The past several decades have seen increased interest in animal culture. Much of the debate has focused on whether any animals have culture, and on how human culture might differ from the culture of animals. Framing the debate in these ways has led to a consideration of culture being a uniquely human phenomenon (Galef 1992), as a single kind of phenomenon that is shared across several (perhaps very many) species (Laland and Hoppitt 2003; Ramsey 2013), or as existing in many species but coming in a unique form in humans (Tomasello 2016). While I think that many species have culture, and that humans may have unique adaptations for cultural learning, the way that most researchers talk about culture is problematic. Most researchers speak of culture as being a single kind of thing that animals either have or don’t have, or if both animals and humans have it, what the humans have is its own single kind of thing, “human culture”. The problem is, I shall argue, that culture comes in a variety of kinds, and that a single species, including humans, may have multiple kinds of culture.
When I say that most researchers treat culture as a single kind, I mean that (1) they treat it as arising from a single kind of psychological process or mechanism, or (2) that even if it is supported by multiple psychological processes, those different processes and mechanisms all produce the same kind of thing. The problem with (1) is that it risks ignoring certain processes that produce culture, while favoring others. This could lead to researchers ignoring instances of culture in certain species, or it may lead researchers to over-intellectualize culture. The latter problem could lead to researchers ignoring examples of human culture that we might share with many species, and instead leads them to focus on examples of human culture that rely on very complex psychological processes, and to search for those same processes in other animals. The underlying assumption is that all examples of culture in humans arise from complex psychological processes. But this assumption is problematic as it keeps us from understanding the nature of culture in our own species as well as in others. The problem with (2) is that researchers may overlook important differences between instances of culture, both when studying it in a single species and when comparing the cultures of different species. For example, if the spread of tool use in a chimpanzee community is cultural and relies on complex forms of cognition, and the same community also has other cultural traditions that rely on less sophisticated psychological processes, lumping both instances together as simply “culture” risks missing important differences between the two cases.
In this chapter, I argue that current research shows that culture comes in at least two different kinds: associative and cognitive; that these kinds are present in very many species of animals; and that the same species may have both kinds of culture. While most of the paradigmatic cases of human culture are cognitive in nature, it is possible that humans also have “lower” forms of culture that are often ignored by researchers. A consequence of all of this is that the way we tend to speak about culture is too simplistic. If we are going to compare cultures in different species, we will first need to determine the kinds of culture each species possesses.
I will adopt Ramsey’s definition of culture: “culture is information transmitted between individuals or groups, where this information flows through and brings about the reproduction of, and a lasting change in, the behavioral trait” (Ramsey 2013, 2017). This definition of culture has advantages over the most common alternatives which stress culture as tradition produced by some kind of social learning (see, e.g., Galef 1992; Whiten and van Schaik 2007). It is also broad enough to allow that animals have culture and that culture could be supported by a variety of different psychological processes and mechanisms.
The view that culture is a tradition stems from the methods researchers typically employ when studying culture in animals. Researchers often begin by looking for evidence of different behavioral traditions in different populations of the same species of animal. For example, researchers studying culture in chimpanzees may be interested in how geographically distinct populations construct different tools. A difficulty with this approach to studying culture is that such traditions may arise because of differing ecological constraints or from the genetic makeup of the communities. Accordingly, researchers must rule out the possibilities that the tradition is not cultural. They often do this by restricting “culture” to those traditions that arise from social learning (see, e.g., Whiten and van Schaik 2007).
By requiring that behavioral traditions are the products of social learning, we avoid the problems of the ecological and genetic causes. However, what counts as social learning is controversial. Stimulus enhancement occurs when a demonstrator exposes an observer to a single stimulus, and, as a result, the observer’s behavior changes with regard to that stimulus. Stimulus enhancement can facilitate the production of widespread behaviors. For example, adult graylag geese will bite at the stems of butterbur plants. Nearby goslings observe this behavior and, as a result, are attracted to the butterbur plant and begin to explore it. The result is that the goslings learn a new feeding technique which becomes widespread in the flock (Fritz et al. 2000). While many researchers hold that such relatively simple forms of learning are examples of social learning (e.g., Heyes 2012), other researchers restrict social learning, or at least the social learning that can produce culture, to those relatively complex forms of learning like imitation, which involve complex cognition (e.g., Galef 1992). If we accept the more conservative definitions of social learning, we risk excluding examples of culture, such as the feeding behaviors of graylag geese, which are acquired by different means.
What is shared across a culture is information. However, “information” is itself a vague term. Genetic information is shared across a species, but sharing genetic information is not the same as sharing cultural information. Ramsey explicitly restricts cultural information to information that “flows through” behavior, and his notion of information is explicitly Drestkean. Dretske employs a teleofunctional account of information where certain states have the function of providing information about some object, event, or relation (Dretske 1980, 1993). Speedometers, when properly set up, provide us with information about speed because they have the function of telling us how fast we are going. Similarly, on this view, organs and behaviors that have a natural function from evolution will also carry information. Most importantly, for present purposes, learning produces functional states that carry information. When an organism learns to avoid a predator, it acquires a psychological state that carries information about that predator. Culture arises when such learning “flows through” the behavior of another individual or group and produces a “lasting change in the behavioral trait” (Ramsey 2013, 2017).
Ramsey’s definition focuses on what is shared by members of the same culture while also dissolving debates about what should count as social learning. However, given the diversity of mechanisms and psychological processes underlying culture, we might suppose that some instances of culture will be considerably different from other instances. For example, culture that arises from relatively basic forms of social learning might be constrained in ways that other instances of culture are not. In this way, we can treat Ramsey’s definition as a general notion under which we can carve out more fine-grained kinds of culture.
It is common in comparative psychology to distinguish between cognition and association. This distinction has recently come under a considerable amount of scrutiny (see, e.g., Penn and Povinelli 2007; Buckner 2013, 2017). For present purposes, it will not be necessary that certain behaviors be explained wholly by cognition or by association, but only that there are some behaviors that are best explained primarily by associative processes and mechanisms, and other behaviors that are best explained by accounts that are primarily cognitive.
Associationists tend to favor explanations of behavior that rely on contingency learning that is based on stimulus-bound associative mechanisms (Penn and Povinelli 2007). Consider stimulus generalization. Animals may learn to respond to a stimulus in a particular way. When presented with new, perceptually similar stimuli, the animal automatically transfers their learned response to these novel stimuli. In other words, the animal has learned to generalize from one stimulus to all perceptually similar stimuli.
Stimulus generalization is clearly stimulus bound: the animal must detect perceptual similarity in order to respond to a novel stimulus in the same way they responded to past stimuli. Furthermore, it is associative – the organism detects the similar perceptual features of the stimulus and associates these with past rewards or punishments.
Cognitive explanations usually appeal to mental representations, or to complex learning processes that rely on structured information processing. Researchers appeal to cognitive explanations of behaviors when they think that the behavior in question is too complex to be explained by associative learning. For example, Weir and Kacelnik found that their New Caledonian crow, Betty, could develop novel methods to construct hook tools from novel materials (Weir and Kacelnik 2006). Since the materials in question were perceptually different from materials that Betty had previously used, it would seem that Betty’s behavior was not stimulus bound. Furthermore, since Betty was developing novel methods for making hook tools, she was able to respond flexibly to the novel materials.
Dretske’s notion of informational systems is silent about whether the system is a product of evolution (e.g., instincts), design (e.g., thermometers), association, or cognition. Ramsey (2013) clearly rules out genetic information from being cultural, and is open to associative learning as giving rise to culture, but he does not distinguish different kinds of culture. However, if we accept a Dretskean approach to information, and we accept that there is a difference between paradigmatic cognitive and associative systems, then we have grounds for distinguishing between cognitive and associative kinds of culture.
Social learning occurs when one learns through others rather than through direct experience (Gariépy et al. 2014). This can occur in many ways ranging from simple stimulus enhancement, e.g., the goslings’ learning to eat butterbur (mentioned above), to the explicit pedagogy that humans often use when teaching each other how to make or use something new (Csibra and Gergely 2011). In this section, I will consider social learning that relies on associative processes. Then I will consider why this kind of culture should be treated differently than other kinds.
Battesti et al. (2012) trained female fruit flies to lay their eggs on one of two possible egg-laying locations by lacing one of them with quinine, which fruit flies find aversive. Later the experimenters removed the quinine but found that these females would continue to prefer the same location, even though both sites lacked quinine. Next, they used these conditioned female fruit flies as “demonstrators” for naïve female fruit flies. The naïve fruit flies copied the preferences of the demonstrators. It would seem that the demonstrators’ preference for certain sites “enhanced” those sites, which led to the formation of a preference in the naïve fruit flies.
Battesti et al.’s experiment clearly shows that fruit flies are capable of socially transmitting information, via stimulus enhancement, about preferred nest sites. While it is unlikely that the observed social behavior of fruit flies would be stable in the wild, Battesti et al. demonstrated that it is possible to produce an environment that could facilitate the development and persistence of culture in fruit flies. In other words, in the right environment, animals capable of only associative social learning could possess culture.
Some might object that the account above is highly artificial and that animals that rely primarily on associative learning would not produce cultural traditions in their natural environments. While it is true that the case of the fruit fly culture is highly artificial, there is nothing in principle that should prevent organisms whose learning is only associative from possessing culture.
For a more ecologically valid example, consider French grunts (a species of fish). French grunts learn where to rest in coral reefs by observing others. This learning is presumably facilitated by local and stimulus enhancement. The result of this learning is that certain populations prefer certain resting grounds, and this preference is intergenerational (Brown and Laland 2003). Another species of fish, the blue-headed wrasse, learns where to mate from group members and prefers such mating sites for generations (Bshary et al. 2001). In both cases, we have evidence of information being transferred behaviorally where this transfer produces a lasting change in the behavioral trait – French grunts and blue-headed wrasse have culture.
Learned associations do not explain all learned behaviors. Some animals produce flexible behaviors that require complex cognition. For example, some animals are able to form and retrieve mental representations or concepts that they use in higher cognitive capacities, such as categorization and inference. Of course, having higher cognitive capacities is not sufficient for having culture. Many complex cognitive capacities serve only individual goals. Nor is having complex cognition and culture sufficient for having cognitive culture; animals with complex cognition may only have associative cultures.
Like associative cultures, cognitive cultures may be formed in a variety of ways. Some animals may transmit culture via imitation; some may share cultural concepts that cause the members of a community to categorize and interact with their surroundings in similar ways. I will consider only one case of cognitive cultures in animals: cultural concepts in chimpanzees. I will begin by first describing cultural concepts in humans, which I take to be uncontroversially cognitive in nature. Then I will draw on studies of wild chimpanzee communities and argue that their behavior is best explained by positing that the chimpanzees have cultural concepts.
Though psychological and philosophical accounts of concepts sometimes diverge, I will adopt an explicitly psychological notion of concepts: concepts are bodies of knowledge stored in long-term memory that underlie our cognitive capacities (Machery 2009). On this view, concepts come in a variety of formats, e.g., prototypes, exemplars, theories, and ideals. The concepts that an organism has enable it to categorize objects and relations, and to make inferences about them.
Individuals may conceptualize the same objects in different ways. This will depend on how they interact and think about the object in question. If one grows up in North America, the kinds of birds that one is likely to see regularly will be different than the kinds of birds that a person living in Central America might experience. Accordingly, we might expect that what individuals from Central America consider to be a typical bird will differ from the birds North Americans consider typical. In this type of case, the populations’ having different concepts is explained by ecological factors and perhaps cultural influences.
But not all differences in concepts can be explained by appeals to ecological differences. Consider the case of expert fishermen in Wisconsin. Expert fishermen from the Menominee tribe in Wisconsin categorize fish according to their ecological relations. This differs from the way that expert European-American fishermen living in the same regions categorize fish. For them, what matters are taxonomic and morphological similarities (Medin et al. 2006). The fishermen are using the same waters and are experiencing the same species of fish. However, the different cultures place different values on fish, which results in different ways of interacting with the various fish species. Accordingly, members of the different communities form different cultural concepts – concepts that are widely shared across a community and whose content depends partly on cultural influences (Ross and Tidwell 2010).
Most psychological studies of animal concepts only consider whether animals have concepts and, if so, what conceptual abilities go along with them. For example, some researchers consider whether animals form concepts of objects in their environment (Tanaka 2006) or whether animals form abstract concepts, such as same/different concepts (Wright and Katz 2006). Other studies investigate what animals can do with their concepts, e.g., whether animals can engage in various forms of inference (for a review of the conceptual abilities of animals, see Zentall et al. 2008). Few studies consider the concepts of wild animals, and fewer are interested in whether the concepts that animals have are cultural. Perhaps the studies most suggestive of cultural concepts in animals are from Gruber and his colleagues (Gruber et al. 2009; Gruber et al. 2011; Gruber et al. 2012), so let us turn to examine that research in some detail.
In the Budongo forest, there is a community of chimpanzees known as Sonso chimpanzees. The Sonso community is notable because, unlike many chimpanzee communities, the Sonso chimps do not use tools to procure food. The sole exception is the leaf “sponges”, which all wild chimpanzees use. About 180 km away, a different community, the Kanyawara chimpanzees, regularly uses sticks to procure food. Gruber and his colleagues sought to determine if the Sonso chimps would use sticks as tools given the opportunity to do so, and whether the Kanyawara would similarly use sticks given the same task.
Gruber and his colleagues devised a honey retrieval task in which chimpanzees could procure honey from a hole in a log that was lying horizontally on the ground. In the first condition, it was possible for the chimpanzees to retrieve the honey using only their hands; in a second condition, the only way the chimpanzees could retrieve the honey was by using a stick. In the first condition, 2 out of 13 Sonso chimps used leaf sponges to acquire the honey; the rest used their hands. Four Sonso chimps also used leaf “sponges” in the second condition, but only one of them successfully retrieved the honey. Kanyawara chimps tended to use sticks in both conditions: 6 out of 10 in the first condition and 11 out of 12 in the second. Gruber et al. concluded that the differences in the chimps’ behavior were due to their cultural knowledge (Gruber et al. 2009).
In a follow-up experiment (Gruber et al. 2011), the second condition was repeated, but this time the condition was modified: a stick with leaves removed from half of it was placed near the hole. The Sonso chimps ignored the stick. Some of the Kanyawara chimps used the stick, while others used sticks from the surrounding environment. In a second condition, with Sonso chimps only, a branch with leaves stripped from half of it was inserted into the hole with honey. Some of the Sonso chimps removed the branch and used the leaves from it to make a sponge; others just removed the branch and tried to obtain honey using their fingers, and others removed the branch and attempted to retrieve the honey using leaf sponges. Some of the chimps smelled the honey on the stick after removing it; four of them consumed the honey on the stick, but none of them tried to use it to procure more honey.
Do the Kanyawara chimpanzees have concepts of their “stick tools”? Experimental studies show that chimpanzees regularly form categories of common objects (including plants) in their surroundings. What’s more, these categories are not best explained by stimulus generalization. Tanaka (2006) found that chimpanzees easily spontaneously categorize flowers, weeds, and trees from their surroundings, and that these categories include items that are perceptually dissimilar, e.g., dandelions and camellias.
Besides forming categories of perceptually dissimilar items, chimpanzees are also able to categorize objects based on thematic relations and functions, though it is difficult for them to do so (Tanaka 2006; Hopper et al. 2015). However, Hopper et al. (2015) found that chimpanzees who observe conspecifics using an object will readily learn the functional properties of that object. In their study, Hopper et al. provided chimpanzees with a polycarbonate rod. The rod can be utilized to retrieve a reward via a “poke” technique or a “lift” technique. The “poke” technique can be learned individually, but the chimpanzees in Hopper et al.’s study had not previously employed the lift technique. Accordingly, Hopper et al. set up their apparatus so that the only way for a chimpanzee to retrieve a reward was by utilizing the “lift” technique. Hopper et al. found that none of their chimpanzees were able to learn a “lift” technique through individual learning. However, 15 out of 18 chimpanzees quickly learned the technique after witnessing a human model or a conspecific successfully use the technique. This suggests that chimpanzees are not particularly good at seeing the functional properties of an object unless they have seen a demonstrator exploiting those properties. It is therefore not surprising that the Sonso chimpanzees do not see that a stick could be used as a tool. We might also expect that if they did see a conspecific using a stick as a tool, the behavior would spread across the community.
Given the conceptual abilities of chimpanzees, it is likely that both the Sonso chimps and Kanyawara chimps have some kind of concept of sticks. However, the Kanyawara’s concept includes knowledge about the functional properties of sticks that make them useful as tools. Given the fact that chimpanzees do not readily learn the functional properties of an object without first witnessing a conspecific using the object, it is unlikely that they would form such concepts individually. Thus, their concept is cultural in the sense that some of the content of the concept exists because of cultural transmission, and this information is common to most Kanyawara community members’ “stick” concept. The Sonso chimpanzees, in contrast, seem to lack a cultural concept of stick as tool, though it is possible that they have some more basic (and non-cultural) concept “stick”.
So far we have seen how culture can arise from both association and cognition. Both kinds of culture are significant. Having a culture affects how individuals interact with their environment and with each other. However, just as cognition gives rise to more flexible behaviors, cognitive cultures also give rise to more flexible cultural behavior. Having cultural knowledge of the functional properties of sticks enables Kanyawara chimpanzees to use sticks in a variety of feeding situations and not just the ones with which they are familiar. French grunts have a cultural preference for certain resting sites, but because they (presumably) lack a concept that contains knowledge about what makes a good resting site, they are only able to respond to the presence of a preferred site (which may not be the best option for nesting).
The distinction is not just important for understanding the differences between kinds of cultures, it is also important for how we conceptualize and discuss culture in general. Much of the interest in animal culture has been on the very question of whether animals have it. One problem with asking the question this way is that researchers have been searching for a single thing “culture” that might be common to both animals and humans. I suspect that part of the reason some researchers recoil at the idea of fish and insects having culture is because they believe that the minds of humans and the minds of fish and insects are too different to share anything as rich as culture. Once we distinguish between associative and cognitive cultures, we see that the claim that certain species have culture is not always the same as claiming that those species have the same kind of thing that humans have. This will depend on what kind(s) of culture we think the species in question has.
Distinguishing between associative and cognitive culture also opens up new avenues of research. We typically assume that human culture is cognitive in nature, but it is possible, perhaps likely, that some culture in humans is associative. For example, Behrens and his colleagues have found that the learning of social value in humans is at least some times associative (Behrens et al. 2008). If this learning of social value leads to culture, then we would have good reason for thinking that human culture is sometimes associative.
Distinguishing between kinds of cultures will obviously influence debates about whether human culture and animal culture are homologous or merely analogous (Tomasello 2016). The answer may turn out to be affirmative on both counts. It may turn out that some associative culture in humans (if there is any) is homologous to associative cultures in other taxa; it may also turn out that some cognitive culture in humans is homologous to cognitive cultures in other animals; and it may also turn out that there are some instances of culture in humans that are genuinely unique in that they rely on processes that only exist in humans. If the latter is the case, then there may be examples of culture in animals that are merely analogous to certain examples of culture in humans.
Once we recognize that culture comes in a variety of kinds, we can begin to see the various ways in which cultures can arise, recognize that variety in our own species and others, and better appreciate the continuities and discontinuities that exist between different species.
N. Emery, N. Clayton, and C. Frith’s (eds.) Social Intelligence: From Brain to Culture (Oxford: Oxford University Press, 2007) contains many excellent papers on social cognition and culture in animals. For more on how human social cognition and culture may be different, see M. Tomasello’s A Natural History of Human Thinking (Cambridge, MA: Harvard University Press, 2014).
Battesti, M., Moreno, C., Joly, D., and Mery, F. (2012). “Spread of Social Information and Dynamics of Social Transmission within Drosophila Groups”. Current Biology 22: 309–313.
Behrens, T. E. J., Hunt, L. T., Woolrich, M. W., and Rushworth, M. F. S. (2008). “Associative learning of social value”. Nature 456: 245–249.
Brown, C., and Laland, K. N. (2003). “Social learning in fishes: a review”. Fish and Fisheries 4: 280–288.
Bshary, R., Wickler, W., and Fricke, H. (2001). “Fish cognition: A primate’s eye view”. Animal Cognition 5: 1–13.
Buckner, C. (2013). “A property cluster theory of cognition”. Philosophical Psychology 28: 307–336.
——— (2017). “Understanding Associative and Cognitive Explanations in Comparative Psychology”. In: Andrews, K., and Beck, J. (eds.) Routledge Handbook of Philosophy of Animal Minds. New York: Routledge.
Csibra, G., and Gergely, G. (2011). “Natural pedagogy as evolutionary adaptation”. Philosophical Transactions of the Royal Society of London B: Biological Sciences 366: 1149–1157.
Dretske, F. (1980). “The intentionality of cognitive states”. Midwest Studies in Philosophy 5: 281–294.
———. (1993). “The nature of thought”. Philosophical Studies: An International Journal for Philosophy in the Analytic Tradition 70: 185–189.
Fritz, J., Bisenberger, A., and Kotrschal, K. (2000). “Stimulus enhancement in greylag geese: Socially mediated learning of an operant task”. Animal Behaviour 59: 1119–1125.
Galef, B. G. (1992). “The question of animal culture”. Human Nature 3: 157–178.
Gariépy, J.-F., Watson, K. K., Du, E., Xie, D. L., Erb, J., Amasino, D., and Platt, M. L. (2014). “Social learning in humans and other animals”. Frontiers in Neuroscience 8: 1–13.
Gruber, T., Muller, M. N., Reynolds, V., Wrangham, R., and Zuberbühler, K. (2011). “Community-specific evaluation of tool affordances in wild chimpanzees”. Scientific Reports 1: 128. DOI: 10.1038/srep00128.
Gruber, T., Muller, M. N., Strimling, P., Wrangham, R., and Zuberbühler, K. (2009). “Wild chimpanzees rely on cultural knowledge to solve an experimental honey acquisition task”. Current Biology 19: 1806–1810.
Gruber, T., Singleton, I., and van Schaik, C. P. (2012). “Sumatran orangutans differ in their cultural knowledge but not their cognitive abilities”. Current Biology 22: 2231–2235.
Heyes, C. (2012). “What’s social about social learning?”. Journal of Comparative Psychology 126: 193–202.
Hopper, L. M., Lambeth, S. P., Schapiro, S. J., and Whiten, A. (2015). “The importance of witnessed agency in chimpanzee social learning of tool use”. Behavioural Processes 112: 120–129.
Laland, K. N., and Hoppitt, W. (2003). “Do animals have culture?”. Evolutionary Anthropology: Issues, News, and Reviews 12: 150–159.
Machery, E. (2009). Doing Without Concepts. New York: Oxford University Press.
Medin, D. L., Ross, N. O., Atran, S., Cox, D., Coley, J., Proffitt, J. B., and Blok, S. (2006). “Folkbiology of freshwater fish”. Cognition 99: 237–273.
Penn, D. C., and Povinelli, D. J. (2007). “Causal cognition in human and nonhuman animals: A comparative, critical review”. Annual Review of Psychology 58: 97–118.
Ramsey, G. (2013). “Culture in humans and other animals”. Biology & Philosophy 28: 457–479.
——— (2017). “What is animal culture”. In: Andrews, K., and Beck, J. (eds.) Routledge Handbook of Philosophy of Animal Minds. New York: Routledge.
Ross, N., and Tidwell, M. (2010). “Concepts and culture”. In: Mareschal, D., Quinn, P. C., and Lea, S. E. G. (eds), The Making of Human Concepts. New York: Oxford University Press, pp. 133–148.
Tanaka, M. (2006). “Spontaneous categorization of natural objects in chimpanzees”. In: Matsuzawa, T., Tomonaga, M., and Tanaka, M. (eds), Cognitive Development in Chimpanzees. Tokyo: Springer.
Tomasello, M. (2016). “The ontogeny of cultural learning”. Current Opinion in Psychology 8: 1–4.
Weir, A. A., and Kacelnik, A. (2006). “A New Caledonian crow (Corvus moneduloides) creatively re-designs tools by bending or unbending aluminum strips”. Animal Cognition 9: 317–334.
Whiten, A., and van Schaik, C. P. (2007). “The evolution of animal ‘cultures’ and social intelligence”. Philosophical Transactions of the Royal Society of London B: Biological Sciences 362: 603–620.
Wright, A. A., and Katz, J. S. (2006). “Mechanisms of same/different concept learning in primates and avians”. Behavioral Processes 72: 234–254.
Zentall, T. R., Wasserman, E. A., Lazareva, O. F., and Thompson, R. K. R. (2008). “Concept learning in animals”. Comparative Cognition and Behavior Reviews 3: 13–45.