Introduction

Rosch et al. (1976) suggested a chronological and hierarchical structure for concepts, such that humans first learn basic level concepts (e.g., dog) and only later are able to learn subordinate (e.g., poodle) and superordinate (e.g., mammal or animal) concepts (see also Mervis & Rosch, 1981). This chronology of concept learning seems tied to language in that the basic level category words are the first learned and the most commonly used. It has been suggested that the formation of superordinate categories relies less upon perceptual feature analysis and more on an understanding of how the category coheres, across significant perceptual variance (Spalding & Ross, 2000). Superordinate categories are thus thought of as being more conceptually based or “abstract” relative to basic level categories, and it has been speculated that language is necessary for the formation of these later categories (Benelli, 1988; Keil, 1988; Nelson, 1988; Premack, 1983). Organisms may be inherently preprogrammed to distinguish between items at the level of the basic concept perceptually (Cerella, 1979; Eimas & Quinn, 1994). However, Mandler (2000) has articulated an opposing view, supported by several studies, in which the conceptualization of superordinate categories by human infants may actually precede that of basic level categories. Mandler’s description highlights the distinction between perceptual and conceptual categorization, a distinction not traditionally acknowledged by other researchers. In her view, exemplars within basic level categories may be associated together on a perceptual basis before exemplars from superordinate categories are associated perceptually. In contrast, when forming conceptual categories, which are based on shared, underlying properties as opposed to perceptual similarity, more global, abstract categories such as animals, foods, etc., may emerge first. This may be the case because children learn about broad categories, such as animate/inanimate distinctions prior to learning specific distinctions such as between reptiles and mammals.

Recent work (Coley, 2007) has indicated that children may make global distinctions such as between animals and non-animals, but are less likely, compared to adults, to consider humans to be similar to other primates or non-primate animals. This recent work, highlighting differences between children and adults with regard to between categorical judgments of similarity, reinforces the notion that such categorization is not made on a purely perceptual basis. In addition, Gelman & Davidson (2013) have shown that both children and adults use category membership more than similarity to make basic level category inferences, although their studies involved experimenter-created rather than actual natural categories. Thus there is some disagreement as to what sorts of categorization depend upon physical similarity, depend upon language and emerge first in the human infant. By studying concept formation in non-human primates one can determine parallels in the emergence of non-language based categorization. In the current study, two species of great ape (orangutans and a gorilla) were required to match images based on biological classifications at the level of species, family or class.

Although taxonomic class groupings may be considered basic level concepts (Roberts & Mazmanian, 1988), it has been suggested that the ability to make taxonomic classifications of natural stimuli depends upon biological or scientific knowledge (Eimas & Quinn, 1994; Hampton, 1998; Inagaki, 1989), as well as language (Anggoro, Medin & Waxman, 2010; Benelli, 1988; Gelman, 1989; Nelson, 1988). Quinn & Tanaka (2007) found that expertise within the same basic level category aided infants in the ability to discriminate other concrete level categories, emphasizing the role of expertise in category discrimination. Coley (2007) showed that children of eight years or older were more likely to categorize humans as being similar to primates and primates as being more similar to mammals than non-mammals, but younger children were not sensitive to these taxonomic groupings, further supporting the notion that intermediate level biological categories are learned rather than perceived. At least in humans, it appears that discriminations are not made solely on the basis of similarity of perceptual features. Categorizing stimuli according to biological taxonomies may then be presumed to be a uniquely human tendency.

Against this supposition, exciting recent work from neuroscience has demonstrated a common code for inferior temporal (IT) object representations in monkeys and humans (Kiani et al., 2007; Kriegeskorte, 2008). This work has demonstrated global representations along a continuum of inanimate to animate objects, but also within category distinctions between different taxonomic groups. Connolly et al. (2012) have suggested a continuum of activation representing categorical structure from insects to primates that mirrors the continuum from inanimate to animate objects. Connolly and colleagues suggest a categorical structure within the domain of animate objects that reflects the biological relations among species, suggesting that such categorization may be innate within primates. Furthermore, Murai and colleagues (Murai et al., 2004; Murai et al., 2005), using a familiarization-novelty preference task, have suggested that infant monkeys, chimpanzees and humans may spontaneously form categories at least at the global level, using categories of mammals, furniture and vehicles. The current experiments investigated the ability to make explicit classifications of more finite natural class distinctions in two other species of Great Ape; orangutans and gorillas. In the case of non-humans, categories would be based on shared observable features rather than on underlying knowledge of taxonomic class structures, particularly given that the only information provided involves visual features in two dimensional photographs. However, it was of interest to determine whether exemplars of more closely related groupings are more readily categorized together compared to more distantly related members of the same class. We predicted that orangutans may readily categorize stimuli from both concrete and intermediate level categories, whereas the gorilla might categorize stimuli more readily at the concrete level.

Subordinate categories, for example, ‘poodles’, are described as being concrete (or least abstract) along a hierarchy of abstraction because exemplars within such categories share many readily perceived features and can be easily distinguished from exemplars from other categories on a purely perceptual basis. Basic level categories, such as ‘dogs’, are described as being intermediate in terms of abstractness. The variability within an intermediate category is greater than the variability within a concrete level category. For instance, the more general category of dogs includes not only poodles but hounds, terriers, and many other types of dogs, which may vary in terms of size, color and distinctive features such as the long, short body of the dachshund. However, category distinctiveness is also increased such that members within an intermediate level category share fewer features with members of other intermediate level categories, whereas concrete exemplars may share many features with exemplars from other concrete level categories subsumed within the same intermediate category. For example, toy poodles may look a lot like the bichon frise but dogs may not look much like other mammals such as whales or marsupials. At the most abstract level, such as ‘animal’, superordinate category exemplars share even fewer perceptual features within a category but also share even fewer features with members of other abstract categories. The category ‘mammal’ may be considered superordinate to the basic level ‘dog’, but, in keeping with previously published studies (Roberts & Mazmanian, 1988; Vonk & MacDonald, 2002; Vonk & MacDonald, 2004; Vonk, Jett & Mosteller, 2012; Vonk et al., 2013), ‘mammals’ will be considered intermediate with ‘animal’ being considered the most abstract level category.

Of course, level of expertise determines category level to some degree. For an expert herpetologist, insects may be easily categorized at much finer levels than would be the case for a third grade science student, or a novice adult, for that matter. Thus, while the most generic level of categorization, e.g., insects may be a basic or intermediate level of category for the novice, a more highly specified category such as hymenoptera may serve as a basic level category for the herpetologist, with categories of wasps, bees, and ants–or even particular species of each, serving as subordinate or concrete levels. For the purpose of describing the current study, it is assumed that apes have no special expertise regarding unfamiliar members of the primate order, or broader class of mammals, birds, fish, insects, so the intermediate level will be used to refer to class while the concrete level will be used to refer to species discriminations.

Often abstract level categories can be discriminated only with some additional conceptual knowledge, rather than by relying on perceived shared attributes. For instance one would not know that insects, birds, amphibians, and mammals all belonged to the category ‘animal’ if one was unaware of their unobservable properties such as the ability to eat, breathe, reproduce, etc. The ease with which category membership can be determined on strictly a perceptual basis thus declines as one moves from concrete to abstract level categories. The terms concrete and subordinate, intermediate and basic, and abstract and superordinate have been used interchangeably. The former terms will be used exclusively throughout the remainder of this manuscript in keeping with previous research (Vonk & MacDonald, 2002; Vonk & MacDonald, 2004; Vonk, Jett & Mosteller, 2012; Vonk et al., 2013).

There is much evidence for concrete level discrimination learning in primates, (Fujita, 1987; Fujita & Matsuzawa, 1986; Fujita et al., 1997; Marsh & MacDonald, 2008; Yoshikubo, 1985) as well as in pigeons (Herrnstein, 1979; Herrnstein, Loveland & Cable, 1976), but there is much less evidence for intermediate or abstract level natural concept discrimination learning (although see Brooks et al. (2013) for evidence in rats). The difficulty with Brooks et al. (2013) is that all of the discriminations were also between animate and inanimate categories (e.g., chairs versus flowers and cars versus humans)–allowing the rats to make more global level discriminations. Recently, investigators (Autier-Dérian et al., 2013) have shown that domestic dogs are capable of categorizing many diverse dog species together into a single basic level “dog” category. The dogs were also able to discriminate between the species, demonstrating concrete level categorization. Caution is appropriate when making cross species comparisons as the reader must take into account possible differences in perceptual systems in different organisms. However, the species tested in relevant paradigms share sophisticated visual acuity and color vision making them suitable candidates for categorical discrimination research. In a more relevant study, Tanaka (2001) demonstrated that chimpanzees were able to discriminate exemplars both within intermediate level categories (at the concrete level) and between intermediate categories. The chimpanzees were trained to match exemplars that belonged to the same concrete level category and subsequently matched those exemplars to other members of the same intermediate, but different concrete level category, when a concrete level match was no longer an option. Because Tanaka’s chimpanzees were trained to make concrete level matches and then tested on intermediate level matches to the same stimuli it is difficult to compare the chimpanzees’ performance on the two levels of discrimination.

In one of only five published attempts to compare concept learning at different levels of abstraction in non-humans, Roberts & Mazmanian (1988) studied concept discrimination by pigeon, squirrel monkey and human subjects across three levels of abstraction, where abstraction was defined as the breadth of the category to be learned. At the concrete level, the subjects were asked to discriminate between photographs of one bird species (kingfishers) and other birds. At the intermediate level they were asked to discriminate between birds and other animals. Finally, at the most abstract level they were asked to discriminate between animals and non-animals. The authors found that humans easily discriminated concepts at all levels of abstraction, whereas both monkeys and pigeons had difficulty with the intermediate level discrimination. This finding was somewhat surprising because this intermediate level corresponds to the basic level that Rosch presumed was easiest for humans to learn (Keil, 1988; Mervis & Rosch, 1981; Rosch et al., 1976). Ross et al. (2003) suggest that children acquire such concepts by the age of six years. However, the results may confirm Mandler’s predictions (2000), particularly if the apes are performing conceptual rather than perceptual categorizations.

Vonk & MacDonald (2002) and Vonk & MacDonald (2004) trained orangutans and a gorilla to discriminate between photographs of members of their own species and humans, and between members of their own species and other primates (concrete level), between primates and other species (intermediate level) and between animals and non-animals (abstract level). The orangutans quickly learned the concrete and intermediate level discriminations and also learned the most abstract discrimination, but with slightly more difficulty. The gorilla subject appeared to have the most difficulty with the intermediate level discrimination, although she also learned all discriminations and showed significant positive transfer to novel stimuli. Thus both species of Great Ape demonstrated the ability to learn concepts at each level of abstraction, but the orangutans appeared to learn the basic or intermediate level discrimination the most readily while the gorilla learned it with the most difficulty. More recent follow-ups have shown chimpanzees to have the most difficulty with the most abstract discriminations (Vonk et al., 2013) in that they required more sessions to reach criterion as discriminations became more abstract, and were less likely to show significant transfer. In contrast, black bears showed significant transfer at all levels of concept discrimination, even when trained on the most abstract problems first (Vonk, Jett & Mosteller, 2012).

Some of the orangutans in the previous study (Vonk & MacDonald, 2004) learned to select photos of primates very rapidly (e.g., within three 10-trial sessions), despite the fact that the primates presented to them were of unfamiliar species. It was possible that they simply selected photos that they preferred. A spontaneous preference indicates that subjects may not have learned to abstract particular concepts or categories as being “correct” within the context of the experiment but implicitly preferred photos that happened to belong in the same taxonomic group. However, the very existence of a preference suggested that they did perceive primates as distinct from other species regardless of whether they explicitly recognized primates as belonging to a coherent category. Another possibility was that they selected photos of primates because these photos were more similar to photos that had previously been presented, although selecting these photos had not been reinforced. The latter explanation is unlikely, because of latent inhibition, the finding that it becomes more difficult to learn to respond to previously unreinforced stimuli due to retroactive interference. The fact that this was not the case for the orangutans suggests that they were attending to the category of the photo and not the specific exemplar itself. In addition, different and diverse primate species were presented in each subsequent transfer photo set, and transfer performance remained high. However, the question remained as to whether or not these apes would be equally likely to learn other intermediate level discriminations, including those more analogous to the bird/other animal discrimination tested by Roberts & Mazmanian (1988). Both chimpanzees and black bears were tested on an intermediate problem in which the two categories were equally inclusive and novel (carnivores for chimpanzees, or primates for bears, versus ungulates). The black bears performed better than the chimpanzees in terms of acquisition and transfer, suggesting the possibility of different mechanisms for forming the discriminations. Here, it was of interest to directly contrast the acquisition of matching intermediate level concepts to their acquisition of matching concrete level concepts in an identical procedure for the orangutans and gorilla tested previously.

The subjects were presented with a delayed matching-to-sample (DMTS) task in order to examine their understanding of several categories simultaneously. In contrast to the previous studies, where the subjects learned to discriminate a single category at a time, use of a DMTS procedure made it possible to have them categorize stimuli from several different species or classes within a single session. Each trial involved presentation of a sample that was replaced by two comparison photos once the subject attended to the sample. The reinforced comparison was a different photo of the same or different member of the same species or family as the sample (Experiment 1), or a photo of a different species from the same class as the sample (Experiment 2). The non-reinforced comparison was a photo of a member of a different primate species (Experiment 1), or a member of a different class (Experiment 2). Experiment 1 tested for concrete level discriminations in that the categorizations could be made by matching perceptual features of the stimuli. In Experiment 2 an effort was made to select photographs of species belonging to the same taxonomic class that were nonetheless perceptually quite distinct from one another. For instance, a photo of a stingray shared few features with a photo of the head of a blenny fish, but both belonged to the fish category. Backgrounds varied both within and between categories. Because the comparison stimuli did not share many perceptual features with the sample stimulus, the subjects’ ability to correctly match the photos might indicate the capacity for forming concepts at the intermediate level of abstraction.