YEARBOOK OF PHYSICAL ANTHROPOLOGY 156:43–71 (2015) To Meat or Not to Meat? New Perspectives on Neanderthal Ecology Luca Fiorenza,1* Stefano Benazzi,2,3 Amanda G. Henry,4 Domingo C. Salazar-Garcıa,3,4,5,6 Ruth Blasco,7 Andrea Picin,8,9,10 Stephen Wroe,11 and Ottmar Kullmer12 1Earth Sciences, University of New England, Armidale, NSW 2351, Australia 2Department of Cultural Heritage, University of Bologna, Ravenna 48121, Italy 3Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany 4Plant Foods in Hominin Dietary Ecology Research Group, Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany 5Department of Archaeology, University of Cape Town, 7700 Rondebosch, South Africa 6Department de Prehistoria i Arqueologia, Universitat de Vale`ncia, Valencia 46010, Spain 7The Gibraltar Museum, 18-20 Bomb House Lane, PO Box 939, Gibraltar 8Department of Prehistory and Early History, Friedrich Schiller Universitat€ Jena, Jena, 07743 Germany 9Neanderthal Museum, Mettmann, 40822 Germany 10Institut Catala de Paleoecologia Humana i Evolucio Social (IPHES), Tarragona, 43007, Spain 11Zoology, University of New England, Armidale, NSW 2351, Australia 12Senckenberg Research Institute, 60325 Frankfurt am Main, Hessen, Germany KEY WORDS zooarchaeology; stable isotopes; dental calculus; tooth wear; paleopathol- ogy; technology ABSTRACT Neanderthals have been commonly proteins that can be consumed: exceeding these values depicted as top predators who met their nutritional causes protein toxicity that can be particularly danger- needs by focusing entirely on meat. This information ous to pregnant women and newborns. Consequently, to mostly derives from faunal assemblage analyses and sta- avoid food poisoning from meat-based diets, Neander- ble isotope studies: methods that tend to underestimate thals must have incorporated alternative food sources in plant consumption and overestimate the intake of ani- their daily diets, including plant materials as well. Yrbk mal proteins. Several studies in fact demonstrate that Phys Anthropol 156:43–71, 2015. VC 2014 American Association there is a physiological limit to the amount of animal of Physical Anthropologists In this manuscript, we review traditional as well as nous group, with similar nutritional needs typified by a more recent approaches for reconstructing the diet in reliance on the consumption of terrestrial animals. This past human populations, and we show how new archaeo- idea was reinforced by the study of stable isotopes and logical discoveries and innovative methods are changing Neanderthal anatomy. The general robusticity of Nean- our views of Neanderthal ecology and behavior. We fur- derthal skeletons, with relatively short limbs and heavy ther underline the importance of reconstructing Nean- trunks, has been interpreted as adaptation to cold stress derthal environments derived from palaeoecological data environments that follow the ecogeographic principles of to better understand and interpret the dietary evidence Bergmann’s and Allen’s rules (e.g., Trinkaus, 1981; Ruff, obtained by these methods. Finally, since the intake of specific foods can be invisible to certain techniques and detect by others, we suggest using a more holistic Grant sponsor: Australian Research Council; Grant number: approach by integrating the findings of more than one DP140102659; Grant sponsor: the University of New England (UNE method. Such comprehensive analyses would enable the Research Seed Grant 2014); Grant sponsor: UNE Partnerships and University of New England (Career Development Award for Early reconstruction of the whole dietary spectrum, which is Career Researchers); Grant sponsor: German Research Foundation; particularly important for species like Neanderthal, who Grant number: FOR771, publication number 69; Grant sponsor: lived under severe and unstable climatic conditions. Beatriu de Pinos-A post-doctoral scholarship, Generalitat de Catalu- Neanderthals are undoubtedly the most studied and nya; Grant sponsor: European Union through Marie Curie Actions, best-known group in the human fossil record. Despite FP7; Grant sponsor: Spanish Ministry of Science and Innovation; that, for more than 100 years since their discovery, Grant number: CGL-BOS-2012-34717; Grant sponsors: Max Planck research on Neanderthal ecology, subsistence strategies, Society; Humboldt Postdoctoral Research Fellowship from the and diet have received remarkably little attention Alexander von Humboldt Foundation. (Ready, 2010). It is only with the emergence of new archeological disciplines and development of innovative *Correspondence to: Dr. Luca Fiorenza, Earth Sciences, Univer- analytical approaches in the 1960s, that scholars began sity of New England, Armidale NSW 2351 Australia. E-mail: lfi[email protected] to look at Neanderthal behavior and adaptations to their environment. Methods such as faunal analysis, lithic DOI: 10.1002/ajpa.22659 technology, and taphonomic studies progressively led to a Published online 19 November 2014 in Wiley Online Library general portrait that defined Neanderthals as a homoge- (wileyonlinelibrary.com). Ó 2014 AMERICAN ASSOCIATION OF PHYSICAL ANTHROPOLOGISTS 44 L. FIORENZA ET AL. Fig. 1. Neanderthal geographic distribution from human fossil remains (Reproduced with permission from Krause et al., Nature, 2007, 449, 902-904). 1994; Holliday, 1997). Yet, a number of traits, such as the opathology, tooth wear studies, and use of dental calcu- hyper-barrel-shape of the thorax, the thickened cortical lus. First, however, it is important to give a general bone and pronounced areas of muscle attachment, the introduction on Neanderthal geographic distribution, length of the calcaneus and the large nasal piriform with a focus on climate and vegetation in Eurasia during aperture, are thought to reflect extremely high levels of the Middle and Late Pleistocene. It will be followed by a physical activity (e.g., Trinkaus, 1986; Franciscus and discussion wherein we summarize this information, tak- Churchill, 2002; Weinstein, 2008; Raichlen et al., 2011). ing into account ecological variation among Neander- Such activity patterns, together with the physiological thals and include nutrition and pathology-based stress induced by cold climates, would have imposed arguments for a diet rich in animal proteins. significant high-energy demands on Neanderthal bodies (Sorensen and Leonard, 2001; Steegmann et al., 2002; NEANDERTHAL WORLD: GEOGRAPHIC Churchill, 2006): metabolic requirements that would DISTRIBUTION, CLIMATE AND VEGETATION have forced Neanderthals to consume an energy-rich diet. Support for this argument mostly derived from Owing to the inexorable links between a habitat and stable isotopic analyses (e.g., Richards and Trinkaus, its organisms (e.g., species of animals and plants), an 2009), which suggested that Neanderthals obtained assessment of Neanderthal subsistence patterns requires nearly all of their dietary proteins from animal sources, an overview of the environments in which they lived. and occupied the higher level of the food trophic web, Neanderthals occupied western Eurasia, a wide geo- similar to the top-level carnivores of that time. The tra- graphic area ranging West from the Iberian Peninsula ditional interpretation of Neanderthals as exclusively East to Siberia (Krause et al., 2007), and North from meat-eaters, has, however, been challenged on several Germany South to the Levant (e.g. McDermott et al., fronts over recent decades. Mounting evidence suggests 1993; Wolpoff, 1996) (Fig. 1). that the nitrogen isotope record may underestimate the This region encompassed considerable topographical consumption of starch/carbohydrate rich plant foods by heterogeneity (e.g., interior and coastal areas, mountain- humans (Ambrose et al., 2003; Hedges and Reynard, ous or relatively flat terrains), soil composition, and varia- 2007; Sponheimer and Lee-Thorp, 2007). More impor- tion in temperature humidity, largely influenced by tantly, analyses of new archaeological evidence from latitude. Besides that, Neanderthals are mostly docu- the Mediterranean coastlines of Southern Europe and mented from marine isotope stages (MIS) 6 through 3, a the Near East, dental wear studies, and microfossils in long period of time characterized by severe climatic condi- calculus, have demonstrated that Neanderthals were tions, with alternating glacial/interglacial cycles. This exploiting a wide variety of food sources (e.g. Stringer wide geographic distribution and climatic fluctuations et al., 2008; El Zaatari et al., 2011; Fiorenza et al., during the Middle and Late Pleistocene drove the forma- 2011a; Henry et al., 2011; Salazar-Garcıa et al., 2013; tion of diverse and discontinuous environments, spanning Sistiaga et al., 2014). This unexpected dietary complex- from warm and forested to cold and open habitats. Chang- ity, coupled with a very wide temporal and geographic ing climate also strongly influenced the distribution pat- range, has led many to reconsider the ecology and for- terns of mammalian herbivores and other food sources aging strategies of Neanderthals. forcing Neanderthals to adapt to the new conditions. To accomplish this task, here we review some tradi- The Mid-Late Pleistocene was marked by a general tional, as well as innovative approaches used in the increase in aridification, but also great instability, with reconstruction of Neanderthal diets, such as lithic and episodes of maximum ice expansion characterized by cold, zooarchaeological analyses,