Culture among animals is most likely more widespread and pervasive than commonly thought and an important avenue to local adaptation; we most likely built upon a very broad, pre-existing cultural capacity

Animal cultures: how we've only seen the tip of the iceberg. Caroline Schuppli and Carel P. van Schaik. Evolutionary Human Sciences, Volume 1 2019, e2, May 9 2019. https://doi.org/10.1017/ehs.2019.1

Abstract: For humans we implicitly assume that the way we do things is the product of social learning and thus cultural. For animals, this conclusion requires proof. Here, we first review the most commonly used procedure for documenting animal culture: the method of exclusion, which charts geographic behavioral variation between populations as evidence for culture. Using published data, we show that, whereas it is an adequate proof of principle, the method of exclusion has major deficiencies when capturing cultural diversity and complexity. Therefore, we propose a new method, namely the direct counting of socially learned skills, which we apply to previously collected data on wild orangutans. This method reveals a far greater cultural repertoire among orangutans, and a different distribution of cultural elements among behavioral domains than found by the method of exclusion, as well as clear ecological correlates for most cultural elements. The widespread occurrence of social learning ability throughout the animal kingdom suggests that these conclusions also apply to many other species. Culture is most likely more widespread and pervasive than commonly thought and an important avenue to local adaptation. The complex and normative dimensions of culture seem unique to our species, but were most likely built upon a very broad, pre-existing cultural capacity that we inherited from our ancestors.

Discussion

The base of the great ape culture iceberg

The orangutan example suggests that by relying on the MoE to assess cultural repertoires we have so far only discovered the tip of the great ape culture iceberg (i.e. C ₁ >> C_ME; Figure 4). The MoE produces a biased sample of highly complex and conspicuous behaviors and dismisses a vast array of socially learned behaviors that covary with ecological factors. By counting socially learned skills, however, we are beginning to get to know the base of this iceberg. Cultural repertoires are mainly composed of basic, low-complexity subsistence skills, most of which show clear ecological correlates (e.g. knowledge of diet composition and processing techniques). Thus, a lot of (but not all) cultural variation may indeed be ecologically induced (C _Ecol is a major part of C ₁ and C _Var).

At the same time, a systematic reliance on social learning under similar ecological conditions may very well lead to many universal cultural behavior patterns across populations. The most striking example in the orangutans for this is nest building: even though it is an orangutan universal, it takes young orangutans years of close observation and subsequent practice before they can build nests good enough to spend the night in (Schuppli et al., 2016a), and socially deprived young apes will never be able to do so (Bernstein, 1962; Videan, 2006). The basic construction of nests (a rim made of intertwined long branches) is highly comparable across different orangutan populations, presumably because it is the most latent solution to the problem (Tennie et al., 2009; high C _U but low C _Ecol).

How much culture is there in other animals?

The points discussed above are unlikely to be true only for orangutans or great apes in general but most certainly apply to all species that rely on social learning. Although numerous species, including insects, fish, birds and mammals, are now known to be capable of social learning (reviewed by Galef and Laland, 2005; Rapaport and Brown, 2008; Reader and Biro, 2010; Whiten, 2017), for most, social learning has so far only been shown in captivity, which does not elucidate to what extent species indeed use this ability in the wild (Reader and Biro, 2010; Whiten and van de Waal, 2018). Even though behavioral scientists now increasingly acknowledge the role of social learning (van Schaik and Burkart, 2011; Tomasello, 1999; van Schaik et al., 2017), it is still widely treated as the rare and complex exception under the skill acquisition modes.

However, social learning can be quite simple given that many forms of social learning (e.g. enhancement or facilitation) do not require higher forms of cognition but nonetheless produce faithful behavioral copies owing to shared affordances. Furthermore, from the perspective of naïve immatures, a strong reliance on social learning is highly adaptive because social learning is less dangerous and more efficient than independent learning: it reduces the risk of getting injured or poisoned, increases learning speed by allowing the learning individual to benefit from what others have figured out before and increases the signal strength of relevant information (van Schaik and Burkart, 2011). Social learning thus allows for the fast acquisition of skills and the acquisition of more complex skills, and naïve individuals will benefit from choosing this option whenever they can. As such, we expect social learning to be most prominent in species with contact between generations, high social tolerance toward immatures, and an extended period of immaturity.

Over the last two decades it has become increasingly clear that social learning is indeed an important means of natural skill acquisition for many mammal and bird species, as evidenced in inherited dietary specializations, selective observations of skilled individuals, master apprentice interactions, effects of the presence of role models on foraging success or links between social networks and skill repertoires (Coelho et al., 2015; Estes et al., 2003; Griesser and Suzuki, 2016; Guinet and Bouvier, 1995; Hobaiter et al., 2014; Kitowski, 2009; Krutzen et al., 2005; Lonsdorf, 2006; Mann et al., 2007; Matsuzawa et al., 2001; Ottoni et al., 2005; Rapaport and Brown, 2008; Schuppli et al., 2016a). Direct observations of the spread of recently made innovations through social groups are bound to be rare but have been made in natural populations (Allen et al., 2013; Hobaiter et al., 2014; Kendal et al., 2010). Interspecific cross-fostering experiments, be they designed or accidental, although both quite rare, have impressively demonstrated the pervasiveness of social learning of life's skills (Rowley and Chapman, 1986; Sheppard et al., 2018; Slagsvold and Wiebe, 2007; Warner, 1988).

Culture is therefore likely to be pervasive in all species that pass on knowledge and skills socially. However, most of these species’ skills will show little or no geographic variation, except for the most complex skills, which are the least likely to be invented and retained. In several species, the acquisition of basic foraging skills was shown to be socially mediated: in aye-ayes (Daubentonia madagascariensis), for example, immatures learn tap-foraging – for which they even have morphological specializations – far less readily in the absence of adult role models (Krakauer, 2005).

Since social learning can be very simple, culture does not require a large brain and it is therefore unlikely to be a hallmark of cognitive complexity (Byrne et al., 2004; Laland and Hoppitt, 2003), although the efficiency of cultural transmission may also favor the evolution of greater investment in brains (van Schaik and Burkart, 2011).

Remaining challenges in the animal culture debate

Detecting animal culture irrespective of geographic variation is challenging and may not always be possible. Aside from peering, social learning can also happen via observation at longer distances, socially induced encounters with environmental features and acoustic transmission. Thus, in order to be able to draw conclusions about and compare cultural repertoires across species, it is crucial to find appropriate ways to detect social learning according to the species’ main transmission mode as well as to take different transmission modes into account. The SLS will thus most likely only rarely produce integral cultural repertoires. In most cases, however, it will be able to lift a significant part of the so far hidden base of the culture iceberg above the surface.

Implications for human culture

Most elements which we nowadays naturally call the product of human culture can be found across the globe and are thus human universals. In this time of increasing connectedness and global exchange even the most complex human innovations often quickly reach the status of universals and would not be recognized as socially learned innovations by their geographic distribution. Yet everyone would agree that these innovations are an important part of our cultural repertoire.

What differentiates animal from human culture is the lack of normativity, the virtual absence of cumulative culture and the enormous diversity of human cultural elements (Laland and Galef, 2009; Whiten, 2017; Whiten and van Schaik, 2007). These three features seem to remain a hallmark of human culture and seem to be linked to the evolution of our species’ skill-intensive, technology-dependent foraging niche (van Schaik et al., 2019; Laland, 2017). However, the unique human cultural constellation was built on a surprisingly broad and evolutionarily deep foundation.