Evidence of Increasing Intensity of Food Processing During the Upper Paleolithic of Western Eurasia
Archaeologists have suggested that subsistence is central to understanding the population trajectory of Middle Paleolithic Neanderthals and Upper Paleolithic modern humans in western Eurasia. Zooarchaeology and stable isotope data have revealed that hunting supplied most of the protein requirements for Middle Paleolithic Neanderthals and early Upper Paleolithic modern humans. However, the application of dental wear, archaeobotany, and other techniques have shown that plants were an important part of the diet in both Middle and Upper Paleolithic societies in warm and cool regions of western Eurasia. Some lines of evidence have indicated that both groups potentially used a relatively similar range of plants even though this contradicts expectations from optimal foraging theory and diet breadth models positing that Middle Paleolithic societies used fewer plant foods. In this contribution, we identify evidence for increases in the use of Upper Paleolithic processing of plant foods in western Eurasia. We propose that increases in human population density throughout the Upper Paleolithic and especially during the late glacial period were supported by the more frequent use of plant food processing technologies, rather than the use of new plant food taxa.
KeywordsPaleolithic diet Aurignacian Gravettian Magdalenian Macrobotanical remains
The predominant models of Middle Paleolithic Neanderthal subsistence have emerged from the study of associated animal remains and lithic tools from Paleolithic sites. These have led to reconstructions of a narrow spectrum diet, which was heavily predicated on energetic returns from prime-aged medium- to large-game (Kuhn and Stiner 2006). In contrast, modern human diets during the Upper Paleolithic have often been thought to be diversified—comprising smaller game, fish, and plants in addition to medium- to large-game—even though there has been relatively little detailed study of plant exploitation during both periods. Subsequent research, applying direct dietary reconstruction techniques including carbon and nitrogen isotopes on collagen, have corroborated that meat was an important part of Neanderthal diets and that medium- and large-sized herbivores were the primary source of their protein intake. Carbon and nitrogen isotopes show that by the mid-Upper Paleolithic, significant quantities of aquatic foods (freshwater fish and mollusks) were featured in the diet (Richards et al. 2000, 2001). Although plants are expected to be of the greatest importance in the more southern warmer regions, stable isotopic dietary information is lacking because warmer climates are less conducive to the survival of ancient collagen in human bones. More recently, a broader application of dietary reconstruction techniques—including dental wear, biomarkers, microbotanicals in tool residues, dental calculus, and dental paleopathology—suggests Neanderthal diets included a substantial but so far unknown amount of plants (Hardy and Moncel 2011; Henry et al. 2011, 2014; Salazar-García et al. 2013; Sistiaga et al. 2014; Fiorenza et al. 2015). Some argue that potentially similar patterns characterize Middle and Upper Paleolithic diets (Hardy and Moncel 2011; Salazar-García et al. 2013; Sistiaga et al. 2014). This is compatible with isotopic data because plants primarily provide carbohydrates and micronutrients in human diets, which cannot be captured with isotopes. Furthermore, the idea that Neanderthal patterns of plant use in the Middle Paleolithic were broadly similar to those of modern humans during the Upper Paleolithic is incongruent with optimal foraging theory, diet breadth models (Winterhalder and Smith 2000), and human behavioral ecological frameworks which have relevance given how they have been verified in the ethnographic record (Winterhalder and Smith 2000). In addition, since Upper Paleolithic modern human populations existed at overwhelmingly higher population densities by the late glacial period, they should have had a higher contribution of plant foods and presumably had use of a broader number of plant species in response to resource depletion (Kelly 1995; Marean 1997; Bocquet-Appel et al. 2005). However, more recently, the widespread application of Niche Construction Theory has opened the way for new models to be developed to explain population changes. Food processing is one of the ways that human societies modify selection pressures and foster higher population densities (Wollstonecroft 2011).
In this contribution, we draw on the concept of food processing niche construction to address this discrepancy within an archaeological framework by examining changes in the vegetal component of Neanderthal and modern human diets and food processing regimes, from the Middle Paleolithic to the end of the Upper Paleolithic. We examine Upper Paleolithic societies as niche constructors and explore if by the late glacial period Upper Paleolithic societies may have had higher intensities of plant resource use than Neanderthals and early Upper Paleolithic societies. We envisage that they may have accomplished a higher intensity of plant use not by using more plant species, but by using more specialized food processing technology and that low specialization food processing technology developed into, or was replaced by, more intensive and specialized technologies that increased the absolute amount of nutrients obtained from edible plants that were already part of the diets of these groups.
Evidence of Similarity of Middle and Upper Paleolithic Plant Dietary Components?
Dental calculus represents one of the few datasets detailing the variability of plant dietary components during the Middle and Upper Paleolithic. Human dental calculus (calcified plaque) adhering to human remains is now known as a useful source of data on the environment and diet of ancient peoples because it contains inclusions of food remains and airborne particles deposited during life (Armitage 1975; Dobney and Brothwell 1986; Salazar-García et al. 2013; Power et al. 2014, 2015a, 2015b; Goude et al. 2018). Since dental calculus gained attention approximately 15 years ago, there have been only a number of limited applications on Middle and Upper Paleolithic human remains due to the fact that human remains are rarely found or are unavailable for much of the western Eurasian Paleolithic. Often the ancient teeth that are available for this research have been heavily handled and subject to wear studies that have inadvertently removed dental calculus from the enamel surface of ancient teeth (Leonard et al. 2015; Power et al. 2015a). Microbotanical dental calculus studies to date have included samples from Spy in Belgium; La Ferrassie, La Chapelle-aux-Saints, La Quina and Abri Pataud in France; Vindija in Croatia; Kůlna, Dolní Věstonice and Předmostí in the Czech Republic; Grotta Guattari and Grotta Fossellone in Italy; and El Sidrón, Sima de las Palomas and El Mirón Cave in Spain (Hardy et al. 2012; Salazar-García et al. 2013; Henry et al. 2014; Power et al. 2015a, 2016, 2018), while genetic and analytical chemistry dietary studies have been conducted for El Sidrón in Spain and Spy in Belgium (Weyrich et al. 2017).
Analyzed samples do not evenly represent the many environments that Neanderthals and modern humans occupied. However, data are available on Neanderthals from Sima de los Palomas in southeastern Spain who lived in warm temperate forests near the Mediterranean Sea and who exhibit more evidence of plant use (Walker et al. 2011). Nonetheless, analyzed samples over-represent groups living in highly cold, and dry environments, including those for the Gravettian period, when the cold-dry conditions meant less plant biomass, which favored a hunting-dominated economy concentrated on large ungulate herds (Kelly 1995; Straus 1995).
Dental calculus is thought to primarily provide information on the presence or absence of plant foods rather than the proportions of consumed foods, but the analysis conducted on these samples has so far failed to find differences in diversity of microbotanical types between Neanderthal and modern human groups (Henry et al. 2014). As sample size remains small, and because there is still a dramatic lack of data on early Upper Paleolithic populations, other lines of evidence are required to infer the degree of plant consumption.
Dental Wear Evidence
Middle Paleolithic Diets
Plant use can be readily discerned from studies of dental microwear given the grit associated with terrestrial resources and the hard seeds, nuts, phytoliths, and seed shells that tend to inflict damage to the enamel surface (Calandra et al. 2012; Karriger et al. 2016; Schmidt et al. 2016). Dental wear represents the largest comparable dataset of Neanderthal and modern human dietary reconstructions. Studies of dental wear suggest Neanderthals and Upper Paleolithic peoples present substantial variability in dietary regimes (El Zaatari et al. 2011; Krueger et al. 2017). Much of this variation can be explained by the ecogeographic distribution of Neanderthals such that individuals living in areas with greater tree cover—who presumably had more access to plant foods due to a milder, less seasonable climate—differ from those inhabiting more open areas (El Zaatari et al. 2011). When texture complexity—a 3-D approximation of enamel surface roughness under different scales of observation—is considered, Neanderthals such as Spy 1 and La Quina 5 from cold-steppe habitats exhibit lower values of 1.37 and 1.18, respectively, which aligns them to Holocene foragers with meat-based diets (El Zaatari et al. 2011). In contrast, El Sidrón 005 and Amud 1 from relatively warmer habitats show much greater texture complexity (2.69 and 3.07, respectively) and are comparable to foragers with mixed diets (El Zaatari et al. 2011). However, it should be mentioned that there are many edible plants on steppe landscapes. For example, geophytes are common as are certain resource-bearing open woodland trees such as terebinth and oak (Hillman 1996), which Neanderthals probably seasonally exploited in warm and moister areas.
Upper Paleolithic Diets
Upper Paleolithic peoples had mechanically challenging diets, particularly those from closed and wooded environments during the late glacial period. These environments offered an abundance of plant resources not available in the open-steppes (El Zaatari and Hublin 2014). However, some Upper Paleolithic peoples had softer diets, leaving less microwear on the teeth, although variation in the hardness of food also characterizes recent-forager diets (El Zaatari et al. 2011, 2016; El Zaatari and Hublin 2014; Schmidt et al. 2016). It is possible that a softer diet is a feature of a greater degree of meat consumption (Schmidt et al. 2016). Although it may be challenging to identify the proportion of meat to plant resources in Paleolithic diets, herders who consume large amounts of meat exhibit lower values for dental microwear textures than do agriculturalists (Schmidt et al. 2016). Meanwhile, plant foods, which can include inadvertent grit and other hard particles, tend to inflict greater damage to the enamel surface resulting in higher textural complexity (DeSantis et al. 2013; Schmidt et al. 2016). The processing of grains and seeds using grindstones or stone hammers can also introduce grit into the diet. Upper Paleolithic peoples appear to have maintained plants in their diets despite climate deterioration during the last glacial maximum of MIS 2 (El Zaatari and Hublin 2014; El Zaatari et al. 2016).
Upper Paleolithic diets show considerable variation in plant use and food processing, reflecting a diversification of subsistence strategies which increases late in the Pleistocene (Lalueza et al. 1996; Pérez-Pérez et al. 2003; Fiorenza et al. 2011; El Zaatari and Hublin 2014; García-González et al. 2015; El Zaatari et al. 2016). Individuals from the Aurignacian exhibit a diet that was relatively soft with comparatively low textural values (El Zaatari and Hublin 2014). Most individuals from Gravettian and Epi-Gravettian periods retain a hard- or gritty-food signal and fall within the convergence of foragers with meat-dominant and mixed (meat and vegetal) diets. However, individuals from some sites, such as Barma Grande, are predicted to have had meat-based diets combined with tough foods (El Zaatari and Hublin 2014). With respect to the Magdalenian sites, the great majority show evidence for a mixed diet (El Zaatari and Hublin 2014), suggesting that increases in plant use and food processing accelerated by the end of the Upper Paleolithic (Fig. 1).
Macrobotanical Plant Remains Suffer from Sampling Biases
Upper Paleolithic societies have left a higher number of sites with macrobotanical assemblages (Fig. 2). Rich datasets are available from the recently excavated central European site of Dolní Věstonice II in the Czech Republic (25 and 30 Kya) (Pryor et al. 2013). Dolní Věstonice is unusual in that flotation yielded rich deposits of non-woody charred matter, most of which were parenchymatous tissues indicating angiosperm underground storage organs. Although this tissue is mostly non-diagnostic of specific species, some specimens could represent underground storage organs of aquatic flora and tap roots from the Asteraceae family. The exploitation of taproots during an intensely cold period, when open tundra and mammoth steppe prevailed in the region, illustrates that plant exploitation in cold regions may be significantly underestimated. Alternatively, it could mean that highly specific plant use subsistence adaptations and hunting-dominated economies existed in the Gravettian without an ethnographic equivalent (Pryor et al. 2013; Power et al. 2016). As colder conditions receded, there is unambiguous evidence that warming heralded a rapid change in subsistence strategies, which increasingly incorporated resources that were previously less available, particularly plant taxa. There is a large increase in the number of sites with macrobotanical remains from the Magdalenian and other contemporaneous sites, which outpaces the estimated increases in human population (Bocquet-Appel et al. 2005). Flotation during the excavation of the Lower Magdalenian site of El Juyo on the Atlantic coast of northeast Spain recovered seeds from oak (Quercus sp.), hazelnut, raspberry (Rubus idaeus), soft-grass (Holcus sp.), and chenopods (Chenopodium sp.) (Online resource Table 1). This assemblage is surprising since acorns are expected to be a low-rank food due to processing requirements and not a feature of the human diet in cool environments of this region when other resources were available. However, acorns vary in palatability according to species, and it is generally expected that they enter the diet when other foods are not available even if encountered opportunistically during the exploitation of oak wood (Primavera and Fiorentino 2013). Oak woodland was rare on the mostly open terrain interspersed with stands of pine (Straus et al. 2013). Overall, charred plant assemblages demonstrate a clear ecological gradient. In temperate areas, resources such as hazelnut appear to have been used but a large proportion of assemblages occur in southern Europe including Klissoura Cave, Franchthi Cave, Theopetra, and Cova de les Cendres. In these relatively warmer regions, legumes and other seeds predominate but hazelnut is also used, echoing the strongly seed-based foraging economy that is detected in southwest Asia during this time (Hansen 1991; Mangafa 2000; Weiss et al. 2004; Aura et al. 2005; Lityñska-Zajac 2010; Martínez Varea and Badal García 2018). It is less clear if evidence of these assemblages points to increasing dietary breadth, although in Israel differences between Middle and Upper Paleolithic seed assemblages are arguably not dramatic due to the rich assemblage found at Kebara (Madella et al. 2002; Weiss et al. 2004; Lev et al. 2005).
Unfortunately, at some early excavations, it is not clear if seed assemblages are from secure contexts or introduced by natural processes, e.g., El Juyo (Freeman et al. 1988). It is unknown to what extent charred seed macrobotanical assemblages are likely to accumulate under non-anthropogenic conditions but many sizable Paleolithic charcoal assemblages yield no charred seeds after flotation (Freeman 1981). Although in some cases seed assemblages are ambiguous, others yield signs that imply they are likely to have been deposited by hominins. Macrobotanical assemblages primarily provide only qualitative insights into gathering economies. Therefore, other factors, such as food preparation, must be considered to adequately address the intensity of plant use in Paleolithic western Eurasia.
Plant Remains Offer Insights into Early Food Processing
The advent of food processing technology is elusive in the human fossil record but it cannot be assumed that technological barriers thwarted the adoption of these technologies even in the Middle Paleolithic. The use of unaltered stone hammers by west African wild chimpanzees to crack nuts demonstrates significant plant processing can be conducted with minimal technology through thrusting percussion tools (Boesch et al. 1994; de Beaune 2004). Furthermore, Upper Paleolithic humans heavily used fire and although different opinions exists on Middle Paleolithic hominin fire use, it appears many groups at least periodically used fire, a key agent in recent human food processing technologies beginning ∼ 300,000 to 400,000 years ago (Dibble et al. 2018; Johns and Kubo 1988; Roebroeks and Villa 2011).
The Role of Food Processing Technology in the Evolution of Paleolithic Diets
There is growing recognition that the defining subsistence trend over the course of human evolution is an increase in dietary quality, both in regard to caloric and nutritional density. In this paradigm, the ubiquity of food processing technology at archaeological sites is of central importance as it determines the pace of this overarching trend. Food processing is particularly relevant for vegetal-sourced nutrition, due to the structural and chemical barriers in plants that deter nutrient absorption. In contrast, animal foods lack these obstacles. Plant nutrients are frequently unavailable to human digestion. For example, nutrients may be encapsulated in cellular walls, stored as starch grains or contain toxins (Butterworth et al. 2016). If the food item is not processed in a way that disrupts structural or chemical barriers to enable bioavailable nutrients to become metabolically active and bioaccessible, they may be excreted from the body and lost (Wollstonecroft et al. 2012; Butterworth et al. 2016). In multi-step processing, bioaccessibility is highly influenced by the sequence of each processing step due to interactions. Furthermore, although pulverizing followed by boiling promotes bioaccessibility in the human body, boiling followed by pulverizing may not (Ydeman et al. 2001; Wollstonecroft et al. 2008), and excessive food processing can result in an unnecessary nutrient loss (Stahl 1984, 1989). Plant foods that respond to plant food processing with increased nutrients are abundant in Eurasian environments (Ellis et al. 2004; Ntone 2017).
Cooking is often thought to be the primary method of extrasomatic processing that increases bioaccessibility (Carmody and Wrangham 2009). Recent ethnographic ex vivo studies have cast doubt that cooking is always important for increasing bioaccessibility as they provide one example of cooking practiced in a savannah hunter-gatherer context that is too brief to substantially increase the nutrients available in plants (Schnorr et al. 2015). Needless to say, hunter-gatherer methods are marked by their diversity, and cooking methods that expose plant foods to heat for hours such as in pit cooking are common in the ethnographic record (Wandsnider 1997). Nonetheless, the difficulty in reconstructing a time transect of Paleolithic cooking intensity affirms that other factors in addition to heat treatment must be considered to reconstruct Paleolithic subsistence change.
Specialized Plant Exploitation and Processing Is Missing in the Archaeological Record
Although dental wear provides evidence that changes in food processing occurred in the Paleolithic (Fig. 1), it is circumstantial. To build a more complete picture of this trend, it is important to consider if there are archaeological traces of the technologies that may have been used to process foods. Most data on Paleolithic technology come from the study of knapped artifacts. From the onset of the Upper Paleolithic, there is more widespread innovation of technologically complex tools such as prismatic blade and bladelets, bone points, and projectile points (de Beaune 1993; Knecht 1993). These tools are directly related to resource provision strategies and offer the potential to gain insight into the dietary strategies of these societies. Although lithic technologies have been intensively studied since the nineteenth century, most of what is known concerns typological and technological change over time rather than tool use histories and food processing (Semenov 1964; Knecht 1993; Hardy et al. 2008). One of the approaches for examining tool function is identifying residues of use adhering to the tool surface. Residue studies attempted on Middle and Upper Paleolithic tools from the Crimea, southwest Germany, and northern Italy have reported the residues of wood, starchy plants, bird, and mammal tissues and have attempted to infer subsistence complexity (Hardy et al. 2001; Hardy and Moncel 2011; Aranguren et al. 2015). However, residue preservation biases are a problem because residues deteriorate over time, limiting the interpretive power of dietary reconstructions. Studies that have applied these analyses often recover multi-origin residues, and have difficulty inferring subsistence patterns from use wear and processing residue (Hardy et al. 2008), while surviving residues may represent manufacturing or other incidental contacts (Rots et al. 2016).
Our primary understanding of Paleolithic food processing technology derives from ethnographic studies of recent hunter-gatherers, which show how the collection and processing of specific resources at times can be inferred from perishable tools. Tools used by recent gatherers with only specialized functions include wicker screening baskets, digging sticks, and seed/fruit beaters (Coville 1904). Others, such as knapped blades, scrapers and axes, burden baskets, leaching bags, fermenting buckets, folded-bark containers, winnowing vessels, or drying mats may have been produced for specialized purposes, but they are technologies with broad applications. For example, foragers can use the same sticks for prying off edible inner tree bark as for dispatching game. However, most technology, whether specialized or not, is expected to have been produced from perishable materials such as wood and fiber and it is extremely seldom that these items may be preserved. A handful of waterlogged wooden implements have survived in special circumstances from 400 to 125 ka in present-day Germany and England (Schoch et al. 2015). Mostly these are interpreted as spears due to the length of the longest examples (up to 2.5 m) and pointed tips; however, their length and points are consistent with digging sticks. Foraging tools are mostly made, used, and disposed of over short periods, leaving few diagnostic markings or use wear, and thus identification would be difficult.
The Ebb and Flow of Changes in Food Processing Intensity Evident in Surviving Paleolithic Technology
The initial pulse in grindstone frequency is associated with the transitional Châtelperronian industry in southwest France (de Beaune 1993). Arguably this trend is ambiguous and hard to contextualize as the origin of Châtelperronian technology has been suggested to either represent continuity with the preceding Mousterian or a Neanderthal technology that is a result of diffusion from modern humans ( d’Errico et al. 1998; Bar-Yosef and Bordes 2010; Higham et al. 2010).
Although the shift to more intensive food preparation was represented by a gradual increase at first, this is not a uniform pattern. During the extreme cold of the Late Glacial Maximum, researchers might expect plant use to drop in relative importance to animal foods. However, macrobotanical data suggest this class of food may have been common in multiple ecogeographic zones, perhaps as a response to climate deterioration, and could have been more common than in the Middle Paleolithic (Fig. 2). Considerable variability in grindstones until the Late Glacial period is a reminder of the difficulty of directly associating culture with biological development (de Beaune 2004). Although the extent of plant food processing is likely to have depended on the type of foods most available in the local environments, we lack the resolution in our dataset to test this scenario (Hillman 1996). None the less we believe as food processing became culturally ubiquitous it fostered further introduction of plants into the diet that may only be consumed with processing (Fig. 3). This may have been particularly true in northern latitudes where plant nutrients were available in smaller packages which required more involved and lengthy nutrient unpacking (Jones 2009). This trend is confirmed with dental wear evidence, which demonstrates an increasing intensity in the use of hard and brittle foods during the Upper Paleolithic (Fig. 1). These foods become apparently dominant in many societies by the Late Glacial period, suggesting a relatively greater role of food processing and plants in the diet.
There are growing efforts to identify higher levels of Paleolithic dietary complexity to highlight the behavioral flexibility of Neanderthals and Upper Paleolithic humans (Klein and Steele 2008; Sistiaga et al. 2014; Weyrich et al. 2017). This effort has produced abundant evidence that the incorporation of plants in the diet is a ubiquitous phenomenon in Eurasia, and although data are sparse, strides have been made on the identification of the specific plant taxa that were used by Middle and Upper Paleolithic societies. Yet such efforts have come at a cost. Too much attention has been paid to how diet was procured and what specific classes of food such as terrestrial mammal, plant, or fish were exploited while understanding how food processing as external digestion allowed dietary change to occur has been largely overlooked. With the notable exception of butchery practices of fauna assemblages, which are well understood, little quantitative information on food processing of plant or animal foods has been available (Klein and Steele 2008; Wollstonecroft 2011; Karriger et al. 2016).
Although reconstructing methods of preparation is deeply challenging, the archaeological record does provide some insight into other areas of food processing. Increases in grindstone, dental wear, and the breadth of plant foods used affirm the evolution of more intensive and complex food processing technologies. However, the progressive increase in food processing was stemmed by the period of climate deterioration during the Glacial Maximum, which probably reduced the supply of foods suitable for intensification. Investigation of the plethora of possible technological practices (Johns and Kubo 1988), used singularly or in complicated sequences, will be essential to consider in any future exploration of Paleolithic subsistence patterns.
We thank Jiri Svoboda, Lawrence Guy Straus, Celia Helena Boyadjian, Elizabeth Velliky, Shira Gur-Arieh, Andrea Picin, Daniela Holst, and Nick Stephens for their suggestions, support, and insights. We thank Stephanie Schnorr for her comments on the manuscript, Mariska Carvalho for artwork and proof reading, and four anonymous reviewers and Nuno Bicho for improving the manuscript.
This research is funded by the Max Planck Society and Fulbright-Belgium.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflicts of interest.
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