Mental States in Animals: Cognitive Ethology Jacques Vauclair

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Mental states in animals: cognitive ethology Jacques Vauclair

This artHe addresses the quegtion of mentaJ states in animak as viewed in ‘cognitive ethology”. In effect, thk field of research aims at studying naturally occurring behaviours such as food caching, individual recognition, imitation, tool use and communication in wild animals, in order to seek for evidence of mental experiences, self-aw&&reness and intentional@. Cognitive ethologists use some philosophical cencepts (e.g., the ‘intentional stance’) to carry out their programme of the investigation of natural behaviours. A comparison between cognitive ethology and other approaches to the investigation of cognitive processes in animals (e.g., experimental animal psychology) helps to point out the strengths and weaknesses of cognitive ethology. Moreover, laboratory attempts to analyse experimentally Mentional behaviours such as deception, the relationship between seeing and knowing, as well as the ability of animals to monitor their own states of knowing, suggest that cognitive ethology could benefit significantly from the conceptual frameworks and methods of animal cognitive psychology. Both disciplines could, in fact, co&ribute to the understanding of which cognitive abilities are evolutionary adaptations.

T he term ‘cognirive ethology’ (CE) was comed by that it advances a purposive or Intentional interpretation Griffin in The Question ofAnimd Au~aarmess’ and later de- for activities which are a mixture of some fixed genetically veloped in other publications’ ‘_ Although Griffin‘s IS’6 transmitred elements with more hexible behaviour?. book was first a strong (and certainly salutary) reacrion (Cognitive ethologists USC conceptual frameworks against the inhibitions imposed by strict behaviourism in provided by philosophers (such as rhe ‘intentional stance’)“. the study of animals, the book was essentially perceived as for realizing their cognitive analyses. As an illustration, an extension of ethology. with the ambitious goal ofexplor- Bennett has offered a scale for evaluating the underlying ing the conscious mental experiences of animals. Thus. by complexity ofsocial exchanges between animals” (see Fig. I); relying on achievements such as bees’ ‘language’. described in the case of social play, several levels of intentionality ate by Von Frisch’, or trained gestural communication in thus postulated. The following categorization has been chimpanzees”, Griffin concluded that these intraspecific drawn from Bekoff” : ‘0 order’ intentionality describes, for and interspecific communicarions constituted a ‘window’ example, the situation in which dog X performs a bow on to animal minds. movement: ‘first-order’ intentionality applies to the situ- Briefly, CE is concerned with claims about the evolu- ation in which dog X wantsY to play with him: ‘second- tionary and comparative study of non-human ammal cog- order’ intentionality applies to a case where X wantsY to nitive processes, consciousness. beliefs. information pro- belirz~r that Y should play with him: finally, ‘third-order’ cessing and rationality in animals-. Cognitive abilities have, intentionality qualifies the situation in which X UUMS Y to apviori, a better chance to express themselves in the natural Mew that X wants Y to play. Based on the analysis of bow environment of the species under study and. consequently, behaviours. BekofP” suggests that play-soliciting behaviours CE relies mainly on field studies. among dogs might express firsr- or perhaps second-order Several topics have thus been investigated by cognitive intentional behaviour. Alarm calls of vervet monkeys to ethologists. Two of them will be presented briefly here. The different classes of predators” have similarly been used to first topic concerns intraspecific exchanges, namely the play assess the complexity and level of communication in these intention in canids. and the second topic is related to inter- non-human primates” (for a critical evaluation of the use cd:+33491 1642 specific exchanges, namely antipredator strategies in birds. of the intentional stance in CE. see the commentaries that 73 Behaviours analysed by the cognitive ethological ap- follow Ref. 13). fax+334917149 38 proaches often pertain to activities already investigated by Ristau’ reports characreristic behaviours of a shorebird, e-mail: vauclai~lnf. more traditional ethologists; However. the novelty of CE is the piping plover (Charadviw ~~lo&s), when confronted cnrs-mrs.fr

ceptualized without reference to cognitive concepts, such as representation or memory” (but see Ref. 7), even though such concepts have amply demonstrated their usefulness and heuristic value in the comparative study of both wild and laboratory animals”~‘“~‘V. The second barrier comes from the central role assigned to consciousness in CE by some cognitive ethologists’. Although this concept has no precise meaning in CE’“, since it is envisioned’ as being synonymous with mental state, thinking or mind, it is nevertheless at the core of the phenomena that have to be elucidated. In strong contrast with the position adopted in CE, most psychologists in the field of animal cognition assume that the cognitive processes of animals are unconscious. Thus, Terrace writes: ‘Just as the modern rationale for using cognitive human terms is not based upon arguments that appeal to consciousness or to introspective reports, the rationale for the Fig. 1 A possible example of ‘second-order’ intentionality study of cognitive processes in animals requires no reference in baboons. A young baboon (A) looks at a female (T) while she eats rhizomes that A is looking for. Suddenly, A screams to animal consciousness”“. As a consequence, and in sharp loudly. thus attracting his mother’s attention: the mother B contrast to the position taken by some cognitive ethologists chases T away and the young baboon has free access to the (most notably Griffin’), comparative psychologists agree food. The interpretation of the young baboon’s behawour that even if one accepts that representations presuppose (who has previously enacted this sequence with other individuals) would be that he made his mother believe that the female conscious experience, it is not the subjective quality of the had been aggressive to him, thus leading her to intervene and experience itself that is under investigation. In fact, com- enable him to reach for the desired food (drawn by B.L Deputte; parative psychologists presume that such a subjective qual- adapted from Ref. 45). ity is impossible to assess. In effect, without at least a system of mutual understanding, it would be difficult for us, to wirh intruders perceived as potential predators: several distrac- paraphrase Nagel”‘, to envision what it is like to be a bat. tion displays have been documented to lure such predators Fortunately, the principal aim of a scientific study of the away from either the nest or young birds. The most im- minds of other animals is not to find out what it is like to be pressive of such protective behaviours is the ‘broken-wing a certain type of animal, but rather to clarify how mental display’. This behaviour can take progressive forms ranging states cause observable behaviours”‘. from a fanning tail to an awkward walk and outstretched Among the criteria retained by cognitive ethologists for arched wings that flutter and drag along the ground. From asserting the existence of mental activities in animals are: her analysis of piping plovers’ behaviours, Ristau claims” (I) the complexity of their actions; (2) their adaptive abil- that rhe conditions (adiustments to the intruder’s behaviour) ities; (3) the flexibility in the sequences of their actions and in which intense distraction displays are used are indicative (4) the anticipation of the result of their actions’. The of the purposive nature (first-order intentional analysis) of choice of such diverse indices has the disadvantage of pro- the behaviour of these birds. In other terms, according to the viding no specific research strategy to study ‘the ambas- cognitive ethologist, the plover, by performing its anti- sadors of thinking’ in animals. The conceptual imprecision predator activity, aims to lead the intruder away from the in CE has, thus, led some scholars to question the validity of nest or from the young. attributing mental experiences to animals, when it could be All ecologically relevant behaviours are potential research only a matter of mental representation”“. areas for CE. Bekoff provides a list of some of these naturally For example, UllmanL? has suggested that CE and its occurring behaviours which comprise food-caching. individ- proponents might commit rwo sophisms: the first fallacy ual recognition, imitation. tool use and communication”‘. being to identifying self-awareness with self-recognition. Ape species (orangutans, gorillas and chimpanzees; see ref- Cognitive ethology and the comparative study of erences within Ref. 23) recognize their own reflections in a cognition mirror; this was first shown by GallupL” who later specu- It must be said that the definition and scope of CE pre- lated” that self-recognition could lead to self-awareness and sented above is extensive enough to encompass other re- the ability to make inferences about the mental states of search areas, such as comparative psychology and compara- others. Self-recognition might, in fact, only express an abil- tive cognition at large”. In effect, the topics of information ity of the animal to represent its own body, or else the abil- processing, of problem solving and thought processes, to ity to use novel, displaced visual feedback about its physical name a few, are at the heart of the experimental approach of state and behaviour’“. As alternative theoretical hypotheses comparative cognition Ii Notwithstanding the convergence could possibly account for mirror recognition in apes (and in general objectives, two main obstacles have so far pre- other animals), further demonstration is required before vented a collaboration between the cognitive ethologist and concluding that these animals have human-like self-aware- the cognitive animal psychologist. First, it is very surprising ness and mental experiences.The second sophism in CE’s that the high reliance of CE on thought processes is con- position on animal thinking is related to the idea that they

Trends in Cognitive Sciences - Vol 1. No. 1, April 1997 plan future activities with conscious intentions”. It appears although they can respond to shifts in the orientation of a that anticipatory activities are at the heart of most adaptive gaze performed by a experimenter (see also Ref. 35). do not behaviours, and do not imply the intervention of inten- appear to appreciate how the eyes connect the experi- tional or conscious processes, as adaptation begins with the menter’s internal states of attention to the world. detection of regularities among environmental events. It is Altogether, the above findings point to at least TWO discrep- likely that an organism will quickly detect and anticipate ancies: (1) possible differences between monkeys and apes these regularities, as observed by Von Frischj in his studies in their respective ability to understand the perception- on insects. This author trained bees to fly towards a food knowledge relationship. and (2) possible differences be- source which changed its location from trial to trial: the tween humans and chimpanzees (as seen in the gaze- bees displayed a kind of anticipatory behaviour. Some bees following experiments) because of the difficulty for the anticipated these changes (as if they understood that the ex- non-human primate to represent the subjective attention of perimenter always placed the food beyond the last visited the other mind. location), and flew immediately to a new location where Whereas the theory of mind explores whether animals food might be found. Here again, the ability to anticipate can understand and appropriately respond to the mental could be confused with planning and conscious intention. states of conspecifics, attention can also be directed to the The question of inrentionality is, indeed, dominant in ways that animals monitor and respond to their own states CE. Interestingly, this issue has also become a controversial of knowing. This capacity to check for subjective ongoing topic within animal cognitive psychology, particularly with cognition (that is, subjective states) has recently been inves- the advent of research into ‘the theory of mind’. In this tigated in animals within the context of uncertaintv moni- field, investigators search for evidence that an individual can toring“’ “. Uncertainty can, for example. be experimentally impute intentions, desires or beliefs to himself or to con- studied in a discrimination problem. Typically. in this type specific?. Such an inquiry has led scientists to propose of experiment, the subject is presented with two primary both a working definition for intentionality and an agenda discrimination responses. The size of the stimulus differ- for carrying out experiments (more specifically among non- ences is then progressively reduced, so that the subject is human primates) to address this issue. Thus, for Woodruff confronted with difficult identifications of the stimulus, and Premack’“, intentionality can be inferred when the close to perceptual limits. At this point, the subject is given sender of a message controls the content of the message and a way to escape (a third response. the uncertain response). understands its consequences on the receiver. With such an This uncerrain response permits the subject to escape into operational framework, these authors have, for example, an easier trial but at a cost (for example. delaying a food re- conducted experiments on deception in chimpanzees (I)an ward). It is thus expected that subjects would initially try troglodytes), in a communicative setup. involving manipu- the primary discrimination response and then the escape relation of information between a chimpanzee and a human sponse when an error was likely to occur. The uncertainty experimenter. Results show that the trained chimpanzees paradigm has been used successfully for testing dolphins can both understand and produce false information, sug- (Tursiopi tmncam) in acoustical discrimination tasks”” and gesting to the authors, a real capacity for deception in the rhesus monkeys in a visual discrimination task’.. Both chimpanzee. species showed an ability to sparingly escape from the most The above experiments have been criticized on a num- difficult trials near threshold, an ability that was identical to ber of grounds, and it is questionable whether they demon- that of human participants tested in the same experimental strate an ability for true deception in the chimpanzee. For setup. Therefore, dolphins and monkeys demonstrated example, one may wonder whether the chimpanzees have both the capacity for self-knowledge and metacognitive re- really attributed sets of mental states or whether they have actions to subjective uncertaintyi’. Further studies should merely reacted to differences in behaviou?“. As Heyes com- examine if the monitoring of their own behaviours is also mented’“, the basic problem with this kind of research is to present in other animals species (comparable abilities might know whether the animals are acting on the basis of reason- also exist in rats) “I. Such directions of research should ulti- ing about observables (the ‘RO interpretation’) or mental mately help cognitive psychologists to establish the relation- states (the ‘RAM interpretation’). As a step towards choos- ships between body self-awareness, cognitive self-awareness ing between one of these interpretations, certain control and awareness of others’ mental states. experiments must be performed, an endeavour that is not systematically undertaken. Concluding remarks Other suggestions related to the presence of mental at- CE has undoubtedly contributed to the wave of interest in tributions in apes (or their absence in monkeys) are pro- exploring the complexity of the social life of animals and vided by experiments that manipulate the understanding of their ‘mental experiences’. However, this field currently causal connections between visual perception and knowl- lacks research methodology and experimental paradigms to edge formation. Such experiments have assessed in chim- fulfil its ambitious programme. Yet, these methods actually panzees” and rhesus monkeys (Macaca mulatta)” ” how an exist and they derive from human cognitive psychology and individual can understand the consequences of the visual the experimental analysis of behaviour”. Both methods experiences of others. Briefly, the results obtained indicate and concepts of the psychological approach can be used that some chimpanzees, unlike some rhesus monkeys, do with success by those biologists interested in the synthetic understand the seeing-knowing relationship. Recent inves- or ecological approach to animal behaviour”‘.“. The suc- tigations with chimpanzees ” indicate that these primates. cessful study of cognitive mechanisms involving naturally

Trends I” Cognltlve Scfencer - Vol. 1, No. 1, April 1997 Table 1. Cognitive ethology versus comparative psychology in cognition programmes

Cognitive ethology Comparative cognition

Goal The study of natural behaviours in natural The study of the generality and continuity of settings from an evolutionary and ecologtcal cognitive processes across species perspective

Scope To investigate minds, including thought To investigate information processing in processes, rationality and consciousness memory, problem solving and non-verbal thought

Methods The use of anectodes and empirical data gained Use of the methods and paradigms of with ethological techniques with many experimental psychology (e.g., reaction different species times), mostly in laboratory settings

Main issue To discover the invariants of cognitive processes To test Darwin’s gradualist hypothesis that pertain to the evolution of human concerning the continuity between human cognition minds and the minds of other animals

imporranr hehaviours has already been carried out (for qualitative observations might thus constitute a first step to example, foraging, memory in food-sroring birds, song document significant social events that could help design perception and recognition”‘, antipredator hehaviou? and experiments for later conrrol of variables in the laboratory. social play”). According to Yoerg and Kamil”. ir is now Second, as nored by Heyes and Dickinson’., the credo of time to think about animal behaviour in a more integrarive cognitive ethologists, according to which animals are less way using complementary approaches including psycho- likely to provide evidence of intentional states in the labora- logical information processing theories and methods. ethol- tory than in the field. needs to be demonstrated. The argu- ogy and hehavioural ecology (see Table 1). It can be ex- ment that hehaviours appearing in artificial environments pected that these integrated comparative approaches will are the result of a long history of training is not inconsistenr enable us to reconstruct how our own cagnirive features with the attrihution of intentionality. Moreover, we have evolved. no evidence. so far, to prove rhat mental states are formed There is a longstanding opposition between ethologists on the basis of a minimal experience (after all, behaviours of and psychologists about the respective virtues of field versus animals in free-living conditions also have a history). laboratory experiments. The former claim that field obser- The merge between laboratory and field studies might vations offer the best opportunity to see the true complexity help significantly in recognizing the importance and role of and intricacies of social exchanges at work, including inten- animal cognition within cognitive sciences. In particular, as tionaliry and attributions of belie& “‘.SF, whereas the latter, proposed by Prato Previde er al.‘“, through the study of in line with the tradition of experimental psychology and cognitive processes in an ethological perspective, research the necessity of performing control experiments and ma- on animals may shed lighr on the coupling between a cog- nipulating experimental variables, believe in laboratory nitive system and its environment, thus introducing into work’ ’ I-. cognitive science an ecological component that is truly Two points can be raised in the debate. First, social needed. phenomena cannot easily be transferred into the laboratory Finally, cognitive etholoo raises the importanr issue of and social intelligence often manifests itself in successful animal welfare and animal rights. Inevitably. repeated solutions to unusual problems”“. Use of anecdotes and quests to determine wherher animals feel, think and have mental experiences fuel the debate over animal righrs issues. Most of the time these questions are addressed by activists Outstanding questions belonging to animal rights movements (see Ref. 48 for a sig- l CE could help place the analysis of cognition within an evolutionary nificant example where activists propose that apes should be framework51,52 and thereby help us to understand the biological given full human rights). Ir is, however, astonishing that framework in which cognitive processes have evolved. those scientists who study the cognitive capacities of non- l Cognitive ethologists claim’that the consideration of individual humans (cognitive ethologists or cognitive psychologists) behaviour is often neglected in favour of the study of the behaviour of have rarely entered the debate (but see Refs 43,50), where the species. The study of a few individuals could verify the existence of strong intraspecific variations and reduce generalizations about the their data and interpretarions would be very helpful. cognitive skills of the whole species.

*The expression of cognitive abilities by animals in their environment and I.. their sensory world needs to be investigated. This growing field of References ‘sensory ecology’53 should aim at ‘taking the animals’ point of view’ by 1 Griffin, D.R. (1976) The Question of Animal Awareness. Rockefeller studying their information processing in conditions as close as possible to University Press those in which they live. 2 Griffin, D.R. (1978) Prospects for a cognitive ethology Behav. Brain Sci. 1, 527-538

Trends in Cognitive Sciences Vol 1, No. 1, April 1997 3 Griffin, D.R. (1984) Animal Thmkmg, Harvard Univewty Press edr), pp 165-185. SmIthsoman lnstitutlon Press 4 Griffin, D.R. (1992) Animal Minds, Umverrlty of Chicago Press 30 Heyes, C M (1993) Anecdotes, trapping and triangulatmg: do animals 5 Von Frisch, K. (1967) The Dance Language and Orientation of Bees. attrlbute mental states? Anrm. Eehav 46, 177-188 Harvard University Press 31 Povinelll. D.J.. Nelson. K E. and Boysen, ST. (1990) ) Inferences about 6 Gardner, R.A. and Gardner, B T (1969) Teaching s,gn language to a guewng and knowmg by chimpanzees (Pan troglodytes) J. Comp. chimpanzee Science 165. 664-672 Psycho/. 104. 203-210 7 Bekoff, M. (1995) in Behavroural Processes. Cognrtfon and Evolution 32 Pownell~. D.J.. Parks, K.A. and Novak, M.A. (1991) Do rhesus monkeys (Vol. 35) (Gervet. J.. Lassalle, J-M, Vancassel, M. and Vaucla~r. J., eds). 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Trends I” Cognitive Sciences Vol 1, No. 1. April 1997