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 brainbased 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 Correspondence: Majid Beshkar, Tehran University of Medical Sciences, Tehran, Iran. Email: [email protected]

Journal of Consciousness Studies, 15, No. 3, 2008, pp. 5–33 Copyright (c) Imprint Academic 2005 For personal use only -- not for reproduction

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vertebrates and even invertebrates, as subjects of consciousness studies will open an entirely new window and shed more light on the problem. 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 ‘consciousness’. 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 consciousness 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 varieties 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 consciousness. An individual’s past history, future plans, and consciousness 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, rendering 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 indicator of self-awareness. Mirror self-recognition is usually explored in animals by recording whether they touch a dye-marked area on visually 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 communication 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 information is perceived by other animals that hear the alarm call, they immediately 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 occurrence (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 consciousness 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 perception. 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 animals 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 consciousness 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 measures 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 anesthesia are all characterized by regular, high-amplitude, and slow voltages at less than 4 Hz. (ii) Consciousness seems to be particularly associated with the thalamocortical system. (iii) Conscious states are associated 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 correctly 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 exploration task in which different versions of the novelty-preference paradigm 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 spatially displaced ‘old familiar’ object relative to a stationary ‘old familiar’ 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 familiar’ 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 provide 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 retrospective 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 recollected 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 movement. They found that chimpanzees exhibited mirror-guided, markdirected 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-primate 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 spontaneously uses a mirror to touch an otherwise imperceptible mark on its own body. All the elephants in this study displayed behaviours consistent with mirror self-recognition, such as bringing food to and eating right in front of the mirror (a rare location for such activity), repetitive, 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 elephants 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 criteria 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 gestures 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 Gardeners 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 simple 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 experimenters 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 animals use acoustically distinct calls when they see three classes of dangerous 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 suggested from, the fact that animals can communicate semantic information 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 reaction without being conscious. In response to such arguments, it should be noted that, in sharp contrast to such examples of machine communication, 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 categories. 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 foraging (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 predators 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 several 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 understand 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 compelling 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 techniques 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 primates. 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 innovative 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 crosspiece 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 manufactured 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 consciousness. 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 conscious 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 consciously. In the case of macaques, Cowey and Stoerig (1995) have demonstrated that the animals can choose between two stimuli presented 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 developed thalamocortical system. Furthermore, in all mammalian species studied so far, waking conscious state is associated with fast, irregular, 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 evidence 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 consistent 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 training 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 stimulus (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 follows presentation of a stimulus noncontingently but, in spite of the fact that pecking is not required, pigeons typically peck at the stimulus. Under these conditions, however, they almost never peck at a stimulus that is never followed by reinforcement. After stable differences 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 accurately say the object’s name. He later learned to answer simple questions 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 communicative 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 information 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 predators (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 demonstrating 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 successfully to obtain food. Tool manufacture and use is not restricted to crows and there is evidence that other avian species such as woodpecker finches also possess 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. Heinrich (1995) investigated the degree to which hungry ravens could understand and solve the totally novel problem presented by food suspended 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 complex series of actions without any preliminary practice or reinforcement. 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 learning 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. Therefore, it is plausible to suggest that the ravens not only solved the string problem, but also understood the nature of the string and its attachment 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 segment 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 information 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 species. However, there is convincing evidence that birds express emotions in their songs (Bay, 1984), and that gees express grief in a way that is pretty similar to grief in young children (Bekoff, 2000). Furthermore, 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 structures 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 structures, 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 mammalian 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 participation of these structures in some of these behaviours, including working 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 critical to look for neurophysiological correlates of the mammalian conscious 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 foraging 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 forage. 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 complex 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 substances 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 duration and length of this straight waggle run is proportional to the distance to the source. Furthermore, the direction in which the dancer moves during the waggle run conveys information about the directions her sisters must fly to reach the goal. The waggle dance also varies 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 movements 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, taking 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 quietly 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 subtle 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’ (Griffin & 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 remember 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 addition, 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 identifying necessary structural correlates of systems underlying consciousness. The search for structures in the cephalopod brain analogous to the reentrant loops of the mammalian thalamocortical system will be particularly 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 identify functionally analogous structures with much confidence. In contrast to weak anatomical evidence, perhaps the most suggestive 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 investigation. Scientific investigation has often achieved substantial progress long before ideally convincing data became available, and in the case of animal consciousness the accumulation of suggestive evidence significantly increases the likelihood that some animals experience 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, supporting 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 vertebrates might be due to the fact that, in contrast to vertebrates, invertebrates 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 arguments, 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 Caledonian 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

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about the task. Another example is provided by the Heinrich’s experiment in which some of ravens introduced to the food-on-string problem 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 sophisticated types of cognitive capacities as evidence of animal consciousness 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, personal 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 specific 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: The evidence 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?’, Animal Behavior, 64, pp. 185–95. Bugnyar, T. & Kotrschal, K. (2004), ‘Leading a conspecific away from food in ravens (Corvus corax)?’ Animal Cognition, 7, pp. 69–76. Bullock, T.H. & Budelmann, B.U. (1991), ‘Sensory evoked potentials in unanesthetized unrestrained cuttlefish: A new preparation for brain physiology in cephalopods’ Journal of Comparative Physiology, 168, pp. 141–50. Butler A.B., (1994), ‘The evolution of the dorsal pallium in the telencephalon of amniotes: 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 the neural basis of consciousness: a bird-mammal comparison’, Bioessays, 27, pp. 923–36. Capaldi, E.A., Robinson, G.E. & Fahrbach, S.E. (1999), ‘Neuroethology of spatial learning: the birds and the bees’, Annual Review of Psychology, 50, pp. 651–82.

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Chapell, J.A. & Kacelnik, A. (2002), ‘Tool selectivity in a non-primate, the New Caledonian crow (Corvus moneduloides)’ Animal Cognition, 5, pp. 71–78. Cheney, D. L. & Seyfarth, R.M. (1990), How Monkeys See the World: Inside the Mind of Other Species (Chicago: University of Chicago Press). Clayton, N.S. & Dickinson, A. (1998), ‘Episodic-like memory during cache recovery by scrub jays’, Nature, 398, pp. 272–4. Clayton, N.S., Yu, K.S. & Dickinson, A. (2001), ‘Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes’, Journal of Experimental Psychology: Animal Behavior Processes, 27, pp. 17–29. Clayton, N.S., Yu, K.S. & Dickinson, A. (2003), ‘Interacting cache memories: evidence 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. 883–88 Dere, E., Huston, J.P. & De Souza Silva, M. A. (2005), ‘Integrated memory for objects, places and temporal order: Evidence for episodic-like memory in mice’, 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 for episodic memory in animals’, Neuroscience and Biobehavioral Reviews, 30, pp. 1206–24. Edelman, G.M. (1989), The Remembered Present: A Biological Theory of Consciousness (NewYork: Basic Books). Edelman, G.M. (2003), ‘Naturalizing consciousness: A theoretical framework’, Proceedings of the National Academy of Sciences of the United States of America, 100, pp. 5520–24. Edelman, G. M. (2004), Wider than the Sky: The Phenomenal Gift of Consciousness (Yale University Press). Edelman, D.B., Baars, B.J. & Seth, A.K. (2005), ‘Identifying hallmarks of consciousness in non-mammalian species’, Consciousness and Cognition, 14, pp. 169–87. Enstam, K.L. & Isbell, L.A. (2002), ‘Comparison of responses to alarm calls by patas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys in relation to habitat structure’, American Journal of Physical Anthropology, 119, pp. 3–14. Fichtel, C. (2004), ‘Reciprocal recognition of sifaka (Propithecus verreauxi verreauxi) and redfronted lemur (Eulemur fulvus rufus) alarm calls’, Animal Cognition, 7, pp. 45–52. Fichtel, C. & Kappeler, P.M. (2002), ‘Referential alarm calls in lemurs’, Behavioral Ecology and Sociobiology, 51, pp. 267–75. Fiorito, G.P. & Scotto, P. (1992), ‘Observational learning in Octopus vulgaris’, Science, 256, pp. 545–74. Fiorito, G. & Chichery, R. (1995), ‘Lesions of the vertical lobe impair visual discrimination learning by observation in Octopus vulgaris’ Neuroscience Letters, 192, pp. 117–20. Fischer, J., Hammerschmidt, K., Cheney, D.L. & Seyfarth, R.M. (2002), ‘Acoustic features of male baboon loud calls: influences of context, age, and individuality’, Journal of Acoustical Society of America, 111, pp. 1465–74.

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Paper received August 2007

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