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Journal of Paleolithic Archaeology

, Volume 1, Issue 4, pp 281–301 | Cite as

Evidence of Increasing Intensity of Food Processing During the Upper Paleolithic of Western Eurasia

  • Robert C. Power
  • Frank L’Engle Williams
Discussion

Abstract

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.

Keywords

Paleolithic diet Aurignacian Gravettian Magdalenian Macrobotanical remains 

Introduction

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.

Specialized diets and activities appear to drive some differences in dental microwear textures of Neanderthals. For example, a comparison of the Croatian sites of Vindija and Krapina indicates less reliance on hard foods compared to prehistoric and recent foragers and early agriculturalists (Karriger et al. 2016). Furthermore, Krapina Neanderthals exhibit elevated anisotropy, or patterning of striations deriving from tough fibrous foods, compared to those at Vindija and most Holocene humans, perhaps from the consumption of plants including grasses (Karriger et al. 2016). Alternatively, this elevated anisotropy could derive from weaving or braiding grasses, using the teeth as tools, as the digestibility of grasses in the hominin gut is questionable. This diversity in Neanderthals from different archaeological sites, however, is smaller than the contrast between Middle and Upper Paleolithic diets, particularly those from the Late Upper Paleolithic (El Zaatari and Hublin 2014; El Zaatari et al. 2016). Instead, Neanderthal and Upper Paleolithic dietary differentiation denotes an increasing use and processing of plant foods (Fig. 1).
Fig. 1

Venn diagram showing an approximate placement of Middle and Upper Paleolithic peoples based on dental wear studies (Lalueza et al. 1996; Fiorenza et al. 2011; El Zaatari and Hublin 2014; García-González et al. 2015). The Aurignacian features the softest diets, probably with a large contribution of meat. Gravettian and Epi-Gravettian sites overlap with the signals derived from recent foragers with meat-based and mixed diets. Magdalenian sites are generally characterized by the consumption of harder foods and resemble those of recent mixed-diet foragers, implying the increased use of plants. The intensity of food processing regimes increased between the Middle Paleolithic and Upper Paleolithic. However, the greatest differences in food processing and the use of plants occurred between the Gravettian and the Magdalenian, reflected in the generally higher complexity values and greater distribution of macrowear facets characterizing the most recent period of the Upper Paleolithic (Fiorenza et al. 2011; El Zaatari and Hublin 2014)

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

Occasionally plants appear depicted in cave paintings, and grass seed representations are found in Magdalenian portable rock art. Although examples cannot be confirmed as representing foods, the analogy of zoomorphic depictions of prey items suggests drawn or carved depictions of plants represent food resources (Tyldesley and Bahn 1983). Clearer evidence is available from archaeobotanical data, although they are scarce prior to the Holocene and are mostly confined to studies on charcoal (Owen 2002; Jones 2009). Mousterian archaeological sites suitable for flotation screening (i.e., occupation sites with extensive burnt deposits and discrete hearths) are found across Europe, but vegetal assemblages are considerably less abundant and less diverse than those in Israel, where large assemblages such as Ohalo II (22–23.5 ka) and Kebara Cave (48–59 ka) have heavily influenced the literature. Archaeologists have reported macrobotanical remains from 29 sites in western Eurasia (Online resource Table 1; Fig. 2). Middle Paleolithic assemblages are mostly found in the Mediterranean region although plant foods have been found as far north as 51° latitude at Rabutz, Neumark-Nord 2, and Lehringen in central Germany (Online resource Table 1). Burnt hazelnut shell (Corylus avellana) associated with archaeological deposits indicates that this energy-dense food was exploited during the MIS 5e Interglacial. Although there is a possibility that these shells entered the archaeological strata by natural processes following a forest fire, it seems unlikely (Toepfer 1958; Thieme et al. 1985). However, due to their hard structure, these robust plant remains are prone to overrepresentation (Jones 2000). The other few existing Middle Paleolithic sites with botanical remains provide a varied picture that indicates that plant use was prevalent primarily in southern Europe (Online resource Table 1). Some assemblages from southern Europe show a diverse range of plant species or genera represented while others do not. Just one plant taxon was reported from Mas-des-Caves on the Mediterranean Coast of France (Lumley 1975). Archaeobotanists have found macroremains from stone pine nut (Pinus pinea) and olive (Oliva spp.) dating to ∼ 52 ka in the western Mediterranean at Gorham’s Cave, Gibraltar (Online resource Table 1). Although olive and pine nuts are caloric foods, pine nut is labor intensive to collect and olive is labor intensive and technologically complicated to render edible (Johns and Kubo 1988). The most diverse macrobotanical assemblage thus-far identified is reported from Theopetra, in Greece (Online resource Table 1) (Mangafa 2000). Archaeologists found lentil (Lens), chickpea (Cicer), pea (Pisum), vetchling (Lathyrus), and several fruit and nut taxa. These varied plant food taxa indicate a complex foraging strategy that has been classified as “broad spectrum.” However, it is difficult to quantitatively assess as many macrobotanical reports lack volumetric estimates or even any quantification. It is clear that assemblages are limited in diversity and show different taxa compared to sites in Israel such as the Neanderthal assemblages at Kebara and Amud caves or the Upper Paleolithic assemblage at Ohalo II (Madella et al. 2002; Weiss et al. 2004; Lev et al. 2005). It is unclear if this lower diversity relates to biases in the intensity of fieldwork, with lower rates of archaeobotanical flotation applied in Europe and on earlier sites. In both areas, archaeobotanical flotation is only occasionally implemented across Paleolithic sites (Jones 2009).
Fig. 2

The number of European Middle and Upper Paleolithic macrobotanical assemblages so far identified (top). The number of sites with macrobotanical remains controlling for estimated population size found per a thousand years (Bocquet-Appel et al. 2005) (bottom). Data are from the Online resource Table 1. All chronologies are based on cal BP dates. The figure excludes assemblages from sites where chronology is poorly established (i.e., Weimar-Ehringsdorf) or outside the period or principal region of interest (e.g., Kebara Cave, Ohalo II, or Rot del Migdia)

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 most detailed reconstructions of Paleolithic plant food processing can be found in Israel at Ohalo II where intensive grinding of a diverse range of grass seed taxa has been detected (Piperno et al. 2004; Weiss et al. 2004; Snir et al. 2015). Yet Ohalo II represents an exception and in most archaeological sites, evidence of food processing is meager or absent. In some cases, food processing can be inferred from surviving macrobotanical remains. The phenotypic traits of plants also allow the inference that food processing was present. For example, Oleuropein is a glycoside that is abundant in raw olive drupes, that renders them inedible (Chinou 2011), and only by detoxifying, whether by curing in brine/leaching or pressing the drupes for oil, can olives be rendered edible (Johns and Kubo 1988). Therefore, the identification of olive remains in southern Iberia from the Middle Paleolithic period offers some evidence for a possible minimum date for the advent of this leaching/pressing technology (Fig. 3; Online resource Table 1). Other plant remains suggest additional behaviorally complex chaîne opératoires that are of major relevance to reconstructing the emergence of food processing technologies. Hazelnuts are an energy-dense resource that appear to have been a reoccurring food item in mild climates during the Upper Paleolithic and interglacial periods in the Middle Paleolithic. Hazelnut remains typically survive through shell charring, presumably during roasting. However, the preparation of roasted hazelnuts indicates the careful application of fire management for cooking (Fig. 3). Preparing hazelnuts without high levels of charring reduces edibility. Therefore, they must be carefully heated but isolated from direct fire contact, for example through shallow pit cooking (Mears and Hillman 2007). Charred hazelnut shell easily survives in the archaeological record but other food remains are far less durable. Evidence of tuber roasting is lacking until the middle of the Upper Paleolithic and the fragility of charred tubers likely greatly underestimates the earlier occurrence of this practice (Fig. 3). Many of the important Upper Paleolithic archaeobotanical assemblages that have been found lack quantification and full taxa lists. Therefore, it is not always clear if and to what extent remains may be charred or uncharred and potentially non-anthropogenic. If such plant remains as depicted in these examples could be confirmed to be anthropogenic, then it would certainly add to the evidence for the increasing complexity of food processing techniques over time.
Fig. 3

The number of taxa identified in European Middle and Upper Paleolithic macrobotanical assemblages (top). The number of taxa identified in European Middle and Upper Paleolithic macrobotanical assemblages controlling for population size (Bocquet-Appel et al. 2005) (bottom). Data are from Online resource Table 1. All chronologies are based on cal BP dates

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 few durable food processing implements include Paleolithic pounders, hammers, and grindstones, used for grinding and pounding (de Beaune 2004). Although this technology is often associated with cereals, hunter-gatherers may grind or pound many categories of food to increase softness, to dehusk, or for detoxification through leaching or other means (Coville 1904; Gott 1982; Johns and Kubo 1988; de Beaune 2004; Mears and Hillman 2007). From a nutritional perspective, grinding and pounding are important as a form of external digestion because they greatly decrease food particle size and increase nutrient bioaccessibility of animal and plant foods (Boback et al. 2007). Grindstone use in the food chain is also a contributing factor to dietary grittiness and dental wear, which may explain significant changes in Upper Paleolithic dental wear patterns (Fig. 1). This technology is not exclusive to food processing and some studies of Upper Paleolithic grindstones have linked some grindstone wear to mineral processing rather than plant use (Svoboda and Přichystal 2005; Svoboda 2007). Yet grindstones are essentially a multipurpose technology. As these tools may be made from stone (although bone and wooden examples are common in the ethnographic record), they survive in unusually representative numbers at archaeological sites. This allows their frequency to be taken to broadly reflect resource intensification once accompanying changes in human population density are taken into account (Fig. 4) (de Beaune 1993; Wright 1994). These thrusting percussion processes are derived from resting percussion, a technology practiced by hominins for several million years (de Beaune 2004). They are considered by some to be a characteristic sign of Upper Paleolithic societies (Stiner 2001, 2013; Haws 2004). Although such technology is known from the African Middle Stone Age (McBrearty and Brooks 2000) in Europe, they are often considered to be absent or archaeologically invisible prior to the transitional Châtelperronian industry, but purported Middle Paleolithic examples have been reported in Iberia, southwestern France, and in the Middle Dniester Valley, Ukraine (Freeman 1964; Chernysh 1987; de Beaune 1993). However, it is not yet clear if their presence signals changes in the intensity of food processing, or is simply a product of increasing population size. To explore if increases in grindstones can be attributed to changes in food processing or increases in population size, we classified grindstones into five periods given that population size estimates are available. These are Mousterian, Aurignacian, Gravettian, Glacial Maximum (Lower Magdalenian and Solutrean), and Late Glacial (Middle, Upper, Final Magdalenian and early Mesolithic prior to 11,500 cal BP). Then, we divided the number of percussion grindstones in each period by the length of each period, and then by estimated population density (Bocquet-Appel et al. 2005; Briggs et al. 2009). Since Mousterian population estimates were produced with different methodologies, we performed this analysis conservatively with a relatively higher estimate of Neanderthal population size (4000). Although we have data on the abundance of Châtelperronian grindstones, we excluded them, as we lack Châtelperronian population estimates. We also excluded many grindstones with low confidence dating or provenience (Online resource Table 2). The results of both models indicate a slow increase in the frequency of grindstones that exceeds modeled population growth (Fig. 4).
Fig. 4

Total numbers of European Middle and Upper Paleolithic grindstones (top). Grindstone frequency in each cultural grouping divided by duration of period and population estimate (Bocquet-Appel et al. 2005; Briggs et al. 2009) (bottom). From sources shown in the Online resource Table 2. All chronologies are based on cal BP dates

It may be noted that the number of grindstones from Mousterian sites is slightly higher than the transitional and Aurignacian contexts. However, given the long duration of the Mousterian, the frequency is lower than at any other time. A rapid increase in use is evident across Europe at Gravettian and Epi-Gravettian sites, reflecting intensive food processing (Svoboda and Přichystal 2005), followed by a period of rarity during the Glacial Maximum (Figs. 4 and 5; Online resource Table 2). Some Gravettian examples have yielded putative plant food residues (Revedin et al. 2010; Aranguren et al. 2015). It is essential to note that wear on any grinding stone tool repetitive enough to create a deep, concave working surface characterizing those from agricultural societies is absent before the Mesolithic. Thus, pre-Mesolithic examples exhibit only low-intensity use and are generally unmodified by primary or secondary reduction (Outils a posterior) (Wright 1992). Reported grindstones are likely underestimates of food processing technology. To grind seeds and nuts, highly mobile Paleolithic hominins may have used modest pieces of naturally shaped stone (manuports) that archaeologists might overlook. Anthropogenically deposited cobbles, which are occasionally found and interpreted as knapping hammer stones, may have been used for bone or plant grinding and pounding; however, without studies confirming their use, they may not be relevant to diet.
Fig. 5

Minimum dates of appearance of heat and food processing technologies in Europe based on the processing requirements of archaeobotanical finds such as pressing/leeching required for olive consumption and production of birch tar (Barton et al. 1999; Koller et al. 2001; Mazza et al. 2006). All chronologies are based on cal BP dates. Hatched = uncertain dates

Discussion

It has been argued that intensive food processing did not commence in Eurasia until modern humans introduced it as part of a suite of new economic strategies (Stiner 2001, 2013; Haws 2004). We can confirm this trend with extant archaeological data on tool use. Although we cannot identify how and when food processing began, the data show an evolution of use that began at the latest by the appearance of Aurignacian-associated modern human societies and ebbed and flowed until rapid increases in the Late Glacial. The strong link between grindstones and plant food preparation hints that this trend does not just mark a changing relationship with diet, it also marks a growing intensity of plant use (Fig. 6) (Wright 1994). This is reinforced by the sharp increases in macrobotanical assemblages recovered by the end of the Late Glacial.
Fig. 6

A chronological overview of the presence of macrobotanical assemblages and grindstones through periods with both forested and open-dominated landscapes in northern and southern regions of western Eurasia during the past 200,000 years. Vegetation phases based on conventional oxygen isotope and pollen reconstructions (van Andel and Tzedakis 1996)

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.

Conclusions

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.

Notes

Acknowledgments

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.

Funding

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.

Supplementary material

41982_2018_14_MOESM1_ESM.docx (125 kb)
ESM 1 (DOCX 124 kb)

References

  1. Aranguren, B., Becattini, R., Mariotti Lippi, M., & Revedin, A. (2015). Grinding flour in Upper Palaeolithic Europe (25,000 years bp). Antiquity, 81, 845–855.Google Scholar
  2. Armitage, P. L. (1975). The extraction and identification of opal phytoliths from the teeth of ungulates. Journal of Archaeological Science, 2, 450–455.Google Scholar
  3. Aura, J. E., Carrión, Y., Estrelles, E., & Jordà, G. P. (2005). Plant economy of hunter-gatherer groups at the end of the last Ice Age: Plant macroremains from the cave of Santa Maira (Alacant, Spain) ca. 12,000-9,000 B.P. Vegetation History and Archaeobotany, 14, 542–550.Google Scholar
  4. Barton, R. N. E., Currant, A. P., Fernández-Jalvo, Y., Finlayson, J. C., Goldberg, P., MacPhail, R., et al. (1999). Gibraltar Neanderthals and results of recent excavations in Gorham’s, Vanguard and Ibex Caves. Antiquity, 73, 13–23.Google Scholar
  5. Bar-Yosef, O., & Bordes, J. G. (2010). Who were the makers of the Châtelperronian culture? Journal of Human Evolution, 59, 586–593.  https://doi.org/10.1016/j.jhevol.2010.06.009.CrossRefGoogle Scholar
  6. Boback, S. M., Cox, C. L., Ott, B. D., Carmody, R., Wrangham, R. W., & Secor, S. M. (2007). Cooking and grinding reduces the cost of meat digestion. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 148, 651–656.Google Scholar
  7. Bocquet-Appel, J. P., Demars, P. Y., Noiret, L., & Dobrowsky, D. (2005). Estimates of Upper Palaeolithic meta-population size in Europe from archaeological data. Journal of Archaeological Science, 32, 1656–1668.Google Scholar
  8. Boesch, C., Marchesi, P., Marchesi, N., Fruth, B., & Joulian, F. (1994). Is nut cracking in wild chimpanzees a cultural behaviour? Journal of Human Evolution, 26, 325–338.Google Scholar
  9. Briggs, A. W., Good, J. M., Green, R. E., Krause, J., Maricic, T., Stenzel, U., Lalueza-Fox, C., et al. (2009). Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science, 325, 318–321.Google Scholar
  10. Butterworth, P. J., Ellis, P. R., & Wollstonecroft, M. (2016). Why protein is not enough: The role of plants and plant processing in delivering the dietary requirements of modern and early Homo. In K. Hardy & L. Kubiak-Martens (Eds.), Wild harvest: plants in the hominin and pre-agrarian human worlds (pp. 31–55). Oxford: Oxbow.Google Scholar
  11. Calandra, I., Schulz, E., Pinnow, M., Krohn, S., & Kaiser, T. M. (2012). Teasing apart the contributions of hard dietary items on 3D dental microtextures in primates. Journal of Human Evolution, 63, 85–98.Google Scholar
  12. Carmody, R. N., & Wrangham, R. W. (2009). The energetic significance of cooking. Journal of Human Evolution, 57, 379–391.Google Scholar
  13. Chernysh, A. P. (1987). The standard multilayered site Molodova V: Archaeology. In I. Goretsky & S. M. Tseitlin (Eds.), The multilayered Paleolithic site Molodova (pp. 7–93). Moscow: Nauka.Google Scholar
  14. Chinou, I. (2011). Assessment report on Olea europaea L., folium, Committee on Herbal Medicinal Products. European Medicines Agency.Google Scholar
  15. Coville, F. V. (1904). Wokas, a primitive food of the Klamath Indians. Annual Report of the United States National Museum, 1902, 725–739.Google Scholar
  16. de Beaune, S. A. (1993). Nonflint stone tools of the Early Upper Paleolithic. In H. Knecht, A. Pike-Tay, & R. White (Eds.), Before Lascaux: the complex record of the Early Upper Paleolithic (pp. 163–191). Boca Raton: CRC Press.Google Scholar
  17. de Beaune, S. A. (2004). The invention of technology. Current Anthropology, 45, 139–162.Google Scholar
  18. d’Errico, F., Zilhão, J., Julien, M., Baffier, D., & Pelegrin, J. (1998). Neanderthal acculturation in Western Europe? A critical review of the evidence and its interpretation. Current Anthropology, 39, S1–S44.  https://doi.org/10.1086/204689.CrossRefGoogle Scholar
  19. DeSantis, L. R. G., Scott, J. R., Schubert, B. W., Donohue, S. L., McCray, B. M., Van Stolk, C. A., et al. (2013). Direct comparisons of 2D and 3D dental microwear proxies in extant herbivorous and carnivorous mammals. Public Library of Science One, 8, e71428.Google Scholar
  20. Dibble, H. L., Sandgathe, D., Goldberg, P., McPherron, S., & Aldeias, V. (2018). Were western European Neandertals able to make fire? Journal of Paleolithic Archaeology, 1, 54–79.  https://doi.org/10.1007/s41982-017-0002-6.CrossRefGoogle Scholar
  21. Dobney, K., & Brothwell, D. (1986). Dental calculus: Its relevance to ancient diet and oral ecology. In E. Cruwys & R. A. Foley (Eds.), Teeth and Anthropology (pp. 55–81). Oxford: BAR International Series 291.Google Scholar
  22. El Zaatari, S., Grine, F. E., Ungar, P. S., & Hublin, J.-J. (2011). Ecogeographic variation in Neandertal dietary habits: Evidence from occlusal molar microwear texture analysis. Journal of Human Evolution, 61, 411–424.Google Scholar
  23. El Zaatari, S., Grine, F. E., Ungar, P. S., & Hublin, J.-J. (2016). Neandertal versus modern human dietary responses to climatic fluctuations. Public Library of Science One, 11, e0153277.Google Scholar
  24. El Zaatari, S., & Hublin, J.-J. (2014). Diet of Upper Paleolithic modern humans: Evidence from microwear texture analysis. American Journal of Physical Anthropology, 153, 570–581.Google Scholar
  25. Ellis, P. R., Kendall, C. W. C., Ren, Y., Parker, C., Pacy, J. F., Waldron, K. W., et al. (2004). Role of cell walls in the bioaccessibility of lipids in almond seeds. American Journal of Clinical Nutrition, 80, 604–613.Google Scholar
  26. Fiorenza, L., Benazzi, S., Henry, A. G., Salazar-García, D. C., Blasco, R., Picin, A., Wroe, S., et al. (2015). To meat or not to meat? New perspectives on Neanderthal ecology. American Journal of Physical Anthropology, 156, 43–71.Google Scholar
  27. Fiorenza, L., Benazzi, S., Tausch, J., Kullmer, O., Bromage, T. G., & Schrenk, F. (2011). Molar macrowear reveals Neanderthal eco-geographic dietary variation. Public Library of Science One, 6, e14769.Google Scholar
  28. Freeman, L. G. (1964). Mousterian developments in Cantabrian Spain. Ph.D. dissertation. University of Chicago.Google Scholar
  29. Freeman, L. G. (1981). The fat of the land: Notes on Paleolithic diet in Iberia. In R. S. O. Harding & G. Telecki (Eds.), Omnivorous primates: gathering and hunting in human evolution (pp. 104–165). New York: Columbia University Press.Google Scholar
  30. Freeman, L. G., Echegaray, J. G., Klein, R. G., & Crowe, W. T. (1988). Dimensions of research at El Juyo. In H. L. Dibble & A. Montet-White (Eds.), Upper Pleistocene prehistory of western Eurasia (pp. 3–39). Philadelphia: University Museum.Google Scholar
  31. García-González, R., Carretero, J. M., Richards, M. P., Rodríguez, L., & Quam, R. (2015). Dietary inferences through dental microwear and isotope analyses of the Lower Magdalenian individual from El Mirón Cave (Cantabria, Spain). Journal of Archaeological Science, 60, 28–38.Google Scholar
  32. Gott, B. (1982). Ecology of root use by the Aborigines of southern Australia. Archaeology Oceania, 17, 59–67.Google Scholar
  33. Goude, G., Salazar-García, D. C., Power, R. C., Terrom, J., Rivollat, M., Deguilloux, M.-F., et al. (2018). A multidisciplinary approach to Neolithic life reconstruction. Journal of Archaeological Method and Theory.  https://doi.org/10.1007/s10816-018-9379-x.
  34. Hansen, J. M. (1991). The Palaeoethnobotany of Franchthi Cave, excavations at Franchthi Cave, Greece. Bloomington, IN: Indiana University Press.Google Scholar
  35. Hardy, B. L., Bolus, M., & Conard, N. J. (2008). Hammer or crescent wrench? Stone-tool form and function in the Aurignacian of southwest Germany. Journal of Human Evolution, 54, 648–662.Google Scholar
  36. Hardy, B. L., Kay, M., Marks, A. E., & Monigal, K. (2001). Stone tool function at the paleolithic sites of Starosele and Buran Kaya III, Crimea: Behavioral implications. Proceedings of the National Academy of Sciences of the United States of America, 98, 10972–10977.Google Scholar
  37. Hardy, B. L., & Moncel, M.-H. (2011). Neanderthal use of fish, mammals, birds, starchy plants and wood 125-250,000 years ago. Public Library of Science One, 6, e23768.Google Scholar
  38. Hardy, K., Buckley, S., Collins, M. J., Estalrrich, A., Brothwell, D., Copeland, L., et al. (2012). Neanderthal medics? Evidence for food, cooking, and medicinal plants entrapped in dental calculus. Die Naturwissenschaften, 99, 617–626.Google Scholar
  39. Haws, J. A. (2004). An Iberian perspective on Upper Paleolithic plant consumption. Promontoria, 2, 49–105.Google Scholar
  40. Henry, A. G., Brooks, A. S., & Piperno, D. R. (2011). Microfossils in calculus demonstrate consumption of plants and cooked foods in Neanderthal diets (Shanidar III, Iraq; Spy I and II, Belgium). Proceedings of the National Academy of Sciences of the United States of America, 108, 486–491.Google Scholar
  41. Henry, A. G., Brooks, A. S., & Piperno, D. R. (2014). Plant foods and the dietary ecology of Neanderthals and early modern humans. Journal of Human Evolution, 69, 44–54.Google Scholar
  42. Higham, T. F. G., Jacobi, R., Julien, M., David, F., Basell, L., Wood, R. E., et al. (2010). Chronology of the Grotte du Renne (France) and implications for the context of ornaments and human remains within the Châtelperronian. Proceedings of the National Academy of Sciences of the United States of America, 107, 20234–20239.Google Scholar
  43. Hillman, G. (1996). Late Pleistocene changes in wild plant-foods available to hunter-gatherers of the northern Fertile Crescent: Possible preludes to cereal cultivation. In D. R. Harri (Ed.), The origins and spread of agriculture and pastoralism in Eurasia (pp. 159–203). London: University College London Press.Google Scholar
  44. Johns, T., & Kubo, I. (1988). A survey of traditional methods employed for the detoxification of plant foods. Journal of Ethnobiology, 8, 81–129.Google Scholar
  45. Jones, G. (2000). Evaluating the importance of cultivation and collecting in Neolithic Britain. In A. S. Fairbairn (Ed.), Plants in Neolithic Britain and beyond (pp. 79–84). Oxford: Oxbow.Google Scholar
  46. Jones, M. (2009). Moving north: Archaeobotanical evidence for plant diet in Middle and Upper Paleolithic Europe. In J.-J. Hublin & M. P. Richards (Eds.), The evolution of hominin diets: integrating approaches to the study of Palaeolithic subsistence (pp. 171–180). Dordrecht: Springer.Google Scholar
  47. Karriger, W. M., Schmidt, C. W., & Smith, F. (2016). Dental microwear texture analysis of Croatian Neandertal molars. PaleoAnthropology, 2016, 172–184.Google Scholar
  48. Kelly, R. L. (1995). The foraging spectrum: diversity in hunter-gatherer lifeways. New York: Eliot Werner Publications.Google Scholar
  49. Klein, R. G., & Steele, T. E. (2008). Gibraltar data are too sparse to inform on Neanderthal exploitation of coastal resources. Proceedings of the National Academy of Sciences of the United States of America, 105, E115 author reply E116.Google Scholar
  50. Knecht, H. (1993). Early Upper Paleolithic approaches to bone and antler projectile technology. Archeological Papers of the American Anthropological Association, 4, 33–47.Google Scholar
  51. Koller, J., Baumer, U., & Mania, D. (2001). High-tech in the Middle Palaeolithic: Neandertal-manufactured pitch identified. European Journal of Archaeology, 4, 385–397.Google Scholar
  52. Krueger, K. L., Ungar, P. S., Guatelli-Steinberg, D., Hublin, J.-J., Pérez-Pérez, A., Trinkaus, E., et al. (2017). Anterior dental microwear textures show habitat-driven variability in Neandertal behavior. Journal of Human Evolution, 105, 13–23.Google Scholar
  53. Kuhn, S. L., & Stiner, M. C. (2006). What’s a mother to do? The division of labor among Neandertals and modern humans in Eurasia. Current Anthropology, 47, 953–981.Google Scholar
  54. Lalueza, C., Pérez-Pérez, A., & Turbón, D. (1996). Dietary inferences through buccal microwear analysis of Middle and Upper Pleistocene human fossils. American Journal of Physical Anthropology, 100, 367–387.Google Scholar
  55. Leonard, C., Vashro, L., O’Connell, J. F., & Henry, A. G. (2015). Plant microremains in dental calculus as a record of plant consumption: A test with Twe forager-horticulturalists. Journal of Archaeological Science Reports, 2, 449–457.Google Scholar
  56. Lev, E., Kislev, M. E., & Bar-Yosef, O. (2005). Mousterian vegetal food in Kebara Cave, Mt. Carmel. Journal of Archaeological Science, 32, 475–484.Google Scholar
  57. Lityñska-Zajac, M. (2010). Plant material from the Klissoura Cave 1 in Greece. Eurasian Prehistory, 7, 87–90.Google Scholar
  58. Lumley, H., de 1975. Cultural evolution in France in its paleoecolgical setting. In K.W. Butzer, & G.L. Isaac (Eds.). After the Australopithecines: stratigraphy, ecology, and culture change in the Middle Pleistocene (pp. 745–808). Mouton, The Hague.Google Scholar
  59. Madella, M., Jones, M. K., Goldberg, P., Goren, Y., & Hovers, E. (2002). The exploitation of plant resources by Neanderthals in Amud Cave (Israel): The evidence from phytolith studies. Journal of Archaeological Science, 29, 703–719.Google Scholar
  60. Mangafa, M. (2000). Plant exploitation from the Middle Paleolithic to the Neolithic: From food gathering to farming. Archaeobotanical study of Theopetra cave. In N. Kyparissi-Apostolika (Ed.). Theopetra Cave: proceedings of the international conference, Trkala (pp. 135–138). Athens, Greek Ministry of Culture and Institute for Aegean Prehistory.Google Scholar
  61. Marean, C. W. (1997). Hunter–gatherer foraging strategies in tropical grasslands: Model building and testing in the East African Middle and Late Stone Age. Journal of Anthropological Archaeology, 16, 189–225.Google Scholar
  62. Martínez Varea, C. M., & Badal García, E. (2018). Plant use at the end of the Upper Palaeolithic: Archaeobotanical remains from Cova de les Cendres (Teulada-Moraira, Alicante, Spain). Vegetation History and Archaeobotany, 27, 3–14.Google Scholar
  63. Mazza, P. P. A., Martini, F., Sala, B., Magi, M., Colombini, M. P., Giachi, G., et al. (2006). A new Palaeolithic discovery: Tar-hafted stone tools in a European Mid-Pleistocene bone-bearing bed. Journal of Archaeological Science, 33, 1310–1318.Google Scholar
  64. McBrearty, S., & Brooks, A. S. (2000). The revolution that wasn’t: A new interpretation of the origin of modern human behavior. Journal of Human Evolution, 39, 453–563.Google Scholar
  65. Mears, R., & Hillman, G. C. (2007). Wild food. London: Hodder & Stoughton.Google Scholar
  66. Ntone, E. (2017). The effect of cell wall encapsulation on digestion of macronutrients derived from nuts: Lipid bioaccessibility, MSc Thesis. Wageningen University.Google Scholar
  67. Owen, L. R. (2002). Reed tents and straw baskets? Plant resources during the Magdalenian of Southwest Germany. In S. L. R. Mason & J. G. Hather (Eds.), Hunter-gatherer archaeobotany: perspectives from the northern temperate zone (pp. 156–174). London: Institute of Archaeology.Google Scholar
  68. Pérez-Pérez, A., Espurz, V., Bermúdez de Castro, J. M., de Lumley, M. A., & Turbón, D. (2003). Non-occlusal dental microwear variability in a sample of Middle and Late Pleistocene human populations from Europe and the Near East. Journal of Human Evolution, 44, 497–513.Google Scholar
  69. Piperno, D. R., Weiss, E., Holst, I., & Nadel, D. (2004). Processing of wild cereal grains in the Upper Palaeolithic revealed by starch grain analysis. Nature, 430, 670–673.Google Scholar
  70. Power, R. C., Salazar-García, D. C., & Henry, A. G. (2016). Dental calculus evidence of Gravettian diet and behaviour at Dolní Věstonice and Pavlov. In J. Svoboda (Ed.), Dolní Věstonice II: chronostratigraphy, paleoethnology, paleoanthropology (pp. 345–352). Brno: Academy of Sciences of the Czech Republic, Institute of Archeology.Google Scholar
  71. Power, R. C., Salazar-García, D. C., Rubini, M., Darlas, A., Harvati, K., Walker, M., et al. (2018). Dental calculus indicates widespread plant use within the stable Neanderthal dietary niche. Journal of Human Evolution, 119, 27–41.Google Scholar
  72. Power, R. C., Salazar-García, D. C., Straus, L. G., González Morales, M. R., & Henry, A. G. (2015a). Microremains from El Mirón Cave human dental calculus suggest a mixed plant-animal subsistence economy during the Magdalenian in Northern Iberia. Journal of Archaeological Science, 60, 39–46.Google Scholar
  73. Power, R. C., Salazar-García, D. C., Wittig, R. M., Freiberg, M., & Henry, A. G. (2015b). Dental calculus evidence of Taï Forest chimpanzee plant consumption and life history transitions. Scientific Reports, 5, 15161.Google Scholar
  74. Power, R. C., Salazar-García, D. C., Wittig, R. M., & Henry, A. G. (2014). Assessing use and suitability of scanning electron microscopy in the analysis of micro remains in dental calculus. Journal of Archaeological Science, 49, 160–169.Google Scholar
  75. Primavera, M., & Fiorentino, G. (2013). Acorn gatherers: Fruit storage and processing in southeastern Italy during the Bronze Age. Origini, 35, 211–227.Google Scholar
  76. Pryor, A. J. E., Steele, M., Jones, M. K., Svoboda, J., & Beresford-Jones, D. G. (2013). Plant foods in the Upper Palaeolithic at Dolní Věstonice? Parenchyma redux. Antiquity, 87, 971–984.Google Scholar
  77. Revedin, A., Aranguren, B., Becattini, R., Longo, L., Marconi, E., Lippi, M. M., et al. (2010). Thirty thousand-year-old evidence of plant food processing. Proceedings of the National Academy of Sciences of the United States of America, 107, 18815–18819.Google Scholar
  78. Richards, M. P., Pettitt, P. B., Stiner, M. C., & Trinkaus, E. (2001). Stable isotope evidence for increasing dietary breadth in the European mid-Upper Paleolithic. Proceedings of the National Academy of Sciences of the United States of America, 98, 6528–6532.Google Scholar
  79. Richards, M. P., Pettitt, P. B., Trinkaus, E., Smith, F. H., Paunović, M., & Karavanić, I. (2000). Neanderthal diet at Vindija and Neanderthal predation: The evidence from stable isotopes. Proceedings of the National Academy of Sciences of the United States of America, 97, 7663–7666.Google Scholar
  80. Roebroeks, W., & Villa, P. (2011). On the earliest evidence for habitual use of fire in Europe. Proceedings of the National Academy of Sciences of the United States of America, 108, 5209–5214.Google Scholar
  81. Rots, V., Hayes, E., Cnuts, D., Lepers, C., & Fullagar, R. (2016). Making sense of residues on flaked stone artefacts: Learning from blind tests. Public Library of Science One, 11, e0150437.Google Scholar
  82. Salazar-García, D. C., Power, R. C., Sanchis Serra, A., Villaverde, V., Walker, M. J., & Henry, A. G. (2013). Neanderthal diets in central and southeastern Mediterranean Iberia. Quaternary International, 318, 3–18.Google Scholar
  83. Schmidt, C. W., Beach, J. J., McKinley, J. I., & Eng, J. T. (2016). Distinguishing dietary indicators of pastoralists and agriculturists via dental microwear texture analysis. Surface Topography: Metrology and Properties, 4, 014008.Google Scholar
  84. Schnorr, S. L., Crittenden, A. N., Venema, K., Marlowe, F. W., & Henry, A. G. (2015). Assessing digestibility of Hadza tubers using a dynamic in-vitro model. American Journal of Physical Anthropology, 158, 371–385.Google Scholar
  85. Schoch, W. H., Bigga, G., Böhner, U., Richter, P., & Terberger, T. (2015). New insights on the wooden weapons from the Paleolithic site of Schöningen. Journal of Human Evolution, 89, 214–225.Google Scholar
  86. Semenov, S. A. (1964). Prehistoric technology. London: Cory, Adams & Mackay.Google Scholar
  87. Sistiaga, A., Mallol, C., Galván, B., & Summons, R. E. (2014). The Neanderthal meal: A new perspective using faecal biomarkers. Public Library of Science One, 9, e101045.Google Scholar
  88. Snir, A., Nadel, D., & Weiss, E. (2015). Plant-food preparation on two consecutive floors at Upper Paleolithic Ohalo II, Israel. Journal of Archaeological Science, 53, 61–71.Google Scholar
  89. Stahl, A. B. (1984). Hominid dietary selection before fire. Current Anthropology, 25, 151–168.Google Scholar
  90. Stahl, A. B. (1989). Plant-food processing: Implications for dietary quality. In D. R. Harris & G. C. Hillman (Eds.), Foraging farming (pp. 171–196). London: Unwin Hyman.Google Scholar
  91. Stiner, M. C. (2001). Thirty years on the “Broad Spectrum Revolution” and paleolithic demography. Proceedings of the National Academy of Sciences of the United States of America, 98, 6993–6996.Google Scholar
  92. Stiner, M. C. (2013). An unshakable Middle Paleolithic? Trends versus conservatism in the predatory niche and their social ramifications. Current Anthropology, 54, S288–S304.Google Scholar
  93. Straus, L. G. (1995). The Upper Paleolithic of Europe: An overview. Evolutionary Anthropology, 4, 4–16.Google Scholar
  94. Straus, L. G., Morales, M. G., Arroyo, A. B. M., & Chiapusso, M. J. I. (2013). The human occupations of El Mirón Cave (Ramales de La Victoria, Cantabria, Spain) during the Last Glacial Maximum/Solutrean period. Espacio, Tiempo y Forma. Serie I, Prehistoria y Arqueología, 1, 413–426.Google Scholar
  95. Svoboda, J., & Přichystal, A. (2005). Nonflint and heavy-duty industries. In J. Svoboda (Ed.), Pavlov I Southeast: a window into the Gravettian lifestyles (pp. 148–166). Brno: Academy of Sciences of the Czech Republic, Institute of Archaeology.Google Scholar
  96. Svoboda, J. A. (2007). The Gravettian on the Middle Danube. Paléo, 19, 203–220.Google Scholar
  97. Thieme, H., Veil, S., Meyer, W., Möller, J., & Plisson, H. (1985). Neue Untersuchungen zum eemzeitlichen Elefanten-Jagdplatz Lehringen. Die Kunde Zeitschrift für niedersächsische Archäologie, 36, 11–58.Google Scholar
  98. Toepfer, V. (1958). Steingeräte und Palökologie der mittelpaläolithischen Fundstelle Rabutz bei Halle (Saale). Jahresschrift für mitteldeutsche Vorgeschichte, 41, 140–177.Google Scholar
  99. Tyldesley, J. A., & Bahn, P. G. (1983). Use of plants in the European Palaeolithic: A review of the evidence. Quaternary Science Reviews, 2, 53–81.Google Scholar
  100. van Andel, T. H., & Tzedakis, P. C. (1996). Palaeolithic landscapes of Europe and environs, 150,000-25,000 years ago: An overview. Quaternary Science Reviews, 15, 481–500.Google Scholar
  101. Walker, M. J., Zapata, J., Lombardi, A. V. V., & Trinkaus, E. (2011). New evidence of dental pathology in 40,000-year-old Neandertals. Journal of Dental Research, 90, 428–432.Google Scholar
  102. Wandsnider, L. (1997). The roasted and the boiled: Food composition and heat treatment with special emphasis on pit-hearth cooking. Journal of Anthropological Archaeology, 16, 1–48.Google Scholar
  103. Weiss, E., Wetterstrom, W., Nadel, D., & Bar-Yosef, O. (2004). The broad spectrum revisited: Evidence from plant remains. Proceedings of the National Academy of Sciences of the United States of America, 101, 9551–9555.Google Scholar
  104. Weyrich, L. S., Duchene, S., Soubrier, J., Arriola, L., Llamas, B., Breen, J., et al. (2017). Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus. Nature, 544, 357–361.Google Scholar
  105. Winterhalder, B., & Smith, E. A. (2000). Analyzing adaptive strategies: Human behavioral ecology at twenty-five. Evolutionary Anthropology, 9, 51–72.Google Scholar
  106. Wollstonecroft, M. M. (2011). Investigating the role of food processing in human evolution: A niche construction approach. Archaeological and Anthropological Sciences, 3, 141–150.Google Scholar
  107. Wollstonecroft, M. M., Ellis, P. R., Hillman, G. C., & Fuller, D. Q. (2008). Advances in plant food processing in the Near Eastern Epipalaeolithic and implications for improved edibility and nutrient bioaccessibility: An experimental assessment of Bolboschoenus maritimus (L.) Palla (sea club-rush). Vegetation History and Archaeobotany, 17, 19–27.Google Scholar
  108. Wollstonecroft, M. M., Ellis, P. R., Hillman, G. C., Fuller, D. Q., & Butterworth, P. J. (2012). A calorie is not necessarily a calorie: Technical choice, nutrient bioaccessibility, and interspecies differences of edible plants. Proceedings of the National Academy of Sciences of the United States of America, 109, 991–991.Google Scholar
  109. Wright, K. I. (1992). A classification system for ground stone tools from the Prehistoric Levant. Paléorient, 18, 53–81.Google Scholar
  110. Wright, K. I. (1994). Ground-stone tools and hunter-gatherer subsistence in Southwest Asia: Implications for the transition to farming. American Antiquity, 59, 238–263.Google Scholar
  111. Ydeman, E., Wickham, M., Faulks, R., Parker, M., Waldron, K., Fillery-Travis, A., et al. (2001). Beta-carotene release from carrot during digestion is modulated by plant structure. In W. Pfannhauser, G. R. Fenwick, & S. Khokhar (Eds.). Biologically-active phytochemicals in food (pp. 429–432). Norwich, Royal Society of Chemistry.Google Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of ArchaeologyMax Planck Institute for the Science of Human HistoryJenaGermany
  2. 2.Department of Human EvolutionMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  3. 3.Department of AnthropologyGeorgia State UniversityAtlantaUSA

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