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Cognitive and communicative abilities of Grey parrots
Applied Animal Behaviour Science 100 (2006) 77–86 www.elsevier.com/locate/applanim
Cognitive and communicative abilities of Grey parrots§ Irene M. Pepperberg * Department of Psychology, Brandeis University, Waltham, MA 02454, USA Available online 19 May 2006
Abstract This paper presents results of almost 30 years of study of the cognitive and communicative activities of Grey parrots (Psittacus erithacus), conventionally regarded as mindless mimics. These studies have demonstrated that Grey parrots can solve various cognitive tasks and acquire and use English speech in ways that often resemble those of very young children. Examples include the concepts of same/different, colour, size and shape. The parrot Alex can also recognize and distinguish numbers up to six, and spontaneously demonstrated his ability to grasp the concept of ‘‘none’’. Given the evolutionary distance between birds and mammals, these results have intriguing implications for the evolution of intelligence, the study of comparative intelligence, and the care and maintenance of birds held in captivity in zoos and as companion animals. # 2006 Elsevier B.V. All rights reserved. Keywords: Parrot; Avian intelligence; Avian communication; Avian animal companion; Captive birds
1. Introduction This paper presents a brief summary of almost 30 years of study of the cognitive and communicative activities of Grey parrots. Much of this work has involved direct contact amongst myself, my students and individual birds, most notably my oldest subject Alex, and describes the cognitive development of each individual. For this reason this paper departs from conventional practice in scientific writing and makes regular use of personal nouns and pronouns (e.g. Alex and I) for the good reason that this format makes the paper easier to read. It has become clear from this work that Alex exhibits cognitive capacities comparable to those of marine mammals, §
This paper is part of the special issue entitled Sentience in Animals, Guest Edited by Dr. John Webster. * Tel.: +1 781 736 2195; fax: +1 781 736 3291. E-mail address: [email protected].
0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2006.04.005
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apes and sometimes 4–6-year-old children (Pepperberg, 1999). Using English vocalizations, Alex labels 50 different objects, 7 colors, 5 shapes and quantities up to and including six. He combines these labels to identify, request, refuse, categorize and quantify about 100 different objects. He has functional use of phrases such as ‘‘Come here’’, ‘‘I want X’’ and ‘‘Wanna go Y’’ where X and Y are, respectively, appropriate object or location labels. He has concepts of category, bigger/smaller, same/different, absence and quantity; some of these will be discussed in detail below. Of particular interest is that his abilities are inferred not from operant tasks common in animal research, but from vocal responses to vocal questions; that is, he demonstrates intriguing communicative parallels with young humans, despite his phylogenetic distance. Younger birds have begun to replicate Alex’s results. It is unlikely that I taught Alex and other parrots these abilities de novo, which suggests that their achievements derive from existent cognitive and neurological architectures. Although this work has interest on its own merit for researchers in psychology, biology, neurobiology, anthropology, linguistics and other scientific disciplines, the data also have implications for the treatment of psittacines in captive situations such as zoos or as human companion animals. 2. Methods 2.1. Animals and housing The subjects of my studies have been several male Grey parrots (Psittacus erithacus). (Note: Their sex has been a matter of chance, as Greys are sexually monomorphic and were not tested until after their acquisition.) The oldest, Alex, was acquired in 1977 when he was approximately 1 year old; he is still a research subject. Alo was acquired at 7 months, in 1991, and was in the laboratory until early 1995. Kyaaro, acquired at about 3 months, also in 1991, remained in the laboratory until 2001. Griffin, obtained at 7 weeks in 1995, is still part of the research, as is Arthur, who was acquired in 1999 when he was approximately a year old. Birds’ living conditions outside of testing and training have been described in detail previously (e.g., Pepperberg et al., 1998), except that now birds always share a room (Pepperberg and Wilkes, 2004). In brief, birds are trained, tested and sleep in the laboratory; sleeping cages are Avian Adventures (28 in. 22 in. 26 in.). Birds have access to their cages except during training and testing, but spend most of their days either on T-stands or atop their cages. Training and testing occurs on T-stands. Water and Harrison’s Bird Diet are available ad lib; fruit, vegetables, nuts, etc. are provided outside of testing and training periods. 2.2. Training The primary training procedure is the Model/Rival (M/R) technique, originally developed by Todt (1975) and adapted for use in my laboratory. Only in specific studies described below have other techniques been employed. The M/R training system (background in Pepperberg, 1999) uses three-way social interactions among two humans and a parrot to demonstrate targeted vocal behavior. The parrot observes two humans handling one or more objects, then watches humans interact: the trainer presents, and queries the human model about, the item(s) (e.g., ‘‘What’s here?’’, ‘‘What color?’’) and gives praise and the object(s) to reward correct answers referentially. Incorrect responses (like those the bird may make) are punished by scolding and temporarily removing item(s) from sight. Thus the second human is a model for the parrot’s responses, its rival for the trainer’s attention, and also illustrates error consequences: the model must try again or talk more clearly if the response was (deliberately) incorrect or garbled, thereby demonstrating corrective feedback. The bird is also queried and rewarded for successive approximations to correct responses; thus training is adjusted to its level. Unlike other laboratories’ M/R procedures (see Pepperberg, 1999), ours interchanges roles of trainer and model, and includes the parrot in interactions to emphasize that one being is not always the questioner and the
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other the respondent, and that the procedure can effect environmental change. Role reversal also counteracts an earlier methodological problem: birds whose trainers always maintained their respective roles responded only to the questioner. Our birds, however, respond to, interact with, and learn from all humans. M/R training exclusively uses intrinsic reinforcers: to ensure closest possible correlations of labels or concepts to be learned with their appropriate referent, reward for uttering ‘‘X’’ is X: the object to which the label or concept refers. Earlier unsuccessful programs for teaching birds to communicate with humans used extrinsic rewards (Pepperberg, 1999): one food that neither related to, nor varied with, the label or concept being taught, thereby delaying label and concept acquisition by confounding the label of the targeted exemplar or concept with that of the food. My birds never receive extrinsic rewards. Moreover, initial use of the label to request the item also demonstrates functionality. Because Alex sometimes fails to focus on targeted objects, I trained him to use the phrase ‘‘I want X’’ to separate labeling from requesting (see Pepperberg, 1999). Thus having identified Y (something he may not desire) by identifying its material, color, shape, etc. (depending upon the question he was posed) his reward is then the right to request something more desirable, which provides flexibility but maintains referentiality. To receive X after identifying Y, Alex must state ‘‘I want X’’ and trainers will not comply until the appropriate task is completed. Thus his labels are true identifiers, not merely emotional requests. Adding ‘‘want’’ provides additional advantages: first, trainers can distinguish incorrect labeling from appeals for other items, particularly during testing, when birds unable to use ‘‘want’’ might not be erring but asking for treats, and scores might decline unrelated to competence. Second, birds may demonstrate low-level intentionality: Alex rarely accepts substitutes when requesting X, and continues his demands (Pepperberg, 1999). 2.3. Testing Birds are tested under rigorous conditions so as to avoid various possible types of cuing. Full details of test procedures can be found in Pepperberg (1999).
3. Results of M/R training As noted above, Alex has acquired several complex cognitive concepts. He not only produces various English labels, but also understands their use and the numerous questions we pose. He is not responding by rote to objects in his environment. So, for example, I can show him a particular object and ask him ‘‘What color?’’ (green), ‘‘What shape?’’ (four-corner), ‘‘What matter?’’ (wood) and ‘‘What toy?’’ (block). He could not respond appropriately unless he comprehended the labels for, and the concepts of, color, shape, matter and toy. Some of his accomplishments involve more abstract concepts of same/different, absence and number. Some of the relevant studies are described here. For discussions of topics such as bigger/smaller, recursion and conjunction, see Pepperberg (1999). 3.1. Same/different and absence According to Premack (1983), same/different requires use of arbitrary symbols to represent relationships of sameness and difference between sets of objects and the ability to denote the attribute that is same or different, that is, requires symbolic representation. Comprehension of related tasks, such as match-to-sample, non-match-to-sample, oddity-from-sample, or homogeneity and non-homogeneity, in contrast, require only that subjects show a savings in the number of trials needed to respond to B and B as a match (or as a homogeneous field) after learning to respond to A and A as a match (and likewise by showing a savings in trials involving C and D after learning to respond appropriately to A and B as non-matching or non-homogenous;
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Pepperberg, 1999). Subjects performing match-to-sample and non-match-to-sample might even be responding based on ‘old’ versus ‘new’, ‘familiar’ versus ‘unfamiliar’ (Premack, 1983), that is, on the relative number of times they experience the A sample versus the different B samples. Subjects that understand same/different, however, not only know that two non-identical red objects are related the same way as are two non-identical blue objects – in terms of color – but also know that the red objects are related to each other a different way than are two non-identical square objects, and, moreover, can transfer this understanding to any attribute of an item (Premack, 1983). A subject would likewise have to understand the concept of difference (Pepperberg, 1999). Using M/R training, my students and I taught Alex not only to produce the appropriate category label for the attribute that is same or different for any combination, but also to respond ‘‘none’’ if nothing is same or different (that is, to the absence of information about these concepts; Pepperberg, 1988), even for objects not used in training or that he cannot label. Furthermore, his responses were still above chance when I tested if he were truly attending to the questions—for example, when the question ‘‘What’s same?’’ was posed with respect to a green wooden triangle and a blue wooden triangle. If he were ignoring the question and responding based on his prior training and object attributes, he would have determined, and responded with the label for, the one anomalous attribute (in this case, ‘‘color’’). Instead, he responded with one of the two appropriate answers [i.e., ‘‘shape’’ or ‘‘mah-mah’’ (matter); Pepperberg, 1987a]. Alex’s use of ‘‘none’’ (Pepperberg, 1988, 1999) is interesting because learning to understand and comment upon non-existence, or even the slightly more basic notion of absence, although seemingly simple, denotes a relatively advanced stage in cognitive and linguistic development (Brown, 1973). An organism reacts to absence only when the expected presence of events, objects or other information in its environment is violated, that is, only when a discrepancy exists between the expected and actual state of affairs (see Pepperberg, 1999). Of course, Alex was responding to the absence of an attribute, not to the absence of an object, which is an important distinction. 3.2. Numerical concepts Given that Alex could understand categories involving attributes inherent to an object (e.g., color, shape) and abstract concepts of same/different and absence, could he form an entirely new categorical class for quantity? Could he be trained to reclassify a group of wooden objects known until now simply as ‘‘wood’’ or ‘‘green wood’’ so that he could identify them as ‘‘five wood’’? To succeed, he would have to understand that a new set of labels, ‘‘one’’, ‘‘two’’, ‘‘three’’, ‘‘four’’, ‘‘five’’ and ‘‘six’’ represented a means to categorize objects based on a combination of physical similarity within a group and the group’s quantity, rather than by physical characteristics alone. He would also have to generalize this new class of numerical labels to sets of novel objects, to objects in random arrays, and to heterogeneous collections. Note that Koehler (1950, 1953) and his colleagues (Braun, 1952; Lo¨gler, 1959) had already demonstrated Grey parrots’ sensitivity to quantity and basic concepts of numerosity and numerousness; that is, that Grey parrots could learn a form of match-to-sample involving sets of novel objects and random dot patterns representing quantity, and that the birds could transfer from simultaneous visual presentations to sequential visual and auditory presentations. But could Alex go beyond these tasks and use number as a categorical label? Could he use numbers symbolically? The several numerical concept studies performed with Alex do not demonstrate that his understanding of number matches that of adult humans (Fuson, 1988), but suggest that his concept of quantity is similar to that of a young child at the beginning stages of true counting.
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He can, for example, recognize and label different quantities of physical objects up to and including six (Pepperberg, 1987b). Objects need not be familiar, nor be placed in any particular pattern, such as a square or triangle. If presented with a heterogeneous collection – of X’s and Y’s – he can respond appropriately to questions of either ‘‘How many X?’’ or ‘‘How many Y?’’ (Pepperberg, 1987b). Work with other types of heterogeneous collections demonstrates even more advanced skills. Alex can be shown a ‘‘confounded number set’’ (collections of four groups of items that vary in two colors and two object categories—e.g., blue and red wood and blue and red wool) and be asked to label the number of items uniquely defined by the combination of one color and one object category (e.g., ‘‘How many blue wood?’’). His accuracy (Pepperberg, 1994) replicates that of humans in a comparable study (Trick and Pylyshyn, 1989). His level is therefore beyond what might be considered subitizing (a perceptual mechanism for recognizing small quantities without actually counting; think of how you label the number of dots on dominoes or dice; Pepperberg, 1999). The mechanisms that Alex uses are difficult to determine (Pepperberg, 1994, 2006). Overall, the data suggest that a non-human, non-primate, non-mammalian animal has a level of competence that, in a chimpanzee, would be taken to indicate a human level of cognitive processing (Pepperberg, 1999). These experiments, however, did not exclude the possibility that Alex might produce but not comprehend his number labels, as did apes and children in some studies (e.g., Savage-Rumbaugh et al., 1980, 1993; Fuson, 1988; Wynn, 1990). Such comprehension is crucial for true numerical competence (Fuson, 1988; Pepperberg, 1999). A student and I therefore performed a comprehension study (Pepperberg and Gordon, 2005), in which Alex was, without prior training on the task, asked ‘‘What color/object is [number]?’’ for collections of various simultaneously presented quantities (e.g., subsets of four, five and six blocks of three different colors; monochrome subsets of two keys, four corks and six sticks). His accuracy was above 80%, and was unaffected by array quantity, mass or contour; sometimes we used larger objects for the smaller quantities. Alex thus demonstrated numerical comprehension competence comparable to that of chimpanzees and very young children. Of particular interest was that at one point in the experiment, Alex, on his own initiative, transferred his ability to use ‘‘none’’ to comment on the absence of an attribute (same/different, bigger/smaller) to the absence of a specific quantity—albeit in a limited sense (Pepperberg and Gordon, 2005). A description of this behaviour follows. On the 10th trial within the first set of 12, Alex was asked ‘‘What color three?’’ to a set of two, three, and six objects. He replied ‘‘five’’, a response that was puzzling. Sometimes when he did not want to perform a given task, he would give all the possible wrong answers (Pepperberg, 1999) or even toss all the exemplars off of the tray, but rarely would he give an irrelevant response. I thus asked him twice more and each time he replied ‘‘five’’. Not attending to the tray, and thinking that maybe he wished to be queried about a different number, I finally said ‘‘OK, Alex, tell me, what color five?’’ He immediately responded ‘‘none’’ (Pepperberg and Gordon, 2005). Remember, there was no set of five objects. As noted above, Alex had been taught to respond ‘‘none’’ if no category (color, shape or material) was same or different when he was queried about the similarity or difference of two objects (Pepperberg, 1988); he had also spontaneously transferred this response to the query ‘‘What color bigger?’’ concerning two identically size objects in a study of relative size (Pepperberg and Brezinsky, 1991), but had never been taught the concept of absence of quantity nor to respond to absence of an exemplar. We thus repeated the question randomly throughout other trials with respect to each possible number to ensure that this situation was not an odd happenstance. On these six ‘‘none’’ trials, Alex made only one error, which, interestingly, was to label a color not on the tray. Remember, I had not trained the conventional term, ‘‘zero’’, to indicate the absence of quantity; Alex’s use of ‘‘none’’ for this purpose was unexpected.
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Overall, his understanding of ‘‘none’’ as a zero-like concept appears to resemble that of 3year-old children. Children actually seem to have to be about 4 years old before they achieve full adult-like understanding of the labels for zero and other numerals (Bialystok and Codd, 2000; Wellman and Miller, 1986). Whether Alex can fully understand the equivalence of ‘‘none’’ to the concept of zero is still to be determined (Pepperberg, 2006). 3.3. Other issues involving training The data that my students and I had accumulated concerning Alex’s cognitive and communicative abilities showed the incredible success of M/R training, but did not explain why it was such a powerful procedure. To answer that question, I would have to determine what would happen if some elements of input were lacking. Answering that question also required additional parrots, because Alex might cease learning merely because training had changed, not because of the type of change. So, while many of the experiments described above were proceeding with Alex, I began working with four new naive Greys – Kyaaro, Alo, Griffin, and Arthur – to test the relative importance of reference, context/function and social interaction in training. 3.4. Eliminating aspects of input My students and I performed eight experiments (Pepperberg, 1999; Pepperberg et al., 2000; Pepperberg and Wilkes, 2004). First, we compared simultaneous exposure of Alo and Kyaaro to three input conditions: I, audiotapes of Alex’s sessions, which were non-referential, not contextually applicable and non-interactive; II, videotapes of Alex’s sessions, which were referential, minimally contextually applicable and non-interactive; and III, standard M/R training. In I and II, birds experienced tapes in social isolation. Condition I paralleled early allospecific song acquisition studies (e.g., Marler, 1970); II involved then-unresolved issues about avian vision and video (e.g., Ikebuchi and Okanoya, 1999). We counterbalanced labels across birds, matching training time across sessions. Second, because interactive co-viewers could increase young children’s learning from video (Rice et al., 1990), a co-viewer now provided social approbation for viewing and pointed to the screen with comments like ‘‘Look what Alex has!’’, but did not repeat targeted labels, ask questions, or relate content to other training. Birds’ attempts at a label would garner only vocal praise. Social interaction was limited; referentiality and functionality matched earlier videotape sessions. Third, because extent of coviewer interaction might affect children’s learning from video, our co-viewer now uttered targeted labels and asked questions. Fourth, so that lack of reward would not deter video learning, a socially isolated parrot watched videos while a student in another room monitored its utterances through headphones and could deliver rewards remotely. Fifth, because birds might habituate to the single videotape used per label (even though each tape depicted many different responses and interactions among Alex and trainers), we used live video from Alex’s sessions. Sixth, because research showed that if adult–child duos failed to focus jointly on objects being labeled, the labels were not acquired (e.g., Baldwin, 1995), a single trainer faced away from the bird (who was within reach of, e.g., a key), talked about the object (‘‘Look, a shiny key!’’, ‘‘Do you want key?’’, etc.; sentence frames; Pepperberg, 1999), but had no visual or physical contact with parrot or object; a bird’s attempts at the targeted label would receive only vocal praise, thereby eliminating some functionality and considerable social interaction. Parrots failed to acquire referential use of targeted labels in any non-M/R condition, but succeeded in concurrent M/R sessions (Pepperberg, 1999). Seventh, we eliminated some interactive aspects of modeling by having a
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single student label objects, query Griffin, jointly attend to objects, and thus interact fully with Griffin and objects. Griffin did not utter labels in 50 such sessions, but clearly produced labels after two or three subsequent M/R sessions. We suspected latent learning: Griffin apparently stored labels, but did not use them until he observed their use modeled. (NB: Birds switched to M/R training after 50 video sessions needed 20 sessions before producing labels.) Finally, we performed video studies with a liquid crystal monitor with Arthur and Griffin to see if standard cathode ray tube flicker-fusion affected learning (Ikebuchi and Okanoya, 1999); birds attended more closely to this screen but did not acquire targeted vocalizations. Results thus emphasize the importance of reference, demonstrations of contextual use/functionality and social interaction in training if parrots are to communicate with humans rather than mimic speech. 3.5. Mutual exclusivity: studying subtle changes in input Our parrots’ learning processes may also parallel young children’s mutual exclusivity (ME) (Pepperberg and Wilcox, 2000). ME refers to children’s assumption during early word acquisition that each object has one, and only one, label (e.g., Liittschwager and Markman, 1994). Along with the whole object assumption (that a label refers to an entire object, not some feature), ME supposedly guides initial label acquisition. ME may also help children interpret novel words as feature labels (overcome the whole object assumption), but very young children may find second labels for items initially more difficult to acquire than the first because second labels are viewed as alternatives (Liittschwager and Markman, 1994). Input, however, affects ME: children (Gottfried and Tonks, 1996) and parrots like Alex, who receive inclusivity data (X is a kind of Y; e.g., color labels taught as additional, not alternative, labels, ‘‘Here’s a key; it’s a green key’’), generally accept multiple labels for items and form hierarchical relations. Thus, shown a wooden block, Alex answers ‘‘What color?’’, ‘‘What shape?’’, ‘‘What matter?’’ and ‘‘What toy?’’ (Pepperberg, 1999). Parrots given colors or shapes as alternative labels (e.g., ‘‘Here’s key’’ and later ‘‘It’s green’’), however, have difficulty learning to use these modifiers for previously labeled items. Griffin, thus trained, initially answered ‘‘What color?’’ with object labels. Similarly, while learning an object label – cup – he answered ‘‘What toy?’’ with colors and had difficulty acquiring ‘‘cup’’. Thus small input changes affect label acquisition as much for parrots as young children. 4. Unexpected similarities between primates and parrots Other unexpected similarities exist for birds and primates with respect to the development of communicative competence. These parallels involve behavior for which underlying mechanisms may suggest a commonality in brain structure and/or information processing. I discuss two studies: combinatory learning and phonological processing. 4.1. Combinatory learning Based primarily on behavioral data, researchers (e.g., Johnson-Pynn et al., 1999) argue that a common neural substrate initially underlies young children’s parallel development of communicative and object (manual) combinations, that a homologous substrate in great apes allows similar, limited, parallel development, and that such data imply a shared evolutionary history for communicative and physical behavior. But Griffin showed comparable limited, parallel combinatorial development of three-item and three-label combinations (Pepperberg and
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Shive, 2001). Percentages of physical and vocal combinations were roughly equal; despite months of training, vocal three-label combinations emerged only when he more frequently initiated three-objects combinations; vocal combinations were generally not those trained; and physical combinations were performed with his beak, not feet. Moreover, unlike Johnson-Pynn et al.’s Cebus (1999), Griffin was not trained on physical tasks and we limited training on threelabel combinations (2,5-corner wood/paper) to see if spontaneous manipulative behavior developed in parallel with vocal complexity. Although Griffin’s behavior – and that of our most advanced subject, Alex (Pepperberg, 1999) – is equivalent neither to human language nor to 2–3-year-old humans’ combinatory behavior, I suggest that our Grey parrots’ behavior patterns match some of non-human primates, that parallel combinatory development is not limited to primates, and that a particular mammalian brain structure is not uniquely responsible for such behavior. Specifically, searches for and arguments concerning responsible substrates and common behavior should not be restricted to primates (Medina and Reiner, 2000). 4.2. Phonological awareness? In a recent study (Pepperberg, 2005) Alex showed what appears to be vocal segmentation and phonological awareness; that is, that he understands that labels consist of individual units that can be recombined in novel ways to create novel vocalizations. The data also suggest that Alex’s ability is a learned behavior, is not uniquely human, and is dependent upon having considerable experience with English speech and sound–letter training. A younger bird, lacking such training, did not engage in such behavior. Note, too, that this behavior demonstrates the process by which Alex acquired the targeted label. In this study, both Arthur and Alex were trained on the label ‘‘spool’’; both parrots knew the similar-sounding ‘‘wool’’, but only Alex had had extensive training on /s/ from an experiment on phonemes. Note that /p/ is particularly difficult for parrots, lacking lips, to acquire, and that they seemingly use esophageal speech in its production (Patterson and Pepperberg, 1998); /sp/ is even more difficult. Arthur produced ‘‘spool’’, but the /p/, when sonagraphed, was actually a whistle. Alex, in contrast, produced ‘‘s[pause]wool’’ for a full year, then switched to a ‘‘spool’’ almost identical to mine when sonagraphed. Exactly because of the difficulty of producing /p/, Alex may have used ‘‘s[pause]wool’’ such that two known utterances provided the overall structure and the pause was a place filler, like that occasionally used by young children, until he could learn how to insert the /p/ and adapt the vowel. Specifically, Peters (2001) suggests that children use fillers to preserve syllable numbers or the prosodic rhythm of targeted vocalizations until the standard form is learned. Alex’s behavior suggests that he, too, was aware of the need for something additional and different to complete the vocalization. Simply omitting or closing the gap – and responding on the basis of sound similarity – would have produced /swUl/ (‘‘swull’’), not /swul/ (‘‘swooool’’). 5. Overall conclusions A key message of this paper, presented within the context of a symposium on Animal Sentience, is to encourage an awareness of, and a sensitivity to, the abilities of non-humans, particularly non-primate and non-mammalian subjects. For far too long, animals in general, and birds in particular, have been denigrated and treated merely as creatures of instinct rather than sentient, intelligent beings. The data presented here and elsewhere (see Pepperberg, 1999)
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demonstrate that many species of animal posses cognitive capacities that we have until now considered unique to humans and other primates. All we need to examine these capacities are some enlightened research tools. My immediate hope is that the material presented here will help us respect the cognitive abilities of creatures who may at first seem so very different from humans but, in reality, share many of our abilities. My long-term hope is that the material will be used to improve and enrich the lives of captive and companion animals, to prevent habitat destruction and unnecessary capture of wild animals, and to strengthen our bonds with non-humans. References Baldwin, D.A., 1995. Understanding the link between joint attention and language. In: Moore, C., Dunham, P.J. (Eds.), Joint Attention: Its Origin and Role in Development. Erlbaum, Hillsdale, NJ, pp. 131–158. Bialystok, E., Codd, J., 2000. Representing quantity beyond whole numbers: some, none and part. Can. J. Expt’l Psychol. 54, 117–128. Braun, H., 1952. Uber das Unterscheidungsvermo¨gen unbenannter Anzahlen bei Papageien. Z. Tierpsychol. 9, 40–91 (Concerning the ability of parrots to distinguish unnamed numbers.). Brown, R., 1973. A First Language. Harvard University Press, Cambridge, MA. Fuson, K.C., 1988. Children’s Counting and Concepts of Number. Springer-Verlag, New York. Gottfried, G.M., Tonks, J.M., 1996. Specifying the relation between novel and known: input affects the acquisition of novel color terms. Child Dev. 67, 850–866. Ikebuchi, M., Okanoya, K., 1999. Male zebra finches and Bengalese finches emit directed songs to the video images of conspecific females projected onto a TFT display. Zool. Sci. 16, 63–70. Johnson-Pynn, J., Fragaszy, D.M., Hirsh, E.M., Brakke, K.E., Greenfield, P.M., 1999. Strategies used to combine seriated cups by chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and capuchins (Cebus apella). J. Comp. Psychol. 113, 137–148. Koehler, O., 1950. The ability of birds to ‘count’. Bull. Anim. Behav. Soc. 9, 41–45. Koehler, O., 1953. Thinking without words. In: Proceedings of the XIVth International Congress of Zoology. pp. 75– 88. Liittschwager, J.C., Markman, E.M., 1994. Sixteen- and 24-month olds’ use of mutual exclusivity as a default assumption in second-label learning. Dev. Psychol. 30, 955–968. Lo¨gler, P., 1959. Versuche zur Frage des ‘‘Za¨hl’’-Vermo¨gens an einem Graupapagei und Vergleichsversuche an Menschen. Z. Tierpsychol. 16, 179–217 (Studies on the question of ‘‘number’’ sense in a Grey parrot and comparative studies on humans.). Marler, P., 1970. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 71, 1–25. Medina, L., Reiner, A., 2000. Do bird possess homologues of mammalian primary visual, somatosensory and motor cortices? TINS 23, 1–12. Patterson, D.K., Pepperberg, I.M., 1998. A comparative study of human and Grey parrot phonation: acoustic and articulatory correlates of stop consonants. JASA 103, 2197–2213. Pepperberg, I.M., 1987a. Acquisition of the same/different concept by an African Grey Parrot (Psittacus erithacus): learning with respect to color, shape, and material. Anim. Learn. Behav. 15, 423–432. Pepperberg, I.M., 1987b. Evidence for conceptual quantitative abilities in the African Grey Parrot: labeling of cardinal sets. Ethology 75, 37–61. Pepperberg, I.M., 1988. Acquisition of the concept of absence by an African Grey parrot: learning with respect to questions of same/different. JEAB 50, 553–564. Pepperberg, I.M., 1994. Evidence for numerical competence in an African Grey parrot (Psittacus erithacus). J. Comp. Psychol. 108, 36–44. Pepperberg, I.M., 1999. The Alex Studies. Harvard University Press, Cambridge, MA. Pepperberg, I.M., 2005. Grey parrots do not always ‘‘parrot’’: roles of imitation and phonological awareness in the creation of new labels from existing vocalizations. In: AISB Proceedings, Hatfield, UK. Pepperberg, I.M., 2006. Grey Parrot (Psittacus erithacus) numerical abilities: addition and further experiments on a zerolike concept. J. Comp. Psychol. 120, 1–11. Pepperberg, I.M., Brezinsky, M.V., 1991. Acquisition of a relative class concept by an African Grey parrot (Psittacus erithacus): discriminations based on relative size. J. Comp. Psychol. 105, 286–294.
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Pepperberg, I.M., Gordon, J.D., 2005. Number comprehension by a Grey parrot (Psittacus erithacus), including a zerolike concept. J. Comp. Psychol. 119, 197–209. Pepperberg, I.M., Shive, H.A., 2001. Simultaneous development of vocal and physical object combinations by a Grey Parrot (Psittacus erithacus): bottle caps, lids, and labels. J. Comp. Psychol. 115, 376–384. Pepperberg, I.M., Wilcox, S.E., 2000. Evidence for a form of mutual exclusivity during label acquisition by Grey parrots (Psittacus erithacus)? J. Comp. Psychol. 114, 219–231. Pepperberg, I.M., Wilkes, S.R., 2004. Lack of referential vocal learning from LCD video by Grey Parrots (Psittacus erithacus). Interact. Stud. 5, 75–97. Pepperberg, I.M., Naughton, J.R., Banta, P.A., 1998. Allospecific vocal learning by Grey parrots (Psittacus erithacus): a failure of videotaped instruction under certain conditions. Behav. Proc. 42, 139–158. Pepperberg, I.M., Sandefer, R.M., Noel, D., Ellsworth, C.P., 2000. Vocal learning in the Grey parrot (Psittacus erithacus): effect of species identity and number of trainers. J. Comp. Psychol. 114, 371–380. Peters, A.M., 2001. Filler syllables: what is their status in emerging grammar? J. Child Lang. 28, 229–242. Premack, D., 1983. The codes of man and beasts. Behav. Brain Sci. 6, 125–167. Rice, M.L., Huston, A.C., Truglio, R., Wright, J., 1990. Words from ‘‘Sesame Street’’: learning vocabulary while viewing. Dev. Psychol. 26, 421–428. Savage-Rumbaugh, E.S., Rumbaugh, D.M., Boysen, S., 1980. Do apes use language? Am. Sci. 68, 49–61. Savage-Rumbaugh, E.S., Murphy, J., Sevcik, R.A., Brakke, K.E., Williams, S.L., Rumbaugh, D.M., 1993. Language comprehension in ape and child. Mono. SRCD 233, 1–258. Trick, L., Pylyshyn, Z., 1989. Subitizing and the FNST Spatial Index Model. University of Ontario, COGMEM #44 (Based on paper presented at 30th Psychonomic Society Meeting, Atlanta, GA.). Todt, D., 1975. Social learning of vocal patterns and modes of their applications in Grey Parrots. Z. Tierpsychol. 39, 178– 188. Wellman, H.M., Miller, K.F., 1986. Thinking about nothing: development of concepts of zero. Br. J. Dev. Psychol. 4, 31– 42. Wynn, K., 1990. Children’s understanding of counting. Cognition 36, 155–193.
Cognitive and communicative abilities of Grey parrots§ Irene M. Pepperberg * Department of Psychology, Brandeis University, Waltham, MA 02454, USA Available online 19 May 2006
Abstract This paper presents results of almost 30 years of study of the cognitive and communicative activities of Grey parrots (Psittacus erithacus), conventionally regarded as mindless mimics. These studies have demonstrated that Grey parrots can solve various cognitive tasks and acquire and use English speech in ways that often resemble those of very young children. Examples include the concepts of same/different, colour, size and shape. The parrot Alex can also recognize and distinguish numbers up to six, and spontaneously demonstrated his ability to grasp the concept of ‘‘none’’. Given the evolutionary distance between birds and mammals, these results have intriguing implications for the evolution of intelligence, the study of comparative intelligence, and the care and maintenance of birds held in captivity in zoos and as companion animals. # 2006 Elsevier B.V. All rights reserved. Keywords: Parrot; Avian intelligence; Avian communication; Avian animal companion; Captive birds
1. Introduction This paper presents a brief summary of almost 30 years of study of the cognitive and communicative activities of Grey parrots. Much of this work has involved direct contact amongst myself, my students and individual birds, most notably my oldest subject Alex, and describes the cognitive development of each individual. For this reason this paper departs from conventional practice in scientific writing and makes regular use of personal nouns and pronouns (e.g. Alex and I) for the good reason that this format makes the paper easier to read. It has become clear from this work that Alex exhibits cognitive capacities comparable to those of marine mammals, §
This paper is part of the special issue entitled Sentience in Animals, Guest Edited by Dr. John Webster. * Tel.: +1 781 736 2195; fax: +1 781 736 3291. E-mail address: [email protected].
0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2006.04.005
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apes and sometimes 4–6-year-old children (Pepperberg, 1999). Using English vocalizations, Alex labels 50 different objects, 7 colors, 5 shapes and quantities up to and including six. He combines these labels to identify, request, refuse, categorize and quantify about 100 different objects. He has functional use of phrases such as ‘‘Come here’’, ‘‘I want X’’ and ‘‘Wanna go Y’’ where X and Y are, respectively, appropriate object or location labels. He has concepts of category, bigger/smaller, same/different, absence and quantity; some of these will be discussed in detail below. Of particular interest is that his abilities are inferred not from operant tasks common in animal research, but from vocal responses to vocal questions; that is, he demonstrates intriguing communicative parallels with young humans, despite his phylogenetic distance. Younger birds have begun to replicate Alex’s results. It is unlikely that I taught Alex and other parrots these abilities de novo, which suggests that their achievements derive from existent cognitive and neurological architectures. Although this work has interest on its own merit for researchers in psychology, biology, neurobiology, anthropology, linguistics and other scientific disciplines, the data also have implications for the treatment of psittacines in captive situations such as zoos or as human companion animals. 2. Methods 2.1. Animals and housing The subjects of my studies have been several male Grey parrots (Psittacus erithacus). (Note: Their sex has been a matter of chance, as Greys are sexually monomorphic and were not tested until after their acquisition.) The oldest, Alex, was acquired in 1977 when he was approximately 1 year old; he is still a research subject. Alo was acquired at 7 months, in 1991, and was in the laboratory until early 1995. Kyaaro, acquired at about 3 months, also in 1991, remained in the laboratory until 2001. Griffin, obtained at 7 weeks in 1995, is still part of the research, as is Arthur, who was acquired in 1999 when he was approximately a year old. Birds’ living conditions outside of testing and training have been described in detail previously (e.g., Pepperberg et al., 1998), except that now birds always share a room (Pepperberg and Wilkes, 2004). In brief, birds are trained, tested and sleep in the laboratory; sleeping cages are Avian Adventures (28 in. 22 in. 26 in.). Birds have access to their cages except during training and testing, but spend most of their days either on T-stands or atop their cages. Training and testing occurs on T-stands. Water and Harrison’s Bird Diet are available ad lib; fruit, vegetables, nuts, etc. are provided outside of testing and training periods. 2.2. Training The primary training procedure is the Model/Rival (M/R) technique, originally developed by Todt (1975) and adapted for use in my laboratory. Only in specific studies described below have other techniques been employed. The M/R training system (background in Pepperberg, 1999) uses three-way social interactions among two humans and a parrot to demonstrate targeted vocal behavior. The parrot observes two humans handling one or more objects, then watches humans interact: the trainer presents, and queries the human model about, the item(s) (e.g., ‘‘What’s here?’’, ‘‘What color?’’) and gives praise and the object(s) to reward correct answers referentially. Incorrect responses (like those the bird may make) are punished by scolding and temporarily removing item(s) from sight. Thus the second human is a model for the parrot’s responses, its rival for the trainer’s attention, and also illustrates error consequences: the model must try again or talk more clearly if the response was (deliberately) incorrect or garbled, thereby demonstrating corrective feedback. The bird is also queried and rewarded for successive approximations to correct responses; thus training is adjusted to its level. Unlike other laboratories’ M/R procedures (see Pepperberg, 1999), ours interchanges roles of trainer and model, and includes the parrot in interactions to emphasize that one being is not always the questioner and the
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other the respondent, and that the procedure can effect environmental change. Role reversal also counteracts an earlier methodological problem: birds whose trainers always maintained their respective roles responded only to the questioner. Our birds, however, respond to, interact with, and learn from all humans. M/R training exclusively uses intrinsic reinforcers: to ensure closest possible correlations of labels or concepts to be learned with their appropriate referent, reward for uttering ‘‘X’’ is X: the object to which the label or concept refers. Earlier unsuccessful programs for teaching birds to communicate with humans used extrinsic rewards (Pepperberg, 1999): one food that neither related to, nor varied with, the label or concept being taught, thereby delaying label and concept acquisition by confounding the label of the targeted exemplar or concept with that of the food. My birds never receive extrinsic rewards. Moreover, initial use of the label to request the item also demonstrates functionality. Because Alex sometimes fails to focus on targeted objects, I trained him to use the phrase ‘‘I want X’’ to separate labeling from requesting (see Pepperberg, 1999). Thus having identified Y (something he may not desire) by identifying its material, color, shape, etc. (depending upon the question he was posed) his reward is then the right to request something more desirable, which provides flexibility but maintains referentiality. To receive X after identifying Y, Alex must state ‘‘I want X’’ and trainers will not comply until the appropriate task is completed. Thus his labels are true identifiers, not merely emotional requests. Adding ‘‘want’’ provides additional advantages: first, trainers can distinguish incorrect labeling from appeals for other items, particularly during testing, when birds unable to use ‘‘want’’ might not be erring but asking for treats, and scores might decline unrelated to competence. Second, birds may demonstrate low-level intentionality: Alex rarely accepts substitutes when requesting X, and continues his demands (Pepperberg, 1999). 2.3. Testing Birds are tested under rigorous conditions so as to avoid various possible types of cuing. Full details of test procedures can be found in Pepperberg (1999).
3. Results of M/R training As noted above, Alex has acquired several complex cognitive concepts. He not only produces various English labels, but also understands their use and the numerous questions we pose. He is not responding by rote to objects in his environment. So, for example, I can show him a particular object and ask him ‘‘What color?’’ (green), ‘‘What shape?’’ (four-corner), ‘‘What matter?’’ (wood) and ‘‘What toy?’’ (block). He could not respond appropriately unless he comprehended the labels for, and the concepts of, color, shape, matter and toy. Some of his accomplishments involve more abstract concepts of same/different, absence and number. Some of the relevant studies are described here. For discussions of topics such as bigger/smaller, recursion and conjunction, see Pepperberg (1999). 3.1. Same/different and absence According to Premack (1983), same/different requires use of arbitrary symbols to represent relationships of sameness and difference between sets of objects and the ability to denote the attribute that is same or different, that is, requires symbolic representation. Comprehension of related tasks, such as match-to-sample, non-match-to-sample, oddity-from-sample, or homogeneity and non-homogeneity, in contrast, require only that subjects show a savings in the number of trials needed to respond to B and B as a match (or as a homogeneous field) after learning to respond to A and A as a match (and likewise by showing a savings in trials involving C and D after learning to respond appropriately to A and B as non-matching or non-homogenous;
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Pepperberg, 1999). Subjects performing match-to-sample and non-match-to-sample might even be responding based on ‘old’ versus ‘new’, ‘familiar’ versus ‘unfamiliar’ (Premack, 1983), that is, on the relative number of times they experience the A sample versus the different B samples. Subjects that understand same/different, however, not only know that two non-identical red objects are related the same way as are two non-identical blue objects – in terms of color – but also know that the red objects are related to each other a different way than are two non-identical square objects, and, moreover, can transfer this understanding to any attribute of an item (Premack, 1983). A subject would likewise have to understand the concept of difference (Pepperberg, 1999). Using M/R training, my students and I taught Alex not only to produce the appropriate category label for the attribute that is same or different for any combination, but also to respond ‘‘none’’ if nothing is same or different (that is, to the absence of information about these concepts; Pepperberg, 1988), even for objects not used in training or that he cannot label. Furthermore, his responses were still above chance when I tested if he were truly attending to the questions—for example, when the question ‘‘What’s same?’’ was posed with respect to a green wooden triangle and a blue wooden triangle. If he were ignoring the question and responding based on his prior training and object attributes, he would have determined, and responded with the label for, the one anomalous attribute (in this case, ‘‘color’’). Instead, he responded with one of the two appropriate answers [i.e., ‘‘shape’’ or ‘‘mah-mah’’ (matter); Pepperberg, 1987a]. Alex’s use of ‘‘none’’ (Pepperberg, 1988, 1999) is interesting because learning to understand and comment upon non-existence, or even the slightly more basic notion of absence, although seemingly simple, denotes a relatively advanced stage in cognitive and linguistic development (Brown, 1973). An organism reacts to absence only when the expected presence of events, objects or other information in its environment is violated, that is, only when a discrepancy exists between the expected and actual state of affairs (see Pepperberg, 1999). Of course, Alex was responding to the absence of an attribute, not to the absence of an object, which is an important distinction. 3.2. Numerical concepts Given that Alex could understand categories involving attributes inherent to an object (e.g., color, shape) and abstract concepts of same/different and absence, could he form an entirely new categorical class for quantity? Could he be trained to reclassify a group of wooden objects known until now simply as ‘‘wood’’ or ‘‘green wood’’ so that he could identify them as ‘‘five wood’’? To succeed, he would have to understand that a new set of labels, ‘‘one’’, ‘‘two’’, ‘‘three’’, ‘‘four’’, ‘‘five’’ and ‘‘six’’ represented a means to categorize objects based on a combination of physical similarity within a group and the group’s quantity, rather than by physical characteristics alone. He would also have to generalize this new class of numerical labels to sets of novel objects, to objects in random arrays, and to heterogeneous collections. Note that Koehler (1950, 1953) and his colleagues (Braun, 1952; Lo¨gler, 1959) had already demonstrated Grey parrots’ sensitivity to quantity and basic concepts of numerosity and numerousness; that is, that Grey parrots could learn a form of match-to-sample involving sets of novel objects and random dot patterns representing quantity, and that the birds could transfer from simultaneous visual presentations to sequential visual and auditory presentations. But could Alex go beyond these tasks and use number as a categorical label? Could he use numbers symbolically? The several numerical concept studies performed with Alex do not demonstrate that his understanding of number matches that of adult humans (Fuson, 1988), but suggest that his concept of quantity is similar to that of a young child at the beginning stages of true counting.
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He can, for example, recognize and label different quantities of physical objects up to and including six (Pepperberg, 1987b). Objects need not be familiar, nor be placed in any particular pattern, such as a square or triangle. If presented with a heterogeneous collection – of X’s and Y’s – he can respond appropriately to questions of either ‘‘How many X?’’ or ‘‘How many Y?’’ (Pepperberg, 1987b). Work with other types of heterogeneous collections demonstrates even more advanced skills. Alex can be shown a ‘‘confounded number set’’ (collections of four groups of items that vary in two colors and two object categories—e.g., blue and red wood and blue and red wool) and be asked to label the number of items uniquely defined by the combination of one color and one object category (e.g., ‘‘How many blue wood?’’). His accuracy (Pepperberg, 1994) replicates that of humans in a comparable study (Trick and Pylyshyn, 1989). His level is therefore beyond what might be considered subitizing (a perceptual mechanism for recognizing small quantities without actually counting; think of how you label the number of dots on dominoes or dice; Pepperberg, 1999). The mechanisms that Alex uses are difficult to determine (Pepperberg, 1994, 2006). Overall, the data suggest that a non-human, non-primate, non-mammalian animal has a level of competence that, in a chimpanzee, would be taken to indicate a human level of cognitive processing (Pepperberg, 1999). These experiments, however, did not exclude the possibility that Alex might produce but not comprehend his number labels, as did apes and children in some studies (e.g., Savage-Rumbaugh et al., 1980, 1993; Fuson, 1988; Wynn, 1990). Such comprehension is crucial for true numerical competence (Fuson, 1988; Pepperberg, 1999). A student and I therefore performed a comprehension study (Pepperberg and Gordon, 2005), in which Alex was, without prior training on the task, asked ‘‘What color/object is [number]?’’ for collections of various simultaneously presented quantities (e.g., subsets of four, five and six blocks of three different colors; monochrome subsets of two keys, four corks and six sticks). His accuracy was above 80%, and was unaffected by array quantity, mass or contour; sometimes we used larger objects for the smaller quantities. Alex thus demonstrated numerical comprehension competence comparable to that of chimpanzees and very young children. Of particular interest was that at one point in the experiment, Alex, on his own initiative, transferred his ability to use ‘‘none’’ to comment on the absence of an attribute (same/different, bigger/smaller) to the absence of a specific quantity—albeit in a limited sense (Pepperberg and Gordon, 2005). A description of this behaviour follows. On the 10th trial within the first set of 12, Alex was asked ‘‘What color three?’’ to a set of two, three, and six objects. He replied ‘‘five’’, a response that was puzzling. Sometimes when he did not want to perform a given task, he would give all the possible wrong answers (Pepperberg, 1999) or even toss all the exemplars off of the tray, but rarely would he give an irrelevant response. I thus asked him twice more and each time he replied ‘‘five’’. Not attending to the tray, and thinking that maybe he wished to be queried about a different number, I finally said ‘‘OK, Alex, tell me, what color five?’’ He immediately responded ‘‘none’’ (Pepperberg and Gordon, 2005). Remember, there was no set of five objects. As noted above, Alex had been taught to respond ‘‘none’’ if no category (color, shape or material) was same or different when he was queried about the similarity or difference of two objects (Pepperberg, 1988); he had also spontaneously transferred this response to the query ‘‘What color bigger?’’ concerning two identically size objects in a study of relative size (Pepperberg and Brezinsky, 1991), but had never been taught the concept of absence of quantity nor to respond to absence of an exemplar. We thus repeated the question randomly throughout other trials with respect to each possible number to ensure that this situation was not an odd happenstance. On these six ‘‘none’’ trials, Alex made only one error, which, interestingly, was to label a color not on the tray. Remember, I had not trained the conventional term, ‘‘zero’’, to indicate the absence of quantity; Alex’s use of ‘‘none’’ for this purpose was unexpected.
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Overall, his understanding of ‘‘none’’ as a zero-like concept appears to resemble that of 3year-old children. Children actually seem to have to be about 4 years old before they achieve full adult-like understanding of the labels for zero and other numerals (Bialystok and Codd, 2000; Wellman and Miller, 1986). Whether Alex can fully understand the equivalence of ‘‘none’’ to the concept of zero is still to be determined (Pepperberg, 2006). 3.3. Other issues involving training The data that my students and I had accumulated concerning Alex’s cognitive and communicative abilities showed the incredible success of M/R training, but did not explain why it was such a powerful procedure. To answer that question, I would have to determine what would happen if some elements of input were lacking. Answering that question also required additional parrots, because Alex might cease learning merely because training had changed, not because of the type of change. So, while many of the experiments described above were proceeding with Alex, I began working with four new naive Greys – Kyaaro, Alo, Griffin, and Arthur – to test the relative importance of reference, context/function and social interaction in training. 3.4. Eliminating aspects of input My students and I performed eight experiments (Pepperberg, 1999; Pepperberg et al., 2000; Pepperberg and Wilkes, 2004). First, we compared simultaneous exposure of Alo and Kyaaro to three input conditions: I, audiotapes of Alex’s sessions, which were non-referential, not contextually applicable and non-interactive; II, videotapes of Alex’s sessions, which were referential, minimally contextually applicable and non-interactive; and III, standard M/R training. In I and II, birds experienced tapes in social isolation. Condition I paralleled early allospecific song acquisition studies (e.g., Marler, 1970); II involved then-unresolved issues about avian vision and video (e.g., Ikebuchi and Okanoya, 1999). We counterbalanced labels across birds, matching training time across sessions. Second, because interactive co-viewers could increase young children’s learning from video (Rice et al., 1990), a co-viewer now provided social approbation for viewing and pointed to the screen with comments like ‘‘Look what Alex has!’’, but did not repeat targeted labels, ask questions, or relate content to other training. Birds’ attempts at a label would garner only vocal praise. Social interaction was limited; referentiality and functionality matched earlier videotape sessions. Third, because extent of coviewer interaction might affect children’s learning from video, our co-viewer now uttered targeted labels and asked questions. Fourth, so that lack of reward would not deter video learning, a socially isolated parrot watched videos while a student in another room monitored its utterances through headphones and could deliver rewards remotely. Fifth, because birds might habituate to the single videotape used per label (even though each tape depicted many different responses and interactions among Alex and trainers), we used live video from Alex’s sessions. Sixth, because research showed that if adult–child duos failed to focus jointly on objects being labeled, the labels were not acquired (e.g., Baldwin, 1995), a single trainer faced away from the bird (who was within reach of, e.g., a key), talked about the object (‘‘Look, a shiny key!’’, ‘‘Do you want key?’’, etc.; sentence frames; Pepperberg, 1999), but had no visual or physical contact with parrot or object; a bird’s attempts at the targeted label would receive only vocal praise, thereby eliminating some functionality and considerable social interaction. Parrots failed to acquire referential use of targeted labels in any non-M/R condition, but succeeded in concurrent M/R sessions (Pepperberg, 1999). Seventh, we eliminated some interactive aspects of modeling by having a
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single student label objects, query Griffin, jointly attend to objects, and thus interact fully with Griffin and objects. Griffin did not utter labels in 50 such sessions, but clearly produced labels after two or three subsequent M/R sessions. We suspected latent learning: Griffin apparently stored labels, but did not use them until he observed their use modeled. (NB: Birds switched to M/R training after 50 video sessions needed 20 sessions before producing labels.) Finally, we performed video studies with a liquid crystal monitor with Arthur and Griffin to see if standard cathode ray tube flicker-fusion affected learning (Ikebuchi and Okanoya, 1999); birds attended more closely to this screen but did not acquire targeted vocalizations. Results thus emphasize the importance of reference, demonstrations of contextual use/functionality and social interaction in training if parrots are to communicate with humans rather than mimic speech. 3.5. Mutual exclusivity: studying subtle changes in input Our parrots’ learning processes may also parallel young children’s mutual exclusivity (ME) (Pepperberg and Wilcox, 2000). ME refers to children’s assumption during early word acquisition that each object has one, and only one, label (e.g., Liittschwager and Markman, 1994). Along with the whole object assumption (that a label refers to an entire object, not some feature), ME supposedly guides initial label acquisition. ME may also help children interpret novel words as feature labels (overcome the whole object assumption), but very young children may find second labels for items initially more difficult to acquire than the first because second labels are viewed as alternatives (Liittschwager and Markman, 1994). Input, however, affects ME: children (Gottfried and Tonks, 1996) and parrots like Alex, who receive inclusivity data (X is a kind of Y; e.g., color labels taught as additional, not alternative, labels, ‘‘Here’s a key; it’s a green key’’), generally accept multiple labels for items and form hierarchical relations. Thus, shown a wooden block, Alex answers ‘‘What color?’’, ‘‘What shape?’’, ‘‘What matter?’’ and ‘‘What toy?’’ (Pepperberg, 1999). Parrots given colors or shapes as alternative labels (e.g., ‘‘Here’s key’’ and later ‘‘It’s green’’), however, have difficulty learning to use these modifiers for previously labeled items. Griffin, thus trained, initially answered ‘‘What color?’’ with object labels. Similarly, while learning an object label – cup – he answered ‘‘What toy?’’ with colors and had difficulty acquiring ‘‘cup’’. Thus small input changes affect label acquisition as much for parrots as young children. 4. Unexpected similarities between primates and parrots Other unexpected similarities exist for birds and primates with respect to the development of communicative competence. These parallels involve behavior for which underlying mechanisms may suggest a commonality in brain structure and/or information processing. I discuss two studies: combinatory learning and phonological processing. 4.1. Combinatory learning Based primarily on behavioral data, researchers (e.g., Johnson-Pynn et al., 1999) argue that a common neural substrate initially underlies young children’s parallel development of communicative and object (manual) combinations, that a homologous substrate in great apes allows similar, limited, parallel development, and that such data imply a shared evolutionary history for communicative and physical behavior. But Griffin showed comparable limited, parallel combinatorial development of three-item and three-label combinations (Pepperberg and
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Shive, 2001). Percentages of physical and vocal combinations were roughly equal; despite months of training, vocal three-label combinations emerged only when he more frequently initiated three-objects combinations; vocal combinations were generally not those trained; and physical combinations were performed with his beak, not feet. Moreover, unlike Johnson-Pynn et al.’s Cebus (1999), Griffin was not trained on physical tasks and we limited training on threelabel combinations (2,5-corner wood/paper) to see if spontaneous manipulative behavior developed in parallel with vocal complexity. Although Griffin’s behavior – and that of our most advanced subject, Alex (Pepperberg, 1999) – is equivalent neither to human language nor to 2–3-year-old humans’ combinatory behavior, I suggest that our Grey parrots’ behavior patterns match some of non-human primates, that parallel combinatory development is not limited to primates, and that a particular mammalian brain structure is not uniquely responsible for such behavior. Specifically, searches for and arguments concerning responsible substrates and common behavior should not be restricted to primates (Medina and Reiner, 2000). 4.2. Phonological awareness? In a recent study (Pepperberg, 2005) Alex showed what appears to be vocal segmentation and phonological awareness; that is, that he understands that labels consist of individual units that can be recombined in novel ways to create novel vocalizations. The data also suggest that Alex’s ability is a learned behavior, is not uniquely human, and is dependent upon having considerable experience with English speech and sound–letter training. A younger bird, lacking such training, did not engage in such behavior. Note, too, that this behavior demonstrates the process by which Alex acquired the targeted label. In this study, both Arthur and Alex were trained on the label ‘‘spool’’; both parrots knew the similar-sounding ‘‘wool’’, but only Alex had had extensive training on /s/ from an experiment on phonemes. Note that /p/ is particularly difficult for parrots, lacking lips, to acquire, and that they seemingly use esophageal speech in its production (Patterson and Pepperberg, 1998); /sp/ is even more difficult. Arthur produced ‘‘spool’’, but the /p/, when sonagraphed, was actually a whistle. Alex, in contrast, produced ‘‘s[pause]wool’’ for a full year, then switched to a ‘‘spool’’ almost identical to mine when sonagraphed. Exactly because of the difficulty of producing /p/, Alex may have used ‘‘s[pause]wool’’ such that two known utterances provided the overall structure and the pause was a place filler, like that occasionally used by young children, until he could learn how to insert the /p/ and adapt the vowel. Specifically, Peters (2001) suggests that children use fillers to preserve syllable numbers or the prosodic rhythm of targeted vocalizations until the standard form is learned. Alex’s behavior suggests that he, too, was aware of the need for something additional and different to complete the vocalization. Simply omitting or closing the gap – and responding on the basis of sound similarity – would have produced /swUl/ (‘‘swull’’), not /swul/ (‘‘swooool’’). 5. Overall conclusions A key message of this paper, presented within the context of a symposium on Animal Sentience, is to encourage an awareness of, and a sensitivity to, the abilities of non-humans, particularly non-primate and non-mammalian subjects. For far too long, animals in general, and birds in particular, have been denigrated and treated merely as creatures of instinct rather than sentient, intelligent beings. The data presented here and elsewhere (see Pepperberg, 1999)
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demonstrate that many species of animal posses cognitive capacities that we have until now considered unique to humans and other primates. All we need to examine these capacities are some enlightened research tools. My immediate hope is that the material presented here will help us respect the cognitive abilities of creatures who may at first seem so very different from humans but, in reality, share many of our abilities. My long-term hope is that the material will be used to improve and enrich the lives of captive and companion animals, to prevent habitat destruction and unnecessary capture of wild animals, and to strengthen our bonds with non-humans. References Baldwin, D.A., 1995. Understanding the link between joint attention and language. In: Moore, C., Dunham, P.J. (Eds.), Joint Attention: Its Origin and Role in Development. Erlbaum, Hillsdale, NJ, pp. 131–158. Bialystok, E., Codd, J., 2000. Representing quantity beyond whole numbers: some, none and part. Can. J. Expt’l Psychol. 54, 117–128. Braun, H., 1952. Uber das Unterscheidungsvermo¨gen unbenannter Anzahlen bei Papageien. Z. Tierpsychol. 9, 40–91 (Concerning the ability of parrots to distinguish unnamed numbers.). Brown, R., 1973. A First Language. Harvard University Press, Cambridge, MA. Fuson, K.C., 1988. Children’s Counting and Concepts of Number. Springer-Verlag, New York. Gottfried, G.M., Tonks, J.M., 1996. Specifying the relation between novel and known: input affects the acquisition of novel color terms. Child Dev. 67, 850–866. Ikebuchi, M., Okanoya, K., 1999. Male zebra finches and Bengalese finches emit directed songs to the video images of conspecific females projected onto a TFT display. Zool. Sci. 16, 63–70. Johnson-Pynn, J., Fragaszy, D.M., Hirsh, E.M., Brakke, K.E., Greenfield, P.M., 1999. Strategies used to combine seriated cups by chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and capuchins (Cebus apella). J. Comp. Psychol. 113, 137–148. Koehler, O., 1950. The ability of birds to ‘count’. Bull. Anim. Behav. Soc. 9, 41–45. Koehler, O., 1953. Thinking without words. In: Proceedings of the XIVth International Congress of Zoology. pp. 75– 88. Liittschwager, J.C., Markman, E.M., 1994. Sixteen- and 24-month olds’ use of mutual exclusivity as a default assumption in second-label learning. Dev. Psychol. 30, 955–968. Lo¨gler, P., 1959. Versuche zur Frage des ‘‘Za¨hl’’-Vermo¨gens an einem Graupapagei und Vergleichsversuche an Menschen. Z. Tierpsychol. 16, 179–217 (Studies on the question of ‘‘number’’ sense in a Grey parrot and comparative studies on humans.). Marler, P., 1970. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 71, 1–25. Medina, L., Reiner, A., 2000. Do bird possess homologues of mammalian primary visual, somatosensory and motor cortices? TINS 23, 1–12. Patterson, D.K., Pepperberg, I.M., 1998. A comparative study of human and Grey parrot phonation: acoustic and articulatory correlates of stop consonants. JASA 103, 2197–2213. Pepperberg, I.M., 1987a. Acquisition of the same/different concept by an African Grey Parrot (Psittacus erithacus): learning with respect to color, shape, and material. Anim. Learn. Behav. 15, 423–432. Pepperberg, I.M., 1987b. Evidence for conceptual quantitative abilities in the African Grey Parrot: labeling of cardinal sets. Ethology 75, 37–61. Pepperberg, I.M., 1988. Acquisition of the concept of absence by an African Grey parrot: learning with respect to questions of same/different. JEAB 50, 553–564. Pepperberg, I.M., 1994. Evidence for numerical competence in an African Grey parrot (Psittacus erithacus). J. Comp. Psychol. 108, 36–44. Pepperberg, I.M., 1999. The Alex Studies. Harvard University Press, Cambridge, MA. Pepperberg, I.M., 2005. Grey parrots do not always ‘‘parrot’’: roles of imitation and phonological awareness in the creation of new labels from existing vocalizations. In: AISB Proceedings, Hatfield, UK. Pepperberg, I.M., 2006. Grey Parrot (Psittacus erithacus) numerical abilities: addition and further experiments on a zerolike concept. J. Comp. Psychol. 120, 1–11. Pepperberg, I.M., Brezinsky, M.V., 1991. Acquisition of a relative class concept by an African Grey parrot (Psittacus erithacus): discriminations based on relative size. J. Comp. Psychol. 105, 286–294.
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