Towards a prehistory of primates.

Haslam, Michael

Introduction

The social and technological traits of living non-human primates (henceforth 'primates') have contributed significantly to reconstructions of the activities of their past common ancestors with humans (van Schaik et al. 2003; Haslam et al. 2009; McGrew 2010; Silk 2011; Whiten 2011; Wynn et al. 2011). Customary tool-use by wild primates, a key trait of interest to archaeologists, has been recorded in tropical Africa, South America and Southeast Asia, including by chimpanzees (Figure 1), orangutans and bearded capuchin monkeys (McGrew 1992; van Schaik et al. 1996; Spagnoletti et al. 2011). Less well studied or less prevalent wild tool-use has also been noted among gorillas, bonobos, long-tailed macaques and both yellow-breasted and blonde capuchins (Hohmann & Fruth 2003; Breuer et al. 2005; Malaivijimond et al. 2007; Canale et al. 2009; Souto et al. 2011). Yet there is a great disparity in the observational time span for human and primate behaviour, because the archaeological record of hominins (human ancestors back to our split with the Pan lineage) has unusual chronological depth.

At present, hominin technical activities have been detected back ~3.4 million years (McPherron et al. 2010), with a well-studied and possibly continuous stone tool record since 2.6 million years ago (mya) (Semaw et al. 2003). This record is augmented by non-stone prehistoric technologies for tens, and in some cases hundreds, of thousands of years (e.g. Thieme 1997). In contrast, we have around half a century of systematic chimpanzee behavioural data, and even less for other primates, although anecdotal reports from West Africa extend back around 400 years (Sept & Brooks 1994). When extinct hominin behaviours are compared with those of living primates (e.g. Joulian 1996; Gowlett 2009; Pruetz & Bertolani 2009; Toth & Schick 2009; de la Torte 2010; Ungar & Sponheimer 2011), we need to ask whether extant primate behaviour is representative of the several million years of behavioural evolution that preceded it. In other words, when did apes, monkeys and other primates become 'behaviourally modern', and how would a more complete primate archaeological record change our perspective on human evolution?

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Behavioural modernity

Significant behavioural changes have occurred in the hominin lineage during the past few million years, and archaeologists studying Homo sapiens have concentrated on the issue of 'behavioural modernity' (Minugh-Purvis 1995; McBrearty & Brooks 2000; Wadley 2001; d'Errico 2003; Henshilwood & Marean 2003; Renfrew 2007; Conard 2008). At the core of this concept is a search for features that are unique to our species, an attempt to identify the process by which the habits and capacities of past humans came to be recognisably similar to those of humans living today (Klein 2000). While this may be a useful driver of debate (d'Errico & Stringer 2011; Shea 2011), the proposal of a radical behavioural shift, or 'human revolution' (Mellars & Stringer 1989; Bar-Yosef 2002) part way through hominin evolution is unusual when placed in a broader zoological context. There is, for example, no literature on the timing and character of the emergence of 'modern Macaca behaviour', or international conferences discussing a possible 'Papio behavioural revolution'.

From the mid twentieth century onwards, the combination of increasing numbers of hominin fossil discoveries and the establishment of long-term field primatology sites opened up new debates over the similarities between hominins and other African primates (e.g. Leakey 1961; Washburn & DeVore 1961; Holloway 1969; Jolly 1970; Foley 1987). Archaeologists explored the ways that the emerging primate literature could inform topics such as early Pleistocene site creation and social structure (Clark 1960; Isaac 1969), but it was modern, twentieth-century primates that were the point of comparison. Little or no attention was given to possible pre-Anthropocene (Steffen et al. 2011) primate behavioural characteristics, except those hypothesised for common human-chimpanzee ancestors (e.g. Parker & Gibson 1979).

The lack of comparative Pan fossils can promote the notion of a static phenotype for all chimpanzees, past and present. For example, whereas hominins are represented by a variety of species on charts of brain volume evolution, chimpanzees can only be represented by a modern value (e.g. Aiello & Dean 1990; Gamble et al. 2011). Yet a number of ancestral panins (the distinct bonobo-chimpanzee lineage) must have existed during their separate evolution over the past 5-7 million years (Kumar et al. 2005). The average time from speciation to extinction for large African mammal species is 2.33 million years (Vrba 2000), while Foley (1993) calculated that African terrestrial primates have a species longevity close to one million years. The one known panin speciation, splitting chimpanzees from bonobos, occurred in the Early Pleistocene (Stone et al. 2010; Wegmann & Excoffier 2010). We can therefore posit a minimum of two (and very likely more) extinct direct panin ancestor species since the split from hominins, with an unknown number of dead-end side branches and additional genera (Wood & Harrison 2011).

Cultural variation observed in living chimpanzees and orangutans (Whiten et al. 2001; van Schaik et al. 2003) suggests that we should not expect the primate archaeological record to be homogeneous in time or space, even when produced by a single species. Extant wild tool-using primates live in a wide range of habitats and have varied social systems (e.g. van Schaik et al. 1999; McGrew 2004; Mannu & Ottoni 2009; Gumert et al. 2011; Shumaker et al. 2011), factors that influence the transmission of technological activities (Biro et al. 2010). The capacity for cultural variation means that, depending on available materials, non-hominin primates likely experimented with a greater range of tool types than those seen today, including a range of non-stone tools (Panger et al. 2002; Byrne 2005; Haslam et al. 2009).

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A full treatment of these topics lies outside the scope of this review, and I therefore concentrate here on three broad and interlinked categories for which a long-term perspective is important for inter- and intra-species behavioural comparisons: geographic patterning, diet and innovation. These three categories also reflect key adaptive shifts in Pliocene hominin evolution (Potts 2007), and their investigation will assist in understanding the causes of hominin divergence from other primates. My focus is on the most intensively studied living close relative to humans, chimpanzees (Nishida et al. 2010), but the concepts are not naturally limited to any one primate (or even non-primate) species.

Towards a prehistory of primates

Geographic patterning

Modern chimpanzees are behaviourally flexible and occupy a wider variety of environments than most primate taxa, including lowland and montane forests, woodlands and drier grasslands or savannah. This adaptability suggests that the current geographic distribution of chimpanzees (Figure 2) is unlikely to directly reflect past distribution. We know that the chimpanzee range is currently shrinking (Butynski 2003), and a significant earlier shift is indicated by the finding of putative chimpanzee fossils in Kenya, ~600km east of the species' current range (McBrearty & Jablonski 2005). The question here is, how did past primate populations spread, split and contract, and how did this affect cultural variation?

Genetic analyses have begun to reveal the population structure and history of the four commonly recognised chimpanzee subspecies: the western (Pan troglodytes verus), Nigeria-Cameroon (P. t. ellioti), central (P. t. troglodytes) and eastern (P. t. schweinfurthii) populations (Goldberg 1998; Gagneux et al. 2001; Yu et al. 2003; Won & Hey 2005; Caswell et al. 2008; Hey 2010; Stone et al. 2010; Wegmann & Excoffier 2010; Bjork et al. 2011). These studies suggest that major rivers in Central Africa (in particular the Niger, Sanaga and Ubangi rivers) act as rarely permeated boundaries to the various subspecies ranges, in addition to isolating the bonobo (Pan paniscus) south of the Congo River (Gagneux et al. 2001; Bjork et al. 2011). Within these regions, the potential importance of Pleistocene refugia in promoting allopatric differentiation has been considered (Lehman & Fleagle 2006), but at least for eastern chimpanzees there is little correlation between posited forest refugia and present-day diversity (Goldberg 1998).

Pounding stone use has been included in the list of cultural traits charted in multi-site chimpanzee studies (Whiten et al. 1999, 2001). These studies recognise clear geographic variation, with wild chimpanzees from different study sites using different combinations of stone and wood hammers and anvils, or alternatively not using stones to crack nuts even when both are available. Explanations offered for this variation include the variety and hardness of available nut species (Boesch & Boesch 1990; McGrew et al. 1997) and limited spatial diffusion of nut-cracking knowledge between sites (McGrew 1992). However, causal mechanisms are difficult to infer over short time spans, and differentiating between cases in which primate cultural variants are absent because knowledge has been lost from a particular site or region, or absent because they were never invented by the resident groups (Wrangham 2006; Whiten et al. 2009), is very difficult without a referent chronological sequence. Experimental evidence from captive primates (e.g. Hayashi et al. 2005; Marshall-Pescini & Whiten 2008b) has limited ability to address this issue, and studies that seek to generalise findings from captive primate subjects may have to acknowledge the limited scope of those findings for understanding primate behaviour before the twentieth century (Boesch 2007; Leavens et al. 2010; Whiten 2011).

It would be particularly interesting to see if chimpanzee use of pounding stones has persisted throughout periods where shifting climates altered the available nut and fruit resources (Dupont et al. 2010), or whether such tool-use disappears and re-appears in tune with environmental changes. In this regard, it is important to note that chimpanzee pounding stone use is currently localised to west Africa (and P. t. verus), which may limit the archaeological study of such traditions and their correlates to this part of the modern chimpanzee range, although recent anecdotal evidence for stone tool-using Nigeria-Cameroon chimpanzees (Morgan & Abwe 2006) suggests that this behaviour might be more widespread. Nonetheless, as a starting point we can hypothesise that stone tool-use as a behaviourally modern trait in Pan is limited by the time of genetic divergence (as a proxy for physical separation) of the western chimpanzees from the central-eastern clade. Present consensus places this process ~1-0.5mya (Becquet et al. 2007; Caswell et al. 2008; Stone et al. 2010; Wegmann & Excoffier 2010), and more likely towards the younger end of that spectrum. Viewed as a specific West African innovation, and not as a remnant behaviour of the hominin-panin last common ancestor, the most plausible hypothesis is that chimpanzee stone tool-use began some time closely prior to 500 000 years ago. While tool-use traits do not always align with genetic divisions in chimpanzees (Lycett et al. 2010), stone tool-use currently does, and excavation of the African primate archaeological record is the only way to test this hypothesis.

Emerging genetic data for the capuchin monkeys of Central and South America (Lynch Alfaro et al. 2011) similarly provide targets for future archaeological investigation. The capuchin Cebus genus has recently been reclassified into two genera (the gracile Cebus and the more robust Sapajus), the result of a late Miocene split potentially related to the establishment of the Amazon River (Hoorn et al. 2010). Use of pounding stones to open palm nuts in the wild is currently only known among Sapajus (Figure 3), in the drier cerrado (grassland to scrub woodland) and caatinga (dry forest and thorn scrub) environments that separate the Brazilian Atlantic and Amazon forests (Moura & Lee 2004; Visalberghi et al. 2007; Canale et al. 2009). Sapajus began to diversify from an origin zone somewhere in the Atlantic Forest around 3-2.5mya, before expanding west into the drier habitats, a movement postulated to have occurred around 0.7mya (Casado et al. 2010; Lynch Alfaro et al. 2011). As forest dwelling capuchins have not been observed to use stone tools, the genetic data therefore provide an initial prospective date for the origins of lithic technology among the capuchins, with the intriguing possibility that it was this specific technological innovation that permitted their dispersal into the previously uninhabited areas. The data further suggest that the north-western members of these dispersing groups subsequently moved into the Amazon rainforest (already occupied by Cebus) after 0.4mya (Lynch Alfaro et al. 2011). We can only speculate at present, but the absence of stone pounding tools among modern Amazonian Sapajus populations may well result from loss of a technological adaptation that was strongly tied to the palm nuts found in the cerrado and caatinga. In this scenario, testable through archaeological exploration, the lithic technologies of both 'behaviourally modern' capuchins and chimpanzees therefore have a Middle Pleistocene origin.

Beyond genetic reconstructions, the recovery of stone (or other) tools used by primates is strong proxy evidence of the presence of those primates at a given time and place. Fortunately, chimpanzees and capuchins transport and accumulate stone materials (Boesch & Boesch 1984; Visalberghi et al. 2007; Canale et al. 2009; Carvalho et al. 2009; Spagnoletti et al. 2011), creating recognisable sites and constructing technological niches that may structure subsequent activity (Figure 3). Redundant patterning has also been documented for chimpanzee nesting sites (Sept 1998; Hernandez-Aguilar 2009), further concentrating group behaviour.

The archaeological study of chimpanzee activity areas is currently in its infancy (Mercader et al. 2002; Carvalho et al. 2008), and a primary difficulty is in distinguishing primate tools from naturally occurring stones, or from hominin behavioural debris. Primate preference for stones of particular density, size and material assist in their discernment (although this approach is less useful once outside the range of preferences seen among living primates), as can the careful documentation of characteristic wear patterns and adhering residues (Mercader et al. 2007). In the Americas, the task is aided by the absence of hominins prior to the terminal Pleistocene (Goebel et al. 2008), meaning that stone pounding tools dated prior to this time may in theory be attributed to non-human primates.

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Diet

Chimpanzees have a mixed and variable diet, including fruits, herbaceous vegetation, insects, vertebrates and secondary products such as honey (e.g. McGrew et al. 1988; Milton 1999; McGrew 2001; Tweheyo et al. 2004; Laden & Wrangham 2005; Sanz & Morgan 2009). Ideally, the recovery of archaeological evidence for past chimpanzee behaviour would allow us to assess the representativeness of modern primate diets, compared to their ancestors throughout the past few million years. As discussed earlier, the adaptability of chimpanzees to a variety of conditions and ability to range across wide areas may act as a buffer to local climate-driven changes in resources; however, it is reasonable to hypothesise that some of the now extinct panin species were more specialised and/or localised than living populations, based on the variation known from the hominin lineage (e.g. the hyper-robust Paranthropus, or the island dwelling Homo floresiensis) and the orangutan lineage (Ungar & Sponheimer 2011; Wood & Harrison 2011). At its simplest, the question that arises is to what extent the range of potential chimpanzee dietary niches were actually exploited by past panin species.

Fortunately, tool-use is pervasive in chimpanzee dietary foraging (McGrew 1992), particularly in the extraction of embedded nutrient rich resources such as nuts, termites, underground storage organs (USOs) and honey (e.g. Boesch & Boesch-Achermann 2000; Deblauwe et al. 2006; Hernandez-Aguilar et al. 2007; Sanz & Morgan 2009). The spearing tools used by Fongoli chimpanzees to disable small prey hidden in tree holes (Pruetz & Bertolani 2007) could similarly be seen as targeting 'embedded' food. Tool-use allows us to record diet-related activities beyond direct observation for primates that are either unhabituated (Sanz et al. 2004; Fowler & Sommer 2007; Canale et al. 2009; Koops et al. 2010) or even deceased (Mercader et al. 2002). Most of the tools manufactured and used by chimpanzees are made of plant materials, which will survive in the short-term (perhaps decades in the case of nests made by modifying living trees; Stewart et al. 2011), but are unlikely to enter the long-term archaeological record other than through fortuitous discard in a waterlogged or hyper-arid setting. Nonetheless, standardisation of the size and physical characteristics of many of these tools (McGrew 2004; Boesch et al. 2009; Sanz et al. 2009) means that they are both recognisable when encountered, and encode information about the traditions and dietary habits of the group that created them.

Even more promising for studying long-term changes in diet is the use of stone and hard wood pounding tools for opening nuts and other food items, as practised by chimpanzees, capuchin monkeys and long-tailed macaques (Boesch & Boesch 1990; Ottoni & Izar 2008; Canale et al. 2009; Carvalho et al. 2009; Gumert et al. 2009). The use of anvil stones has been presented as a plausible mechanism for the initial stage leading to deliberate stone tool fracture among hominins (Marchant & McGrew 2005), and if this is the case then it is worth exploring the reasons why present-day chimpanzees have not followed a similar path to stone tool manufacture. Stone tools used by chimpanzees have a demonstrated antiquity of over 4000 years in the Tai Forest of Cote d'Ivoire (Mercader et al. 2007), and there is no reason to suspect that the stone tool record left by past primates in Africa, Asia and South America is not still present and awaiting study by archaeologists and primatologists.

As pounding tools are currently recognised as primarily a dietary adaptation, then at a minimum the antiquity of embedded food exploitation can be investigated through systematic excavation and analysis of these artefacts. However, there are also more complex diet-related questions that may be addressed through the analysis of stone artefacts used by chimpanzees and other primates. For example, the relationship between the physical character (shape, size and density) of selected stone tools and the food types exploited with them deserves greater attention. Chimpanzees and capuchins choose stone tools based on their performance characteristics and fitness for the task at hand (Boesch & Boesch 1982; Visalberghi et al. 2009), an ability we may reasonably expect panin ancestors to also have possessed. Along with microscopic residues adhering to used tools (Mercader et al. 2007; Haslam et al. 2010), the search for correlations of form and function would allow assessment of the composition, size and hardness of the foods targeted by past primates. With added chronological resolution, such assessments will permit the reconstruction of a behavioural component to primate diet evolution, which can then be further refined through concurrent environmental reconstruction of artefact find spots and consideration of dental morphologies and wear (Ungar 1998).

The exploitation of embedded foods provides a nutritional advantage to tool-using primates (Wrangham 2006). While it is rarely considered that either a chimpanzee direct ancestor or a side branch of the panin lineage may have developed radically different or perhaps even more complex technology than extant individuals, the selective impetus is there, in the form of nutrient and calorie-rich nuts, as well as in underground starchy foods (Hernandez-Aguilar et al. 2007). Each primate lineage has had millions of years in which to discover, spread, lose and re-discover the benefits of technology, and it is unlikely that the forms of stone tool-use observed among living primates are the only ones ever to have evolved. The increased energetic returns gained by accessing embedded resources is a plausible reason to hypothesise that tool-use traditions at least equivalent in complexity to modern behaviour may have been repeatedly discovered by past primate, and hominin, populations.

Innovation

Cumulative cultural change plays a key role in behavioural studies attempting to differentiate primate and human learning processes (Marshall-Pescini & Whiten 2008a), with investigation into mechanisms such as imitation and emulation (Tennie et al. 2009). Studies of human behavioural modernity have turned in recent years to the impact of demography on permitting and sustaining behavioural innovations and patterns (Shennan 2001; Powell et al. 2009; Richerson et al. 2009). Chimpanzee research has also begun to explore these connections (Mitani 2006; Lycett et al. 2009), with a correlation shown between larger female group sizes and the number of habitual and customary cultural traits in several wild chimpanzee communities (Lind & Lindenfors 2010). This again raises the possibility that chimpanzee groups affected by recent human activities may not be behaviourally representative of past panins.

The same genetic studies that seek to identify past chimpanzee population expansions and contractions (e.g. Won & Hey 2005; Caswell et al. 2008) also provide spatio-temporal targets for investigating the occurrence of periods of more and less rapid cultural innovation. Mitochondrial studies that reconstruct female population size trends may be of special interest in this regard, if females were a primary vector for cultural transmission in the past (Lycett et al. 2010). Unfortunately, genetic studies do not provide precise information on the timing of past bottlenecks and expansions, with date estimates varying widely depending on the model and calibration points used (Stone et al. 2010). However, archaeological evidence for origins and changes in primate cultural traditions could assist in narrowing the error margins of genetic studies, as it has done for calibrations of the human mitochondrial 'clock' (Soares et al. 2009).

Each of the chimpanzee subspecies may have been genetically distinct for longer than H. sapiens has existed as a species (Wegmann & Excoffier 2010; but see Gonder et al. 2011), which leaves a significant amount of time over which any cumulative effects of cultural innovation may have operated among the panins. Analysis of material culture left by primate populations that were larger and better connected than those of today would provide a much needed comparison to short-term laboratory-based studies that suggest chimpanzees do not accumulate modifications (Tennie et al. 2009). In particular, the long-term perspective provided by archaeology allows for assessment of whether panin accumulative processes operate on a slower scale than has been observable in the few decades of chimpanzee research.

Genetic data show that Central African chimpanzee populations have the largest current effective population size, and that unlike the western and eastern subspecies they did not go through a substantial population bottleneck in the Pleistocene (Wegmann & Excoffier 2010). The strong bottleneck effects seen for the western and eastern populations, as well as for the bonobos, might suggest that central populations are the ones to look to for cultural continuities and accumulation over the past few million years (Sanz & Morgan 2010). However, P. t. troglodytes have received less intensive field study than the western and eastern populations; for the 19 (out of 39) cultural variants identified by Whiten et al. (2001) that involve tool-use, 11 have insufficient data for assessing their presence among one or both of the Central African Goualougo and Lope communities (Lycett et al. 2010). It is therefore not possible on present evidence to identify whether the presence of larger populations over longer time periods has had an impact on the innovation and cultural retention rates of modern chimpanzees. Nevertheless, a reasonable prediction based on demography would be that cultural innovation rates were consistently highest among past Central African panins, with cultural founder effects active among the diverging western and then eastern chimpanzee subspecies from around 500 000 years ago.

Discussion: a primate archaeological perspective

The three aspects of primate behaviour considered briefly here, diet, geographic variation and innovation, were chosen to point up the benefits of bringing an archaeological approach to primatology (Haslam et al. 2009). This approach improves our understanding of primate behavioural evolution in its own right, complementing studies of psychological and manual skills (e.g. Byrne 2005), in addition to generating comparative data for the study of human evolution. The reviewed topics are not mutually exclusive, since geographical expansions may stimulate or derive from innovations, and new innovations that relate to diet may be preferentially taken up by other individuals and groups (Nishida et al. 2009). It is also important to remember that, even among humans, seemingly adaptive behaviours can be lost (Henrich 2004). Without knowing just how chequered the temporal pattern of cultural variation may be (Wrangham 2006), we should not automatically regard living tool-using primates (or indeed any cultural species) as representative of their entire ancestral lineages. For example, based on emerging genetic data, I have hypothesised that stone tool-use observed in Brazilian capuchin monkeys may be no more than 700 000 years old, and the same behaviour among West African chimpanzees perhaps little more than 500 000 years old. But across these taxa (and others) there may have been numerous instances of technological discovery, loss and re-discovery over that time period, dependent on demography and the availability of suitable tools and dietary targets. Now that the conceptual constraint of a lone Homo-Pan stone tool-using clade is abandoned, a key task is to examine the independent technological trajectory of each tool-using group.

The idea of cross-referencing hominin and primate activities is not new in archaeology, but directly investigating the activities of past primates does involve a shift away from humans and our ancestors as the sole focus of prehistoric study. In practice, the methods required differ little from those used in Palaeolithic archaeology. Surveys are necessary to determine the prevalence and distribution of tool materials, and their geographical intersection with habitats suitable for resources such as palm nuts and social insects, regardless of whether these are currently used by extant primates. The Brazilian cerrado and caatinga zones certainly hold promise in this regard, as does the Dahomey Gap savannah that separates the Upper and Lower Guinea rainforests (Mayr & O'Hara 1986) (Figure 2). Forest expansion in the latter area is linked to an increase in the pioneer oil palm Elaeis guineensis (Salzmann & Hoelzmann 2005), favoured for nut-cracking and pestle-pounding by the extant Bossou chimpanzees of Guinea (Sugiyama 1994).

Excavations are needed both within and outside the current range of tool-using primate species, especially in areas where environmental reconstructions indicate the previous existence of suitable habitats (e.g. Dupont et al. 2010). Information on changes to major river systems, as barriers to both gene and information flow, may assist in setting temporal limits to cultural processes. Initial dating programs also need to target durable, culturally relevant materials such as broken nut shells. Use-wear and residue analyses will continue to be valuable in distinguishing primate tools from natural objects, including use-wear on concentrations of broken stone debris that may reveal tool re-use behaviours akin to the early stages of hominin stone knapping. Key plant residues include starches found in nuts and USOs, the lipids and resins found in these same sources, and fragments of nut shells and structural tissue pounded into tool surfaces. Animal residues may include hair (such as the bushbaby hair found adhering to a chimpanzee spear in Senegal: Pruetz & Bertolani 2007), termite and ant parts, fats and marrow (Boesch & Boesch 1989), blood and by-products such as honey (Boesch et al. 2009; Sanz & Morgan 2009).

Realistically, the initial age estimates provided in this review for the origins of extant primate stone tool-use will require revision. These estimates are partly based on genetic dates, which have wide error margins, and in any case population genetic divergence cannot by default be assumed to correlate with material culture changes in any animal (including hominins). Finally, we should remember that hominins have filled the niche of cognitively advanced, large bodied, tool-using primate for the past few million years, which probably had a negative impact on the evolution of similar roles among our close relatives. Debatably, this impact may have included intermittent hominin occupation of African forests from the Middle Pleistocene onwards (Mercader 2002). It is possible that we and our ancestors are the reason modern chimpanzees display limited rates of cultural evolution, and it is likely that the survival of extant primate species in Africa is to some extent a function of their ability to co-exist with hominins (Jablonski 2002). Outside Africa, the Asian macaques also have a long shared history with Homo, while in the Americas a lack of Pleistocene hominins may have permitted greater primate technological experimentation. Our ability to address issues such as these will strongly benefit from an archaeological approach, and an ability to see beyond behaviourally modern primates will offer new perspectives on both the relevance of primatological referents to human evolution, and on the variability and time depth of non-human primate behaviour.

Acknowledgements

I am grateful to Dora Biro, Bill McGrew, Susana Carvalho, Elisabetta Visalberghi, Dorothy Fragaszy and three anonymous reviewers for discussions and helpful comments on earlier drafts. I would also like to thank all the researchers working on the evolution of primate technology, on whose insightful work this review draws. The author received funding from a UK Arts and Humanities Research Council Early Career Fellowship, and European Research Council Starting Grant No. 283959 (PRIMARCH).

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Received: 6 May 2011; Accepted: 6 October 2011; Revised: 8 December 2011

Michael Haslam, Research Laboratory for Archaeology and the History of Art, University of Oxford, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK (Email: michael.haslam@rlaha.ox.ac.uk)