NATURALIZING ANIMAL MINDS
Comparative cognitive ethology is an important extension of classical ethology because it explicitly licenses hypotheses about the internal states of animals in the tradition of classical ethologists such as Nobel laureates Niko Tinbergen and Konrad Lorenz. However, although ethologists such as Lorenz and Tinbergen used terms such as "intention movements," they used them quite differently from how they are used in the philosophical literature. "Intention movements" refers to preparatory movements that might communicate what action individuals are likely to do next, and not necessarily to their beliefs and desires, although one might suppose that the individuals did indeed want to fly and believed that if they moved their wings in a certain way they would fly. This distinction is important to mark because the use of such terms does not necessarily add a cognitive dimension to classical ethological notions, although it could.
In his early work Tinbergen identified four overlapping areas with which ethological investigations should be concerned -- namely, evolution (phylogeny), adaptation (function), causation, and development (ontogeny), and his framework also is useful for those interested in animal cognition (Jamieson and Bekoff, 1993). The methods for answering questions in each of these areas vary, but all begin with careful observation and description of the behavior patterns that are performed by the animals under study. The information afforded by these initial observations allows a researcher to exploit the animal's normal behavioral repertoire to answer questions about the evolution, function, causation, and development of the behavior patterns that are performed in various contexts.
Donald R. Griffin and modern cognitive ethology
The modern era of cognitive ethology and its concentration on the evolution and evolutionary continuity of animal cognition is usually thought to have begun with the appearance of Donald R. Griffin's (1976/1981) book The Question of Animal Awareness: Evolutionary Continuity of Mental Experience. Griffin's major concern was to learn more about animal consciousness, and then, as now, Griffin wanted to come to terms with the difficult question of "what is it like to be a particular animal?" (for critical discussion of Griffin's agenda see Jamieson and Bekoff, 1993). While Griffin was mainly concerned with the phenomenology of animal consciousness, it is only one of many important and interesting aspects of animal cognition (Allen and Bekoff, 1997). Indeed, because of its broad agenda and wide-ranging goals, many view cognitive ethology as being a genuine contributor to cognitive science in general. For those who are anthropocentrically minded, it should be noted that studies of animal cognition can also inform, for example, inquiries into human autism.
METHODS OF STUDY
The tractability of cognitive questions involves application of a diverse set of comparative methods in order to draw inferences about cognitive states and capacities. Cognitive research may include staged social encounters, playback of recorded vocalizations, the presentation of stimuli in different modalities, observation of predator-prey interactions, observation of foraging behavior, neurobiological techniques, and studies of social and other sorts of learning. Computer analyses also are useful for those who want to learn what kind of information must be represented in an adequate computational model.
There are no large differences between methods used to study animal cognition and those used to study other aspects of animal behavior. Differences lie not so much in what is done and how it is done, but rather how data are explained. Allen and Bekoff (1997) argue that the main distinction between cognitive ethology and classical ethology lies not in the types of data collected, but in the understanding of the conceptual resources that are appropriate for explaining those data.
Perhaps one area that will contribute more to the study of animal minds than it does to other areas of comparative ethology is neurobiology and behavior. Those interested in the cellular or neural bases of behavior and animal cognition and consciousness may use techniques such as positron emission tomography (PET) that are also employed in other endeavors. In general, studies using brain imaging (see APPLICATIONS OF NEUROIMAGING TO THE STUDY OF COGNITION) have provided extremely valuable data for humans engaged in various sorts of activities, whereas the use of these and other imaging techniques on animals has not been pursued rigorously for individuals engaged in activities other than learning or memory in captivity. Furthermore, while neurobiological studies are extremely important to those interested in animal cognition, there remains an explanatory gap between neurophysiological processes and behavior.
Behavioral studies usually start with the observation, description, and categorization of behavior patterns that animals perform. The result of this process is the development of an ethogram, or behavioral catalogue, of these actions. Ethograms present information about an action's form or morphology and its code name. Descriptions can be based on visual information (what an action looks like), auditory characteristics (sonograms, which are pictures of sounds), or chemical constituents (output of chromatographic analyses of glandular deposits or urine or feces, for example). It is essential that great care be given to the development of an ethogram, for it is an inventory that others should be able to replicate without error. Permanent records of observations allow others to cross-check their observations and descriptions against original records. The number of actions and the breadth of categories that are identified in a behavioral study depends on the questions at hand, but generally it is better to split rather than to lump actions in initial stages, and lump when questions of interest have been carefully laid out.
In studies of behavior it is important to know as much as possible about the sensory world of the animals being studied. Experiments should not be designed that ask animals to do things that they cannot do because they are insensitive to the experimental stimuli or unmotivated by the stimuli. The relationships between normal ecological conditions and differences between the capabilities of animals to acquire, process, and respond to information is the domain of a growing field called "sensory ecology". A good ethologist asks "what is it like to be the animal under study" and develops an awareness of the senses that the animals use singly or in combination with one another. It is highly unlikely that individuals of any other species sense the world the same way we do, and it is unlikely that even members of the same species sense the world identically all of the time, and it is important to remain alert to the possibility of individual variation.
Stimulus control and impoverished environments
While carefully conducted experiments in the laboratory and in the field often are able to control for the influence of variables that might affect the expression of behavioral responses, it is usually the case that there is a possibility that the influence of some variable(s) cannot be accounted for. Field studies may be more prone to a lack of control because the conditions in which they are conducted are inherently more complex and less controllable.
An illustration of the concern for undercontrol is found in the excellent cognitive ethological field research of Cheney and Seyfarth (1990) on the behavior (e.g. communication and deception) and minds of vervet monkeys. In their studies of the attribution of knowledge by vervets to each other, Cheney and Seyfarth played back vocalizations of familiar individuals to other group members. These researchers were, however, concerned about their inability to eliminate "all visual or auditory evidence of the [familiar] animal's physical presence" (p. 230). Actually, this inability may not be problematic if the goal is to understand "how monkeys see the world." Typically, in most social situations the physical presence of individuals and access to stimuli from different modalities may be important to consider. Vervets, other nonhumans, and humans may attribute mental states using a combination of variables that are difficult to separate experimentally. Negative or inconclusive experimental results concerning vervets' or other animals' attribution of mind to other individuals may stem from impoverishing their normal environment by removing information that they normally use in attribution. Researchers might also be looking for complex mechanisms involved in the attribution of minds to others and might overlook relatively simple means for doing so. Just because an animal does not do something does not mean that it cannot do it (assuming that what we are asking the animal to do is reasonable, that is within their sensory and motor capacities). Thus, insistence on absolute experimental control that involves placing and maintaining individuals in captivity and getting them accustomed to test situations that may be unnatural may greatly influence results. And these sorts of claims, if incorrect, can wreak havoc on discussions of the evolutionary continuity of animal cognitive skills. Cheney and Seyfarth recognize some of these problems in their discussion of the difficulties of distinguishing between alternative explanations maintaining either that a monkey recognizes another's knowledge or a monkey monitors another's behavior and adjusts his own behavior to the other.
Although control may be more of a problem in field research than in laboratory work, it certainly is not the case that cognitives ethologist should abandonfield work. Cognitive ethologists and comparative or cognitive psychologists can learn important lessons from one another. On the one hand, cognitive psychologists who specialize in highly controlled experimental procedures can teach something about the importance of control to those cognitive ethologists who do not peform such research. On the other hand, those who study humans and other animals under highly controlled and often contrived and impoverished laboratory conditions can broaden their horizons and learn more about the importance of more naturalistic methods: they can be challenged to develop procedures that take into account possible interactions among stimuli within and between modalities in more naturalistic settings. For example, among those who are interested in important and "hot" questions about animal minds that are typically studied in controlled captive conditions (e.g. inquiries into the possibility of self-recognition) there is a growing awareness that more naturalistic approaches are needed. The use of single tests relying primarily on one modality, for example vision, for comparative studies represents too narrow an approach. Ultimately, all types of studies should be used to exploit the behavioral flexibility or versatility of the animals under study, a criterion for attributions of complex information processing or consciousness.
SOME CRITICISMS OF COGNITIVE ETHOLOGY
While most criticism comes from those who ignore the successes of cognitive ethology, those who dismiss it in principle because of strong and radical behavioristic leanings, or those who do not understand basic philosophical principles that inform cognitive ethology, it should be pointed out that more mechanistic approaches to the study of animal cognition are not without their own faults. For example, comparative psychologists often disregard how relevant a study is to the natural existence of the animals under study and pay too much attention to the logical structure of the experiments being performed without much regard for more naturalistic approaches. Noncognitive mechanistic "rules of thumb" also can be very cumbersome, nonparsimonious, and often appeal to hard-to-imagine past coincidences. Furthermore, it is not clear if the differences between noncognitive rules of thumb and cognitive explanations are differences in degree rather than differences in kind. Both noncognitive and cognitive explanations can be "just-so" stories (just like many evolutionary explanations) that rely on hypothetical constructs, and neither applies in all situations.
THREE CASE STUDIES
Ristau studied injury-feigning in piping plovers (the broken-wing display) and wanted to know if she could learn more about deceptive injury-feigning if she viewed the broken-wing display as an intentional or purposeful behavior ("the plover wants to lead the intruder away from her nest or young") rather than a hard-wired reflexive response to the presence of a particular stimulus, a potentially intruding predator. She studied the direction in which birds moved during the broken-wing display, how they monitored the location of the predator, and the flexibility of the response. Ristau found that birds usually performed the display in the direction that would lead an intruder who was following them further away from the threatened nest or young, and also that birds monitored the intruder's approach and modified their behavior in responses to variations in the intruder's movements. These and other data lead Ristau to conclude that the plover's broken-wing display lent itself to an intentional explanation -- that plovers purposely lead intruders away from their nests or young and modified their behavior in order to do so.
In another study of antipredator behavior in birds, Bekoff (1995a) found that western evening grosbeaks modified their vigilance or scanning behavior depending on the way in which individuals were positioned with respect to one another. Grosbeaks and other birds often trade-off scanning for potential predators and feeding -- essentially (and oversimplified), some birds scan while others feed and some birds feed when others scan. Thus, it is hypothesized that individuals want to know what others are doing and learn about others' behavior by trying to watch them. Bekoff's study of grosbeaks showed that when a flock contained four or more birds, there were large changes in scanning and other patterns of behavior that seemed to be related to ways in which grosbeaks attempted to gather information about other flock members. When birds were arranged in a circular array so that they could see one another easily compared to when they were arranged in a line that made visual monitoring of flock members more difficult, birds who had difficulty seeing one another were (i) more vigilant, (ii) changed their head and body positions more often, (iii) reacted to changes in group size more slowly, (iv) showed less coordination in head movements, and (v) showed more variability in all measures. The differences in behavior between birds organized in circular arrays when compared to birds organized in linear arrays were best explained by accounting for individuals' attempts to learn, via visual monitoring, about what other flock members were doing. This may say something about if and how birds attempt to represent their flock, or at least certain other individuals, to themselves. It may be that individuals form beliefs about what others are most likely doing and predicate their own behavior on these beliefs. Bekoff argued that cognitive explanations were simpler and less cumbersome than noncognitive rule-of-thumb explanations (e.g. "scan this way if there are this number of birds in this geometric array" or "scan that way if there are that number of birds in that geometric array." Noncognitive rule-of-thumb explanations did not seem to account for the flexibility in animals' behavior as well or as simply as explanations that appealed to cognitive capacities of the animals under study.
Social play behavior is another area that lends itself nicely to cognitive inquiries. The study of social play involves issues of communication, intention, role playing, and cooperation, and the results of this type of research may yield clues about the ability of animals to understand each others' intentions. Play also is a phenomenon that occurs in a wide range of species and affords the opportunity for a comparative investigation of cognitive abilities, extending the all-too-common narrow focus on primates that dominates discussions of nonhuman cognition. A recent study of the structure of play sequences in canids (Bekoff 1995b) showed that an action called the "bow" (an animals crouches on its forepaws, elevates its hindend, and may wag its tail) often is used immediately before and immediately after an action that can be misinterpreted and disrupt ongoing social play.
The social play of canids (and of other mammals) contains actions, primarily bites, that are used in other contexts (e.g. agonistic or predatory encounters) that do not contain bows. It is important for individuals to tell others that they want to play with them and not fight with them or eat them, and this message seems to be sent by play-soliciting signals, such as the bow, that occur almost only in the context of social play. In canids and other mammals, actions such as biting accompanied by rapid side-to-side shaking of the head are used in aggressive interactions and also during predation and could be misinterpreted when used in play. Bekoff hypothesized that if bites accompanied by rapid side-to-side shaking of the head or other behavior patterns could be misread by the recipient and could result in a fight, for example, then the animal who performed the actions that could be misinterpreted might have to communicate to its partner that this action was performed in the context of play and was not meant to be taken as an aggressive or predatory move. On this view, bows would not occur randomly in play sequences; the play atmosphere would be reinforced and maintained by performing bows immediately before or after actions that could be misinterpreted. The results of Bekoff's study of different canids supported the inference that "bows" served to provide information about other actions that followed or preceded it. In addition to sending the message "I want to play" when bows were performed at the beginning of play, bows performed during social play seemed to carry the message "I want to play despite what I am going to do or just did -- I still want to play" when there might be a problem in the sharing of this information between the interacting animals. The noncognitive rules-of-thumb, "play this way if this happens" and "play that way if that happens" seemed to be too rigid an explanation for the flexible behavior that the animals showed.
WHERE TO FROM HERE?
Those interested in animal cognition should resist temptations to be speciesistic cognitivists who make sweeping claims about the cognitive abilities (or lack thereof) for all members of a given species. A concentration on individuals and not on species should form an important part of the agenda for future research in cognitive ethology. There is a lot of individual variation in behavior within species and sweeping generalizations about what an individual ought to do because she is classified as a member of a given species must be taken with great caution. Furthermore, people often fail to recognize that in many instances sweeping generalizations about the cognitive skills (or lack thereof) of species and not of individuals are based on small data sets from a limited number of individuals representing few taxa, individuals who may have been exposed to a narrow array of behavioral challenges. The importance of studying animals under field conditions cannot be emphasized too strongly. Field research, that includes careful and well-thought out observation, description, and experimentation that does not result in mistreatment of the animals is extremely difficult to duplicate in captivity. While it may be easier to study animals in captivity, they must provided with the complexity of social and other stimuli to which they are exposed in the field; in some cases this might not be possible.
Cognitive ethologists should also strive to make the study of animal cognition tractable by carefully operationalizing the processes under study. Cognitive ethology can raise new questions that may be approached from various levels of analysis. For example, detailed descriptive information about subtle behavior patterns and neuroethological data may be important for informing further studies in animal cognition, and may be useful for explaining data that are already available. Such analyses will not make cognitive ethological investigations superfluous, because behavioral evidence is primary over anatomical or physiological data in assessments of cognitive abilities.
To summarize, those positions that should figure largely in cognitive ethological studies include: (i) remaining open to the possibility of surprises in animal cognitive abilities; (ii) concentrating on comparative, evolutionary, and ecological questions and sampling many different species including domesticated animals -- going beyond primates and avoiding talk of "lower" and "higher" animals, or at least laying out explicit criteria for using these slippery and value-laden terms; (iii) naturalizing methods of study by taking the animals' points of view (talking to them in their own languages) and studying them in conditions that are as close to the conditions in which they typically live; often animals do not do what we expect them do (sometimes prey will approach predators) and knowledge of their natural behavior is important in the development of testable and realistic models of behavior; (iv) trying to understand how cognitive skills used by captive animals may function in more natural settings; (v) studying individual differences; (vi) using all sorts of data, ranging from anecdotes to large data sets; and (vii) appealing to different types of explanations as best explanations of the data under scrutiny. Cognitive ethology need not model itself on other fields of science such as physics or neurobiology in order to gain credibility. Hard-science envy is what led to the loss of animal and human minds in the early part of the twentieth century.
We are a long way from having an adequate data base from which stipulative claims about the taxonomic distribution of various cognitive skills, or about the having of a theory of mind, can be put forth. Consider studies that show that some monkeys cannot perform imitation tasks that some mice can. If the point is to answer the question are monkeys smarter than mice or not it is misleading, for there is no reason to expect a single linear scale of intelligence. In the world of mice it may be more important to be able to do some things than it is in the world of monkeys, but in other respect a monkey may have a capacity that a mouse would lack. There also is much variation within species, and this also must be documented more fully.
It is unlikely that science will make complete contact with the nature of animal minds at any single point. Both "soft" (anecdotal) information and "hard" (empirical) data from long-term field research are needed to inform and to motivate further empirical experimental research. So, questions such as "do mice ape?" or "do apes mice"? are premature. Does this mean that many, some, or no animals have or do not have a mind or a theory of mind? It also would be premature to attempt to answer definitively these questions at this time given our current state of knowledge.
I thank Colin Allen, Carron Meaney, Ann Wolfe, Lawrence Shapiro, Eric Saidel, some students in my critical thinking class in animal cognition, and the editors for helpful comments.
Allen, C., and Bekoff, M.: Species of Mind: The Philosophy and Biology of Cognitive Ethology (Cambridge, Massachusetts: MIT Press,1997).
Bekoff, M.: Vigilance, flock size, and flock geometry: Information gathering by western evening grosbeaks (Aves, fringillidae). Ethology 99 (1995a), 150- 161.
Bekoff, M.: Play signals as punctuation: The structure of social play in canids. Behaviour 132 (1995b), 419-429.
Bekoff, M., and Allen, C.: 'Cognitive ethology: Slayers, skeptics, and proponents', Anthropomorphism, Anecdote, and Animals: The Emperor's New Clothes? ed. R. W. Mitchell, N. Thompson, and L. Miles (Albany, New York: SUNY Press 1996), (in press).
Bekoff, M., and Jamieson, D., ed.: Readings in Animal Cognition. (Cambridge, Massachusetts: MIT Press, 1996).
Cheney, D. L., and Seyfarth, R. M.: How Monkeys See the World: Inside the Mind of Another Species (Chicago: University of Chicago Press, 1990).
Griffin, D. R:. Animal Minds (Chicago: University of Chicago Press, 1992).
Jamieson, D., and Bekoff, M.: On aims and methods of cognitive ethology. Philosophy of Science Association, 2 (1992), 110-124.
Ristau, C. ed.: Cognitive ethology: The Minds of Other Animals. Essays
in Honor of Donald R. Griffin (Hillsdale, New Jersey: Lawrence Erlbaum,
Bekoff, M., and Jamieson, D., ed.: Readings in Animal Cognition (Cambridge, Massachusetts: MIT Press, 1996).
Griffin, D. R:. Animal Minds (Chicago: University of Chicago Press, 1992).
Ristau, C. ed.: Cognitive Ethology: The Minds of Other Animals. Essays
in Honor of Donald R. Griffin (Hillsdale, New Jersey: Lawrence Erlbaum,
FOR ANNOTATED NAME INDEX
The Question of Animal Awareness: Evolutionary Continuity of Mental Experience (New York: The Rockefeller University Press, 1976/1981).
Prospects for a cognitive ethology. Behavioral and Brain Sciences, 4 (1978), 527- 538.
Animal Thinking (Cambridge, Massachusetts: Harvard University. Press. 1984).
Animal Minds (Chicago: University of Chicago Press, 1992).
While Griffin's work has been favorably reviewed in numerous places, it often is dismissed as being too anecdotal and philosophically naive. Regardless, few contest that it was his 1976/1981 book that rekindled interest in the rigorous, comparative, and evolutionary study of nonhuman animal minds.