armchair dilusions versus empirical real-ities: a neurological model for the continuity of ape and human languaging’, inM. Goodman & M.L.A. Moffat (Eds.), Probing Human Origins (Cambridge,MA: American Academy of Arts and Sciences) pp. 87–101.

Fragaszy, D.M., & Visalberghi, E. (1989), ‘Social influences on the acquisition oftool-using behaviors in tufted capuchin monkeys (Cebus apella)’, Journal ofComparative Psychology, 103, pp. 159–70.

Gardener, R.A. & Gardener, B.T. (1969), ‘Teaching sign language to a chimpan-zee’, Science, 165, pp. 664–72.

Gould J.L. (1976), ‘The dance language controversy’, Quarterly Review of Biol-ogy, 51, pp. 211–24.

Greene, E. & Meagher, T. (1998), ‘Red squirrels, Tamiasciurus hudsonicus, pro-duce predator-specific alarm calls’, Animal Behavior, 55, pp. 511–18.

Greiveldinger, L., Veissier, I. & Boissy, A. (2007), ‘Emotional experience insheep: Predictability of a sudden event lowers subsequent emotionalresponses’, Physiology and Behavior, 92, pp. 675–83.

Griffin, D.R. (1995), ‘Windows on animal minds’, Consciousness and Cognition,4, pp. 194–204.

Griffin, D.R. (1998), ‘From cognition to consciousness’, Animal Cognition, 1, pp.3–16.

Griffin, D.R. & Speck, G.B. (2004), ‘New evidence of animal consciousness’, Ani-mal Cognition, 7, pp. 5–18.

Gursky, S. (2003), ‘Predation experiments on infant spectral tarsiers (Tarsius spec-trum)’, Folia Primatologica (Basel), 74, pp. 272–84.

Hart, B.L., Hart, L.A., McCoy, M. & Sarath, C.R. (2001), ‘Cognitive behavior inAsian elephants: Use and modification of branches for fly switching’, AnimalBehavior, 62, pp. 839–47.

Hauser, M.D., Kralik, J., Botto-Mahan, C., Garrett, M. & Oser, J. (1995), ‘Self-recognition in primates: phylogeny and the salience of species-typical features’,Proceedings of the National Academy of Sciences of the United States of Amer-ica, 92, pp. 10811–14.

Heinrich, B. (1995), ‘An experimental investigation of insight in common ravens(Corvus corax)’, Auk, 112, pp. 994–1003.

Hunt, G.R. (1996), ‘Manufacture and use of hook-tools by New Caledonian crows(Corvus moneduloides)’, Nature, 379, pp. 249–51.

Hunt, G.R. (2000a), ‘Tool use by the New Caledonian crow (Corvus monedu-loides) to obtain Cerambycidae from dead wood’, Emu, 100, pp. 109–14.

Hunt, G. R. (2000b), ‘Human-like, population-level specialization in the manufac-ture of pandanus tools by New Caledonian crows Corvus moneduloides’, Pro-ceedings of the Royal Society B: Biological Sciences, 267, pp. 403–13.

Hunt, G.R. & Gray, R.D. (2003), ‘Diversification and cumulative evolution in NewCaledonian crow tool manufacture’, Proceedings of the Royal Society B: Bio-logical Sciences, 270, pp. 867–74.

Kart-Teke, E., De Souza Silva, M.A., Huston, J.P. & Dere, E. (2006), ‘Wistar ratsshow episodic-like memory for unique experiences’, Neurobiology of Learningand Memory, 85, pp. 173–82.

Kiriazis, J. & Slobodchikoff, C.N. (2006), ‘Perceptual specificity in the alarm callsof Gunnison’s prairie dogs’, Behavioral Processes, 73, pp. 29–35.

ANIMAL CONSCIOUSNESS 29

Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction

Page 26: Animal Consciousness

Lin, A.C., Bard, K.A. & Anderson, J.R., (1992), ‘Development of self-recognitionin chimpanzees (Pan troglodytes)’, Journal of Comparative Psychology, 106,pp. 120–27.

Manser, M. B. (2001), ‘The acoustic structure of suricates’ alarm calls varies withpredator type and the level of response urgency’, Proceedings of Biological Sci-ences, 268, pp. 2315–24.

Manser, M.B., Bell, M.B. & Fletcher, L.B. (2001), ‘The information that receiversextract from alarm calls in suricates’ Proceedings of Biological Sciences, 268,pp. 2485–91.

Marino, L. (2004), ‘Dolphin cognition’, Current Biology, 14, pp. 910–11.Mather, J.A. (1991), ‘Foraging, feeding and prey remains in middens of juvenile

Octopus vulgaris (mollusca, cephalopoda)’, Journal of Zoology London, 224,pp. 27–39.

Mather, J.A. (2007), ‘Cephalopod consciousness: Behavioural evidence’, Con-sciousness and Cognition, doi:10.1016/j.concog.2006.11.006.

Menzel, R., De Marco, R.J. & Greggers, U. (2006), ‘Spatial memory, navigationand dance behaviour in Apis mellifera’, Journal of Comparative Physiology A.Neuroethology, Sensory, Neural, and Behavioral Physiology, 192, pp. 889–903.

Mercado, E., Murray, S.O., Uyeyama, R.K., Pack, A.A. & Herman, L.M. (1998),‘Memory for recent actions in the bottlenosed dolphin (Tursiops truncates),Repetition of arbitrary behaviors using an abstract rule’, Animal Learning andBehavior, 26, pp. 210–18.

Meyer, M., Baumann, S., Wildgruber, D. & Alter, K. (2007), ‘How the brainlaughs: Comparative evidence from behavioral, electrophysiological andneuroimaging studies in human and monkey’, Behavioral Brain Research, 182,pp. 245–60.

Michelsen, A., Andersen, B.B., Storm, J., Kirchner, W.H. & Lindauer, M. (1992),‘How honeybees perceive communication dances, studied by means of amechanical model’, Behavioral Ecology and Sociobiology, 30, pp. 143–50.

Miller, D.B., & Blaich, C.F. (1986), ‘Alarm call responsivity of mallard ducklings:III. Acoustic features affecting behavioral inhibition’, DevelopmentalPsychobiology, 19, pp. 291–301.

Morin, A. (2006), ‘Levels of consciousness and self-awareness: A comparison andintegration of various neurocognitive views’, Consciousness and Cognition, 15,pp. 358–71.

Moriyama, T. & Gunji, Y.P. (1997), ‘Autonomous learning in maze solution byoctopus’, Ethology, 103, pp. 499–513.

Nakamichi, M. (1999), ‘Spontaneous use of sticks as tools by captive gorillas’,Primates, 40, pp. 487–98.

Nomoto, S. (1996), ‘Diurnal variations in fever induced by intravenous LPS injec-tion in pigeons’, Pflüg Arch., 431, pp. 987–89.

Owings, D.H. & Hennessy, D.F. (1984), ‘The importance of variation in sciuridvisual and vocal communication’, in J.O. Murie & G.R. Michener (Eds.), TheBiology of Ground Dwelling Squirrels (Lincoln: University of Nebraska Press)pp. 171–200.

Panksepp, J. & Burgdorf, J. (2003), ‘“Laughing” rats and the evolutionary ante-cedents of human joy?’, Physiology and Behavior, 79, pp. 533–47.

Pepperberg, I.M. (1991), ‘A communicative approach to animal cognition: A studyof conceptual abilities of an African grey parrot’, in C.A. Ristau (Ed.), CognitiveEthology: The Minds of Other Animals (Hillsdale, NJ: Erlbaum) pp. 153–86.

Pepperberg, I.M. (1994), ‘Vocal learning in grey parrots (Psittacus erithacus):Effects of social interaction, reference, and context’, Auk, 111, pp. 300–13.

30 M. BESHKAR

Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction

Page 27: Animal Consciousness

Pepperberg, I.M. (1999), The Alex studies, Cognitive and Communicative Abilitiesof Grey Parrots (Cambridge, MA: Harvard University Press).

Pepperberg, I.M. (2004), ‘Insightful string-pulling in grey parrots (Psittacuserithacus) is affected by vocal competence’, Animal Cognition, 7, pp. 263–66.

Placer, J. & Slobodchikoff, C.N. (2000), ‘A fuzzy-neural system for identificationof species-specific alarm calls of Gunnison’s prairie dogs’, Behavioral Pro-cesses, 52, pp. 1–9.

Placer, J. & Slobodchikoff, C.N. (2001), ‘Developing new metrics for the investi-gation of animal vocalizations’, Intelligent Automation and Soft Computing, 7,pp. 1–11.

Platzen, D. & Magrath, R.D. (2005), ‘Adaptive differences in response to twotypes of parental alarm call in altricial nestlings’, Proceedings of Biological Sci-ences, 272, pp. 1101–6.

Plotnik, J.M., de Waal, F.B. & Reiss, D. (2006), ‘Self-recognition in an Asian ele-phant’, Proceedings of the National Academy of Sciences of the United States ofAmerica, 103, pp. 17053–57.

Poole, J. (1998), ‘An exploration of a commonality between ourselves and ele-phants’, Etica and Animali, 9, pp. 85–110.

Pruetz, J.D. & Bertolani, P. (2007), ‘Savanna chimpanzees, Pan troglodytes verus,hunt with tools’, Current Biology, 17, pp. 412–17.

Rainey, H.J., Zuberbühler, K. & Slater, P.J. (2004), ‘Hornbills can distinguishbetween primate alarm calls’, Proceedings of Biological Sciences, 271, pp.755–9.

Ramakrishnan, U. & Coss, R.G. (2000), ‘Recognition of heterospecific alarmvocalizations by bonnet macaques (Macaca radiata)’, Journal of ComparativePsychology, 114, pp. 3–12.

Randall, J.A., McCowan, B., Collins, K.C., Hooper, S.L. & Rogovin, K. (2005),‘Alarm signals of the great gerbil: Acoustic variation by predator context, sex,age, individual, and family group’, Journal of Acoustical Society of America,118, pp. 2706–14.

Reinhard, J., Srinivasan, M.V. & Zhang S. (2006), ‘Complex memories in honey-bees: Can there be more than two?’, Journal of Comparative Physiology A.Neuroethology, Sensory, Neural, and Behavioral Physiology, 192, pp. 409–16.

Reiss, D. & Marino, L. (2001), ‘Mirror self-recognition in the bottlenose dolphin:A case of cognitive convergence’, Proceedings of the National Academy of Sci-ences of the United States of America, 98, pp. 5937–42.

Savage-Rumbaugh, E.S. & Lewin, R. (1994), Kanzi: The Ape at the Brink of theHuman Mind (New York; Wiley).

Schwartz, B.L., Colon, M.R., Sanchez, I.C., Rodriguez, I.A. & Evans, S. (2002),‘Single-trial learning of “what” and “who” information in a gorilla (Gorillagorilla gorilla): Implications for episodic memory’, Animal Cognition, 5, pp.85–90.

Schwartz, B.L., Hoffman, M.L. & Evans, S. (2005), ‘Episodic-like memory in agorilla: A review and new findings’ Learning and Motivation, 36, pp. 226–44.

Schwartz, B.L., Meissner, C.M., Hoffman, M., Evans, S. & Frazier, L.D. (2004),‘Event memory and misinformation effects in a gorilla (Gorilla gorilla gorilla)’,Animal Cognition, 7, pp. 93–100.

Searcy, Y.M. & Caine, N. G. (2003), ‘Hawk calls elicit alarm and defensive reac-tions in captive Geoffroy’s marmosets (Callithrix geoffroyi)’, FoliaPrimatologica (Basel), 74, pp. 115–25.

Seth, A.K., Baars, B.J. & Edelman, D.B. (2005), ‘Criteria for consciousness inhumans and other mammals’, Consciousness and Cognition, 14, pp. 119–39.

ANIMAL CONSCIOUSNESS 31

Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction

Page 28: Animal Consciousness

Seyfarth R.M. & Cheney D.L. (2003), ‘Meaning and emotion in animal vocaliza-tions’, Annals of the New York Academy of Science, 1000, pp. 32–55.

Seyfarth, R.M., Cheney, D.L. & Marler, P. (1980), ‘Vervet monkey alarm calls:Evidence for predator classification and semantic communication’, AnimalBehavior, 28, pp. 1070–94.

Shettleworth, S.J. (1998), Cognition, Evolution, and Behavior (New York: OxfordUniversity Press).

Shillito, D.J., Gallup, G.G. & Beck, B.B. (1999), ‘Factors affecting mirror behav-ior in western lowland gorillas’, Animal Behavior, 57, pp. 999–1004.

Shriner, W.M. (1998), ‘Yellow-bellied marmot and golden-mantled ground squir-rel responses to heterospecific alarm calls’, Animal Behavior, 55, pp. 529–36.

Shuster, G. & Sherman, P.W. (1998), ‘Tool use by naked mole-rats’, Animal Cogni-tion, 1, pp. 71–74.

Slobodchikoff, C.N., Kiriazis, J., Fischer, C. & Creef, E. (1991), ‘Semantic infor-mation distinguishing individual predators in the alarm calls of Gunnison’s prai-rie dogs’, Animal Behavior, 42, pp. 713–19.

Sufka, K.J. & Hugues, R.A. (1991), ‘Differential effects of handling on isola-tion-induced vocalizations, hypoalgesia, and hyperthermia in domestic fowl’,Physiology and Behavior, 50, pp. 123–33.

Sutherland, N. S. (1969), ‘Shape discrimination in rat, octopus, and goldfish: Acomparative study’, Journal of Comparative Physiology and Psychology, 67,pp. 60–176.

Tebbich, S., Taborsky, M., Fessl, B. & Blomqvist, D. (2001), ‘Do woodpeckerfinches acquire tool-use by social learning?’, Proceedings of the Royal SocietyB: Biological Sciences, 268, pp. 2189–93.

Templeton, C.N., Greene, E. & Davis, K. (2005), ‘Allometry of alarm calls:Black-capped chickadees encode information about predator size’, Science,308, pp. 1934–37.

Tobach, E., Skolnick, A.J., Klein, I. & Greenberg, G., (1997), ‘Viewing of self andnonself images in a group of captive orangutans (Pongo pygmaeus Abellii)’,Perceptual and Motor Skills, 84, pp. 355–70.

Tonooka, R. (2001), ‘Leaf-folding behavior for drinking water by wild chimpan-zees (Pan troglodytes) at Bossou, Guinea’, Animal Cognition, 4, pp. 325–34.

Tschudin, A., Call, J., Dunbar, R.I., Harris, G. & van der Elst, C. (2001), ‘Compre-hension of signs by dolphins (Tursiops truncatus)’, Journal of ComparativePsychology, 115, pp. 100–5.

Visalberghi, E. & Limongelli, L. (1994), ‘Lack of comprehension of cause-effectrelations in tool-using capuchin monkeys (Cebus apella)’, Journal of Compara-tive Psychology, 108, pp. 15–22.

Weir, A.A.S., Chappell, J. & Kacelnik, A. (2002), ‘Shaping of hooks in New Cal-edonian crows’, Science, 297, p. 981.

Weiskrantz, L. (1999), Consciousness Lost and Found (Oxford: Oxford Univer-sity Press).

Weiskrantz, L. (1991), ‘Disconnected awareness for detecting, processing, andremembering in neurological patients’, Journal of the Royal Society of Medi-cine, 84, pp.466–70.

Wells, M.J. & Young, J.Z. (1969), ‘The effect of splitting part of the brain orremoval of the median inferior frontal lobe on touch learning in octopus’, Jour-nal of Experimental Biology, 56, pp. 381–402.

Wells, M.J. & Young, J.Z. (1972), ‘The median inferior frontal lobe and touchlearning in the octopus’, Journal of Experimental Biology, 56, pp. 381–402.

32 M. BESHKAR

Copyright (c) Imprint Academic 2010For personal use only -- not for reproduction

Page 29: Animal Consciousness

Westergaard, G.C. (1988), ‘Lion-tailed macaques (Macaca silenus) manufactureand use tools’, Journal of Comparative Psychology, 102, pp. 152–9.

Wilcox, R.S. & Jackson, R.R. (1998), ‘Cognitive abilities of Areneophagic jump-ing spiders’, in R.P. Balda, I.M. Pepperberg, & A.C. Kamil. (Eds.) Animal Cog-nition in Nature: The Convergence of Psychology and Biology in Laboratoryand Field (San Diego, CA: Academic) pp. 411–34.

Wilcox, S. & Jackson, R. (2002), ‘Jumping spider tricksters: Deceit, predation,and cooperation’, in M. Bekoff, C. Allen & G.M. Burghardt (Eds.), The Cogni-tive Animal: Empirical and Theoretical Perspectives on Animal Cognition(Cambridge, MA: MIT Press) pp. 27-45.

Zentall, T.R., Clement, T.S., Bhatt, R.S. & Allen, J. (2001), ‘Episodic-like mem-ory in pigeons’, Psychonomic Bulletin & Review, 8, pp. 685–90.

Zimmerman, K. (1952), ‘Werkzeug-Benutzung durch eine Zwergmaus’Zeitschriftfur Tierpsychologie, 9, p. 12.

Zuberbuhler, K. (2000), ‘Referential labeling in Diana monkeys’, Animal Behav-ior, 59, pp. 917–27.

Zuberbuhler, K. (2001), ‘Predator-specific alarm calls in Campbell’s guenons’,Behavioral Ecology and Sociobiology, 50, pp. 414–22.

Paper received August 2007

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