Dietary Inferences Through Dental Microwear and Isotope Analyses of the Lower Magdalenian Individual from El Miron Cave (Cantabr

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Journal of Archaeological Science 60 (2015) 28e38

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Dietary inferences through dental microwear and isotope analyses of the Lower Magdalenian individual from El Miron Cave (Cantabria, Spain)

* Rebeca García-Gonzalez a, , Jose Miguel Carretero a, b, Michael P. Richards c, d, Laura Rodríguez a, e, Rolf Quam b, f, g a Laboratorio de Evolucion Humana, Departamento de CC, Historicas y Geografía, Facultad de Humanidades y Educacion, Universidad de Burgos, C/ Villadiego s/n, 09001 Burgos, Spain b Centro UCM-ISCIII de Investigacion sobre la Evolucion y Comportamiento Humanos, Avda. Monforte de Lemos, 5, 28029 Madrid, Spain c Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany d Laboratory of Archaeology, Department of Anthropology, University of British Columbia, Vancouver, Canada e Centro Nacional de Investigacion sobre la Evolucion Humana (CENIEH), Paseo Sierra de Atapuerca s/n, 09002 Burgos, Spain f Department of Anthropology, Binghamton University (SUNY), Binghamton, NY 13902-6000, USA g Division of Anthropology, American Museum of Natural History, Central Park West @ 79th St., New York, NY 10024-5192, USA article info abstract

Article history: Dietary habits are inferred from dental microwear and isotope analyses of the Magdalenian human in- Available online 27 March 2015 dividual from the site of El Miron, dated to 15,460 ± 40 BP. The pattern of dental microwear was established on the buccal surface of the lower fourth premolar and on the bottom of facet 9 on the Keywords: occlusal surface of the lower third molar. The results obtained through analysis of different surfaces are Hunteregatherer diet consistent and indicate a mixed diet for this Lower Magdalenian individual, including meat, aquatic Hominin resources and vegetables. These results are in agreement with those obtained through isotope analysis. Dental microwear This implies a generalized exploitation of the environment as has been previously established in other Upper Paleolithic El Miron Cave Late Upper Palaeolithic specimens. © Cantabrian Spain 2015 Elsevier Ltd. All rights reserved.

1. Introduction primates (Gordon, 1982; Teaford and Walker, 1984; Teaford and Oyen, 1989; Teaford and Robinson, 1989; Ungar, 1994), dietary Dietary reconstruction is an important class of analysis in habits in fossil hominins (Puech, 1983; Puech et al., 1983a; Puech paleoanthropology, since diet influences a number of human be- et al., 1986; Grine, 1986; Ryan and Johanson, 1989; Ungar and haviors, including, such things as mobility patterns or social orga- Grine, 1991; Lalueza et al., 1993, 1996; Perez-P erez et al., 2003; nization (Clutton-Brock and Harvey, 1977). This kind of study can be Grine et al., 2006; Estebaranz et al., 2009) and subsistence strate- addressed through isotope and dental microwear analysis. Isotopic gies in both prehistoric and recent humans (Bullington, 1991; analysis is able to determine diet through the Carbon and Nitrogen Molleson and Jones, 1991; Molleson et al., 1993; Perez-P erez isotope ratios (Richards and Hedges, 1999; Richards et al., 2000, et al., 1994; Ungar and Spencer, 1999; Schmidt, 2001; Romero 2001; García-García et al., 2009). et al., 2004; Teruyuki, 2005; Mahoney, 2006a,b, 2007; Hogue and Dental microwear analysis has proven to be a useful technique Melsheimer, 2008; Kruege and Ungar, 2009; Gamza and Irish, with which to characterize diet-related adaptations in non-human 2012; Romero et al., 2013; El-Zaatari and Hublin, 2014). These studies are based on the relationship between dental microwear patterns and the general types of foods upon which an organism relies (Schmidt, 2001). The analysis of these patterns can be carried * Corresponding author. Laboratorio de Evolucion Humana, Edificio IþDþi, Uni- out through the study of occlusal or buccal surfaces. ~ versidad de Burgos, Plaza Misael Banuelos s/n, 09001 Burgos, Spain. Occlusal microwear is affected by both abrasion and perhaps E-mail addresses: [email protected] (R. García-Gonzalez), [email protected] e (J.M. Carretero), [email protected] (M.P. Richards), [email protected] tooth tooth wear. Thus, it yields a surface with pits and scratches. (L. Rodríguez), [email protected] (R. Quam). Scratches are formed by particles such as grit, dust and phytoliths http://dx.doi.org/10.1016/j.jas.2015.03.020 0305-4403/© 2015 Elsevier Ltd. All rights reserved. R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38 29 adhering to the food, while pits are caused by tooth-to-tooth 2. Material contact. Thus, hard diets, which are reflected by an increase in compression forces, produce frequent and large pits (Gordon, This study is based on the analysis of teeth from the human 1982; Teaford and Walker, 1984; Teaford and Oyen, 1989; mandiblerecovered from El Miron Cave. Dental microwear analysis Teaford and Runestad, 1992; Mahoney, 2006a,b). However, a diet was performed in the lower right fourth premolar (P4) and lower rich in tough foods requires an increase in shear, producing left third molar (M3) from the human mandible. Lower first (M1) numerous long and narrow scratches (Gordon, 1982; Teaford and and second (M2) molars were excluded from the study because Walker, 1984; Teaford, 1988; Walker and Teaford, 1989; Ungar they showed a high degree of dental wear (see Carretero et al., and Spencer, 1999; Mahoney, 2006a,b). In addition, the pattern 2015). Stable isotope analysis was carried out on collagen extrac- of microwear can be altered by other agents, such as chewing ted from the bone as part of the radiocarbon dating process for the biomechanics, age and size of abrasive particles (Bullington, 1991; El Miron individual. Mahoney, 2006b,c). Microwear data for comparative purposes were obtained from On the other hand, buccal microwear is only affected by abra- different bibliographic sources. For the P4, these data were sion; thus, pits are rarely formed (Puech and Pant, 1980; Perez- extracted from Lalueza et al. (1996), who analyzed the buccal sur- Perez et al., 1994; Ungar and Spencer, 1999). The variables face of the P4,M1 and M2, either mandibular or maxillary, in ten analyzed in this case are the density and orientation of the striae different samples. Although our data come from a lower P4, com- (Perez-P erez et al., 1994; Lalueza et al., 1996). The number of parisons with data provided by Lalueza et al. (1996) are possible buccal striation depend on the abrasive particles present in the since the intra-individual variation is smaller than the inter- food, such plant phytoliths, sand or ash, while the length of the individual variation (Perez-P erez et al., 1994). The different striation may depends on other additional factors, such the pres- comparative samples are sorted into four dietary groups: 1) agri- sure applied by the chewing muscles (Perez-P erez et al., 1994). culturalist group, which is characterized by an exclusively vege- Studies on fossil hominins have suggested that vertical scratches tarian diet; 2) hunteregatherers from tropical environments, should become longer and more frequent in meat-eating pop- showing a diet with a higher intake of vegetable foods than that of ulations, while horizontal ones should be more abundant and meat; 3) carnivorous hunteregatherer and pastoralists, whose diet longer in a diet with a high consumption of vegetables (Puech, is mainly based on meat and 4) hunteregatherers from arid envi- 1978, 1979; Puech and Pant, 1980; Puech, 1983; Puech and ronments, with a mixed diet. Albertini, 1981; Puech et al., 1980, 1983a,b, 1986). Subsequent In the case of the M3, comparative data have been limited to the research has shown that the indices of relative frequency of bottom of facet 9 (located toward central fossa of the distobuccal scratches (categorized by their orientation) are more informative cusp) on second and third lower molars, because there is a high about dietary habits (Perez-P erez et al., 1994; Lalueza et al., 1996; intra-individual variation between teeth and in the location of the Perez-P erez et al., 1999). wear facet (Mahoney, 2006a,b,c). Occlusal microwear data of The selection of the tooth surface to study depends on the type comparative collections were obtained from Mahoney (2007), who of information desired, although a recent study demonstrated provides both summary statistics and raw data for each group. The that, at least in Australopithecus afarensis, buccal and occlusal samples used by Mahoney (2007) included those from four pre- microwear analysis offers consistent results (Estebaranz et al., historic human groups belonging to different archaeological pe- 2009). There are two main factors to bear in mind for making riods in the southern Levant, plus two molars from the late Upper this choice. First, it is important to note that meat consumption is Paleolithic Ohalo II site. The prehistoric groups are: Natufian hard to infer through the occlusal microwear pattern (Mahoney, hunteregatherers, early Pre-Pottery Neolithic people from Sultain 2007). And secondly, both the formation dynamic and overall sites (PPNA), Pre-Pottery Neolithic hunters and farmers (PPNB) and turnover rate shown in these two surfaces are clearly different Chalcolithic farmers. From this four, two dietary sets can be (Teaford and Oyen, 1989; Perez-P erez et al., 1994; Romero et al., established: one with a hard diet (Natufian and PPNB samples) and 2007). The turnover rate is faster on the occlusal surfaces than the other with a softer diet (PPNA and Chalcolithic samples). on the buccal ones, so the dental microwear pattern in the former is more susceptible to the “last supper effect” (Perez-P erez et al., 3. Methods 1994; Romero and De Juan, 2007; Romero et al., 2007, 2012). Therefore, analysis of microwear features on buccal surfaces 3.1. Imaging procedure provides information about dietary habits over a relatively longer period of time, while the interpretation of these features on The two teeth from El Miron were imaged directly using an occlusal surfaces should reflect seasonality of food resource environmental scanning electron microscope (ESEM) JEOL JSM- exploitation (Rivals and Deniaux, 2005, Rivals et al., 2009a,b; 6460LV in lower vacuum mode. The use of ESEM in physical an- Merceron et al., 2010). thropology is growing, as it eliminates the necessity of casting Thus, to obtain more complete dietary inferences through procedures. Although this is a great advantage, it is important to dental microwear patterns, both buccal and occlusal analyses point out that this technique presents some limitations. The most should be integrated. In this sense, the main goal of the present important is the “skirt effect” which adversely affects the spot size study is to make dietary inferences through dental microwear (Timofeeff et al., 2000). The spot size is a dimensionless magnitude patterns on buccal and occlusal surfaces of the partial human which measures the probe current (i.e., the current that impinges skeleton recovered from a Lower Magdalenian context in El Miron upon the specimen and generates the imaging signals). In the ESEM Cave. These results are compared with those obtained through used in this study, the spot size varies between 0 and 99 (0 implies a stable isotopic analysis. minimum probe current and 99 a maximum one). The skeleton from El Miron Cave is referred to as the “Red Lady” Several procedures can be used to minimize this effect, because the bones were stained with ochre (for a complete including maximizing the relationship among working distance, anthropological study, see Carretero et al., 2015). It has been accelerating voltage, pressure and brightness and contrast levels directly dated to 15,460 ± 40 BP, which, together with the strati- (Timofeeff et al., 2000; Kirk et al., 2009). graphic position and the associated archaeological material, place it Although these cautions were all taken into account, spot size in the Lower Cantabrian Magdalenian (Straus et al., 2011, 2015). for images used in this study were clearly larger (between 66 and 30 R. 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73) than those which are frequently used. Nonetheless, the quality Finally, we deﬁne a new variable, pit size, as the product of geo- of the images is sufﬁcient to carry out a quantitative approach metric mean of pit width and length. based on dental microwear features (Fig. 1). 3.3. Analysis of buccal microwear pattern

3.2. Data collection In order to infer dietary habits in the Red Lady, two different approaches were carried out. First, microwear features measured fi In the case of P4, digitized micrographs of the buccal surface on the buccal surface of the P4, were entered into the rst two were taken at a magnification of 100. To ensure compatibility discriminant functions (DF) calculated previously by Lalueza et al. with other studies, these measurements were taken in a selected (1996). These DFs provide good discriminant power among the area of 0.56 mm2 (Perez-P erez et al., 1999). The length and angles of four basic dietary groups mentioned above. all scratches were measured using Adobe Photoshop™ software The DF combines a number of variables, and its application al- using specific tools for taking linear and angular measurements. lows us to assign an unclassified case to a defined group (Gil-Flores First, the boundaries of each microwear feature were established. In et al., 2001). To classify a new case, it must preserve values for the order to avoid bias in the recognition of these boundaries, digitized all different variables that were entered into each DF, and thus the micrographs were previously processed with the high pass filter scores are obtained. These DF scores are used to place the unclas- available in the Adobe Photoshop™ software. This filter expands sified case in one of the groups. Since Lalueza et al. (1996) provide the gray levels, facilitating the identification of the ends in each the coefficients of these DF, we can calculate the scores attained by microwear feature. Negative angles were transformed into positive these two functions, and the corresponding classification for El ones, by adding 180. All observed scratches were classified by Miron. However, it is not possible to determine the posterior categories of orientation, following recommendations of Perez- probabilities that the Miron individual belongs to one of the four Perez et al. (1994, 1999). These categories are: vertical (V), mesio- dietary groups since we do not have the raw data from the sample occlusal to disto-cervical (MD), disto-occlusal to mesio-cervical the DF is based on. Thus, the classification of El Miron is based only (DM) and horizontal (H). The inclusion of the scratches on one of on the obtained discriminant scores. these categories depends on the orientation of the striation and the We have calculated the discriminant scores for the Miron indi- position of the tooth. As in our case, the studied tooth was a lower vidual for the first and second functions proposed by Lalueza et al. right fourth premolar the values for each categories were: V (1996). These two functions were created from the number of hori- (67.5e112.5), MD (22.5e67.5), DM (112.5e157.5) and H zontal scratches, the number of mesio-occlusal to disto-cervical (0e22.5 and 157.5e180). scratches, the standard deviation of the length of disto-occlusal to For each category, the following three summary variables were mesio-cervical striae, the mean of the length of the total striations, the calculated: number (N), mean (X) and standard deviation of the standard deviation of the length of all the striations, the length (STD). In addition, three indices were calculated: the num- standard deviation of the length of vertical scratches, the mean of the ber of vertical and horizontal scratches divided by the total number length of the horizontal scratches and the total number of of striations (NV/NT and NH/NT) and the number of horizontal striations. The first function was: 0.11364*NH 0.03017*NMD striations divided by the vertical ones (NH/NV) (Perez-P erez et al., 0.00169*STDDM 0.01485*XT þ 0.00958*STDT -0.00468 1994, 1999; Lalueza et al., 1996). *STDV þ 0.00454*XH þ 0.00203*NT þ 0.06819. It explains 66.70% of For the M3, the occlusal surface was imaged, and, specifically, the variance and has a canonical correlation of 0.8093. The second one the bottom of facet 9 has been imaged at 500 (Mahoney 2006a,c). was: 0.05361*NH þ 0.09573*NMD þ 0.00730*STDDH 0.01340 Four different micrographs were taken in adjacent locations in the *XT 0.00922*STDT þ 0.01098*STDV þ 0.00061*XH þ 0.03253 bottom of facet 9. Pits and scratches were measured and counted *NT 0.42014, accounting for 26.84% of the total variance and has a using the same software as in the case of the P4. A 4:1 ratio was canonical correlation of 0.6581. chosen to distinguish between these two microwear features The scores attained for El Miron individual were subsequently (Mahoney, 2006a,b,c). The variables analyzed were, frequency or placed on the scatterplot of the discriminant functions proposed by percentage of pits, mean length and width of pits and scratches. Lalueza et al. (1996), in order to know if this specimen is included within the 95% equiprobability ellipses of the four dietary groups. In addition, we compare the scores obtained for El Miron individual with those attained for different human fossils (which have been classified in one of these four dietary groups) to establish the most probable diet (based on buccal microwear) of the Red Lady. The second approach was based on the indices of relative frequency of striations by orientation, because these indices provide information about dietary habits (Perez-P erez et al., 1994; Lalueza et al., 1996). For this reason, the relationships between the NH/NT and NV/NT indices were compared among the El Miron individual and the four previously mentioned dietary groups.

3.4. Analysis of occlusal microwear pattern

In the case of the occlusal surface of M3, univariate, bivariate and multivariate analyses were carried out. First, considering the frequency of pits, as well as the length and width of both pits and scratches, can provide insights into the orientation of the forces applied during the chewing cycle, individual values for these variables taken in El Miron were compared with those from four Fig. 1. Microwear on the buccal surface of the El Miron P4. comparative samples derived from Mahoney (2007). These R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38 31

Table 1 Number, length and variation of microwear striations on the buccal surface of the P4 from El Miron.

DM Horizontal MD Vertical Total

N X STD N X STD N X STD N X STD N X STD

P4 4 55.8 25.1 8 110.8 60.8 54 79.3 50.4 78 94.3 45.8 144 88.5 48.7 N: Number of striations, X: Mean length of striations in micrometers, STD: Standard deviation of length of striations in micrometers. DM: Striations with a disto-occlusal to mesiocervical orientation, MD: Striations with a mesio-occlusal to distocervical Orientation. comparisons were carried out through standard scores (Z-scores). the diet of the individual. As this was undertaken at the end of the The Z-score is the number of standard deviations a datum is above/ project, it was not possible to also sample fauna from the burial, below the mean and it is calculated as the datum minus the which would be useful to provide the isotopic baseline needed to reference mean divided into the standard deviation of the reference fully interpret the human isotope values. This is of particular rele- sample. In this way, we have calculated a different Z-score for each vance here, since a large fluctuation in faunal baseline values, variable and relative to each comparative sample, considering especially nitrogen isotope values, has been reported for this time values below or above 1.96SD statistically significant (Sokal and period (Richards and Hedges, 2003). Therefore, we provide only a Rolf, 1979). preliminary interpretation of the human values and must await a To calculate Z-scores, the raw data for each variable must follow full faunal isotope analysis to make a more definitive statement a normal distribution. Since all variables failed this assumption, about the diet. they were transformed. In the case of percentages of pits, we have used an arcsine transformation, and for the length and width of 4. Results both pit and scratches data were log-transformed (Sokal and Rolf, 1979). The normality of the distribution of transformed data was 4.1. Buccal microwear analysis cheeked by ShapiroeWilk's test. In no case was the null hypothesis that the population is normally distributed rejected (p-values were Descriptive statistics for dental microwear features of the Miron 0.14; 0.06; 0.24; 0.18 and 0.6 for the arcsine transformed percentage P are provided in Table 1. of pits, length and width of pits and length and width of scratches, 4 Based on these variables, we can infer that the buccal microwear respectively). pattern consists of striations of different lengths and with mainly The second approach is focused on the relationship among vertical orientations, but also with others showing a disto-occlusal different microwear variables. We have focused on the relationship to mesiocervical orientation. between pit size and the percentage of pits, on the one hand, and When these microwear measurements were entered into the scratch width and pit size, on the other. Pit size and percentage of first two discriminant functions calculated by Lalueza et al. (1996), pits can be analyzed together, since both are related to hardness of the discriminant scores obtained for the Red Lady were 0.96 for the diet (Molleson et al., 1993; Mahoney, 2007), while scratch the first function and 8.12 for the second one. These scores place width and pit size reflect the size of abrasive particles (Mass, 1994; this specimen well outside of the 95% equiprobability ellipses of the Schmidt, 2001; Mahoney, 2007). four dietary groups considered by Lalueza et al. (1996) (Fig. 2). The analysis of these associations was carried out through In Fig. 3, the relative frequencies of vertical and horizontal Pearson's correlation coefficients. If the relationship was statisti- striations are plotted against one another. The low number of cally significant and strong enough (R2 0.60), a regression equation was constructed and a residual analysis was performed based on the comparison of the standardized residuals. A standardized residual is defined as the real value minus the predicted value for the regression equation, divided by the standard deviation of the regression (Sokal and Rolf, 1979). A negative standardized residual implies that the real value of the specimen falls below the value predicted by the regression equation, while a positive standardized residual indicates the opposite. In those cases where the correlation coefficient was low (R2 < 0.60) and/or not statistically significant, a visual inspection of the scatterplot distributions was carried out. Finally, Discriminant Function Analysis (DFA) was performed using the raw data published by Mahoney (2007). These data were transformed in order to fit to a normal distribution (see above). Our results with this analysis of comparative samples are similar to those obtained by Mahoney (2007), and both the discriminant scores and the posterior probability of belonging to any particular group can be calculated for the El Miron specimen.

3.5. Dietary inferences through isotope analysis

Collagen was extracted from the bone using methods outlined in Fig. 2. Discriminant function analysis of four dietary groups based on microwear measurements taken on the buccal surface of the P (modiﬁed from Lalueza et al., Straus et al. (2015). 4 1996) and the position of the El Miron specimen. Black lines represent the 95% equi- Subsequently, the carbon and nitrogen isotope ratios of the probability ellipses of each dietary group and solid black circles the centroid of each extracted collagen were measured in order to have an indication of ellipse. Solid gray circle: El Miron specimen. 32 R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38

Fig. 3. Plot of NH/NT index vs NV/NT index for four dietary groups (modiﬁed from Lalueza et al., 1996) and the El Miron specimen. Black lines represent the 95% equiprobability ellipses of each dietary group and solid black circles the centroid of these ellipse. Solid gray circle: El Miron specimen. horizontal striations and the high number of vertical ones in the Red Lady show the closest similarity with the carnivorous group.

4.2. Occlusal microwear analysis

The dental microwear variables taken on the occlusal surface of the M3 from El Miron are provided in Table 2. Fig. 4 shows the Z-score profiles of the dental microwear variables for M3 from El Miron relative to the comparative samples mean. Fig. 4. Z-scores profile of six dental microwear variables taken on the bottom of facet 9 As seen in Fig. 4, the M from El Miron shows a low percentage 3 of the M3 from El Miron relative to the comparative samples. Diamond: Natufian of pits, especially relative to Natufians and PPNB people, but also samples, Square: PPNA sample, Triangle: PPNB sample, Circle: Chalcolithic sample. when compared with PPNA and Chalcolithic humans. Nevertheless, Data for the comparative samples from Mahoney et al. (2007). Discontinuous lines this pit density is more similar to the Ohalo II molars (Mahoney, indicate those values placed below/above 1.96 SD. 2007). El Miron exhibits pits whose length and width do not differ statistically from those of the Natufian and Chalcolithic The scratches are narrower than both Natufian samples. However, these pits are significantly longer than those of hunteregatherers and PPNB farmers, but these differences are only the PPNA, but shorter than those of the PPNB period. Regarding the statistically significant in the case of the PPNB. The scratch width in width of the pits, the mean value for this microwear feature in El the Red Lady is 1.3 SD below the Natufian mean and 1.3 SD above Miron is markedly lower than those displayed by PPNA and Chal- the mean of both PPNA and Chalcolithic samples (Fig. 4). Thus, colithic people. According to the length and width of the pits, the although the width of the scratches on the occlusal surface of the pit size of the Red Lady is quite similar to the Natufian sample mean M3 from El Miron is well within the Natufian, PPNA and Chalcolithic (z-score ¼0.5) and 1.5 SD below of the PPNB mean. However, this ranges of variation, this value is at the lower end of the Natufian value is very high when compared with both the PPNA and the range of variation, as well as being at the upper limit of the range of Chalcolithic sample means.

Table 2 Microwear measurements on the occlusal surface of the M3 from El Miron. All measurements in micrometers, except percentage of pits.

Miron Number of features % Pits Pit length Pit width Scratch length Scratch width

Pits Scratches x sd x sd x sd x sd x sd

a M3 24 112 21.3 3.0 1.6 2.1 1.2 29.2 17.6 1.1 0.4 a M3 20 170 11.7 4.2 2.1 2.6 1.7 35.2 26.9 1.3 0.5 a M3 26 124 20.9 3.4 1.7 2.8 0.4 23.6 19.4 0.9 0.4 a M3 25 173 14.4 3.8 1.6 1.7 0.5 17.7 14.3 1.1 0.4 Meanb 23.7 144.7 17.1 4.8 3.6 1.7 2.3 0.9 26.4 19.5 1.1 0.4

a Measurements from four micrographs. b Mean value from four micrographs. R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38 33

Fig. 6 shows the relationship between scratch width and pit size. It is important to note that there is a positive correlation across the entire sample (adjusted R-squared ¼ 0.68; p 0.01), suggesting that these two microwear features may reflect similar causal agents (Mahoney, 2007). In this case, the El Miron specimen falls within the range of variation of the Natufian and PPNB samples, but closer to those specimens showing smaller pits and narrower scratches. In fact, the residual analysis indicates that this value is closer to those shown by the Chalcolithic sample, but inside the range of this sample and the PPNA (Fig. 7). Finally, when the El Miron specimen was entered into the DFA as an unassigned individual, the resulting discriminant scores were 0.783 and 0.665 for the first and second functions respectively. These scores placed the Red Lady in an intermediate position between those samples with a hard diet and those with a soft one, falling inside the 95% equiprobability ellipses of Natufian, Chalcolithic and PPNA samples (Fig. 8). In fact, it was not classified into either of the two hard diet groups (Natufian hunteregatherers Fig. 5. Pit size plotted against the percentage of pits in comparative samples and the and PPNB farmers), and the probabilities of belonging to PPNA and Ohalo II and El Miron specimens. Black continuous and discontinuous lines: 95% Chalcolithic samples are very low (P ¼ 38% and P ¼ 32%, respec- fi equiprobability ellipses of Natu an and PPNB samples, respectively. Gray continuous tively). Therefore, the El Miron specimen cannot be classified and discontinuous lines: 95% equiprobability ellipses of PPNA and Chalcolithic samples. Open circles represent the centroid of the ellipses. clearly into any one group, since it showed a peculiar microwear pattern, consisting of frequent narrow and short scratches and few intermediate-size pits. the mean of PPNA and Chalcolithic samples. Although scratches are wider in El Miron than in the PPNA and Chalcolithic, these differences do not reach statistical significance. 4.3. Isotope analysis Regarding the length of the scratches, the Red Lady value is only 0.5 SD and 0.1 SD above the mean of the Natufian and PPNB sam- The extracted collagen had preservation characteristics consis- ples, but it is well below that of the PPNA sample (Fig. 4). tent with well preserved collagen (DeNiro, 1985) with a C:N ratio of 13 Fig. 5 compares the percentage of pits with pit size in the 3.2 and a collagen yield of 3.2%. The d C value was 18.2‰ and the ‰ comparative samples, the Ohalo II specimens and the El Miron M3. 15 N value was 10.2 . In the absence of a faunal baseline, a pre- For the pit size, the El Miron individual is well above the means for liminary interpretation of this result would indicate a likely regular the PPNA and Chalcolithic samples, but it is just within the range of input of some marine protein into the diet of this individual. the latter group. However, it is outside the limits of the 95% equi- Assuming that for this time period the end point values for 100% probability ellipses of the PPNB and Natufian samples. This is also terrestrial diets and 100% marine diets are 20‰ and 12‰, true for the Ohalo II Epipaleolithic specimens, although their means respectively, this would indicate a diet where approximately 20% of are closer to the Chalcolithic group than that of El Miron. These the dietary protein came from marine sources. The slightly elevated findings show that, when pit size is considered separately, the El nitrogen isotope value is consistent with this interpretation, Miron specimen does not differ from Natufian and PPNB samples, although, as noted below, the nitrogen isotope value is identical to a but in relative terms, this value is closer to the Chalcolithic sample. contemporary human that does not have carbon isotope values indicating a marine dietary input. Nevertheless, this interpretation is consistent with the presence of abundant salmon remains in the

Fig. 6. Scratch width plotted against the pit size in comparative samples and the Ohalo II and El Miron specimens. Open squares: Natuﬁan samples, Diamonds: PPNA sample, Triangles: PPNB samples, Open circles: Chalcolithic samples; Solid square: El Miron specimen; Solid circles: Ohalo II specimens. Continuous line: Regression line calculated Fig. 7. Mean and range (no-outliers) from the standardized residuals for each based on the entire sample (Scratch width ¼ 0.29 þ 0.81*pit size; adjusted R2 ¼ 0.68; comparative sample and the El Miron specimen. Squares represent the mean and the p ¼ 0.01; SD of estimate ¼ 0.23). bars the (no-outlier) range. 34 R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38

and given the vast area of the continental shelf off northern Aqui- taine that was still dry land during the Oldest Dryas versus the narrow strip of dry land off Cantabria.

5. Discussion and conclusions

The results obtained through dental microwear analysis on the buccal surface of the P4, show that the abrasiveness of the diet in the El Miron individual was more similar to that displayed for tropical hunteregatherers than the other dietary groups. However, it is important to note that the Red Lady falls outside of the 95% equiprobability ellipse of this group (Fig. 2). This is due to the very high score provided by the second discriminant function for the El Miron specimen. As Lalueza et al. (1996) established, this function is highly correlated with the total number of striations and is negatively correlated with the length of all the striations. The total number of striations showed by the Red Lady's P4,is Fig. 8. Plot of the two first functions of the Discriminant Analysis carried out on well above those presented by all comparative groups used to microwear variables taken on the occlusal surface of the M3. Function 1 was calculated generate the discriminant function (Fig. 9). However, this value is from pit length, scratch width and pit width and function 2 from scratch length and quite similar to that exhibited by the Banyoles (Neandertal) and percentage of pits (see Mahoney, 2002, for further details). The black continuous and Abri-Pataud (Gravettian-age modern human) fossils (NT ¼ 145, discontinuous lines represent the 95% equiprobability ellipses of Natufian and PPNB ¼ samples, respectively. Gray continuous and discontinuous lines: 95% equiprobability NT 139 respectively; in Lalueza et al., 1996). ellipses of PPNA and Chalcolithic samples. Open circles represent the centroid of the The Banyoles individual was clearly classified as a hunter- ellipses (black: Natufian and PPNB samples, gray: PPNA and Chalcolithic samples). egatherer from an arid environment group with a posterior prob- Solid square: El Miron specimen, solid circles: Ohalo II specimens. ability of 98.13%, while the Upper Paleolithic early modern human from Abri Pataud is located within the two mixed-diet groups Lower Magdalenian levels in El Miron (García Leaniz and (64.12% posterior probability to belong to the tropical hunter- Consuegra, 2001). egatherer group and 35.88% posterior probability to belong the Although there are human isotope values for Gravettian (i.e., arid hunteregatherers) (Lalueza et al., 1996). The main difference 30,000 to 20,000 BP, Richards and Trinkaus, 2009) and Late Upper between these two fossils lies in the score for the first discriminant Paleolithic (13,000 to 12,000 BP, Richards, 2009) individuals from function, which is highly correlated with the number of horizontal other regions of Europe, there is only one individual, an adult fe- striations. The number of horizontal striations showed by Banyoles male from Saint-Germain-la-Riviere (France), with a direct radio- (NH ¼ 45) is quite different than that presented by Abri-Pataud carbon date and isotope values from the same time period as Miron (NH ¼ 26) (Lalueza et al., 1996). This distinction is responsible for (Drucker and Gambier, 2005). This individual dates to the classification of the first specimen among the tropical hunter- 15,780 ± 200 uncal. BP (essentially contemporary with the El Miron egatherers, while the latter is included in the hunteregatherer 13 15 individual) and the isotope values are d C 19.2‰ and d N 10.2‰. from arid environments. The Saint-Germain-la-Riviere individual has a more terrestrial The number of horizontal striations on the buccal surface of the isotope value than El Miron. This might be expected since this in- El Miron specimen is low (NH ¼ 8) and well below both Banyoles dividual is from a somewhat more inland location than El Miron, and Abri-Pataud. However, it is comparable to that exhibited by La

Fig. 9. Total number of striations on the buccal surface of P4 on comparative samples and El Miron specimen. Comparative samples are derived from Lalueza et al. (1996) and are sorted by dietary group. Squares represent the mean and lines the range including ± 1SD. R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38 35

Chaise Suard, Qafzeh 9, La Quina V and Amud 1 Neandertals this, since a high density of striations might be indicative of the (NH ¼ 9, 9, 7 and 6, respectively) (Lalueza et al., 1996). The highest inclusion of plant foods in the diet (Perez-P erez et al., 2003). posterior probabilities for all these specimens classified them as Nevertheless, it is important to remember that total number of belonging to the tropical hunteregatherers group. striations and their lengths are related to the abrasiveness of the In the same way, the mean of the striation lengths for the El diet (Perez-P erez et al., 1993; Lalueza et al., 1996). Thus, these Miron specimen is lower than those presented by all modern findings only reveal that the diet of the Red Lady was as abrasive as samples, although very close to those showed by the arid hunter- that of the tropical hunteregatherers group. egatherer groups (Fig. 10a). However, the Red Lady and the African The results from the relative frequency of scratches by orien- Middle Pleistocene Broken Hill individual exhibit striations whose tation, indicate a diet based mainly on meat. The apparent mean length is comparable (Fig. 10b). The Broken Hill specimen is contradiction between this result and that obtained from the DFA, classified in the tropical hunteregatherer group with a chance of could be due to the fact that the buccal microwear pattern of El 99.92%. Miron specimen does not correspond to that shown by the Thus, considering all of the data, we could infer that the diet for comparative samples (Perez-P erez et al., 2003). Although there the El Miron individual was equivalent to that of hunteregatherers were no significant differences in the diet composition between the from tropical environments. This group shows a diet with a higher Red Lady and the most carnivorous groups, the former shows a intake of vegetables than meat (Lalueza et al., 1996). Based on this, more abrasive microwear pattern. However, we must bear in mind we could infer that the buccal microwear pattern in the Red Lady that this mismatch could be also due to the fact that we are was due mainly to a mixed diet including more resources from studying a single individual, and discordances within an individual gathering than hunting. The high number of striations supports in the dietary inferences are not uncommon. A larger sample of

Fig. 10. Comparison of length of total number of striations among the El Miron specimen and modern comparative samples (a) and fossil specimens (b). Modern and fossil samples are from Lalueza et al. (1996). EM: El Miron, Mt: Montmaurin, Bh: Broken Hill, LCHS: LA Chaise Suard, ChB: La Chaise Bourgeois-Delauney, Mr: Marillac, LQV: La Quina V, T2: Tabun 2, S4: Skhul 4, Q9: Qafzeh 9, LM: La Madeleine, VS: Veyrier-sous-Saleve, AP: Abri-Pataud, A1: Amud 1, Ba: Banyoles, Ml: Malarnaud, SC: St. Cesaire, Cm: Cro-Magnon, RdB: Rond-du Barry, T1: Tabun 1, G2: Gibraltar 2. Squares represent the mean and lines the range including ± 1SD. Discontinuous lines in Fig. 10a separate the different dietary groups. 36 R. García-Gonzalez et al. / Journal of Archaeological Science 60 (2015) 28e38 individuals from El Miron may reveal a more consistent patterning, If this is the case, we could infer that the Red Lady would have with fewer contradictions across the sample. consumed hard foods occasionally and her diet mainly consists in The mismatch between the P4 microwear pattern of the El tough foods. Miron specimen and that showed by other fossil specimens also Another possible explanation for this question arises with the occurs on the occlusal surface of the M3 of the Red Lady. relationship between scratch width and pit size. As shown above The low frequency of pits shown by the Red Lady may reflect a (Figs. 6 and 7), the El Miron specimen shows relatively narrower relatively soft and tough diet, requiring more shearing rather than scratches than the mean of the entire sample, as do the PPNA and compressive forces during the chewing cycle (Schmidt, 2001; Chalcolithic samples. Therefore, based on the pit size and scratch Mahoney, 2007). A diet based on this class of foods yields small width, we could infer that the size of abrasive particles adhering to pits, as pit size reflects the amount of crushing needed to commi- the food ingested by the Red Lady was similar to those in the diet of nute the foods (Molleson et al., 1993). Thus, it would be expected the PPNA and Chalcolithic samples. Mahoney (2007) has already that pit size would be equivalent to that displayed by the two asserted that the smaller size of abrasive particles associated with groups with a softer diet. However, pit size in the Red Lady is the food eaten by these two populations, could be due to different similar to that seen in the Natufian and PPNB samples (i.e., hard underlying causes. In the PPNA sample, this was caused by a sig- diets). Although upon first inspection pitting and pit size seem to be nificant consumption of marine resources (following Mahoney inconsistent, it is important to take into account the relationship (2007) with particles adhering to aquatic foods being finer than between these two microwear variables. The El Miron specimen those adhering to terrestrial foods), while in the Chalcolithic sam- shows pits whose mean size is large relative to the mean per- ple the main cause was the influence on food by efficient cooking centage of pits displayed by Chalcolithic sample, although within of with ceramic utensils. Since no ceramics have been found in the its range of variation (Fig. 5). Therefore, when these two variables Magdalenian levels at the Miron site, we may assume that the diet are treated together, results from pit density and pit size are of the Red Lady would have incorporated some aquatic resources. consistent. This assumption is consistent with results found by Marín-Arroyo The absolutely large pits of the Red Lady could be due to a diet (2009, 2013), Marin-Arroyo and Geiling (in this issue) and Straus including abrasive agents similar in size to those found in the et al. (2011), which established that, although the diet of the Natufian hunteregatherers and PPNB forager-agriculturalists Lower Magdalenian inhabitants from El Miron Cave included (Schmidt, 2001). However, large abrasive particles not only mainly red deer and ibex, it also consisted of salmon, smaller fish enlarge the pits, but also yield wider scratches (Mass, 1994; and (when the humnas were at the shore) molluscs. The significant Mahoney, 2007). Based on scratch width (Fig. 4), the size of abrasive presence of aquatic foods (presumably mostly salmon) in the diet is particles adhering to the foods appears to be equivalent in the Red confirmed by the stable isotope analyses data from El Miron, which Lady and the Natufian, PPNA and Chalcolithic samples. Again, these indicates a diet with an important contribution from marine foods, findings seem to be contradictory. If abrasive particle size is perhaps up to 20% of the diet. responsible for both pit size and scratch width, it is difficult to In sum, although the microwear pattern presented in both the interpret the El Miron individual since she shows longer pits than buccal and occlusal surfaces of the El Miron specimen is difficult to the PPNA and Chalcolithic samples, while their scratch widths do accommodate within the patterns shown by the different not differ statistically. Thus, it could be assumed that the microwear comparative samples, some conclusions are possible. The Red Lady features' size not only depends on the size of abrasives adhering to consumed a mixed diet, including fish, meat and vegetables (the the food, but also on other aspects such as the angle of incidence of latter also suggested by dental calculus analysis by Power et al. (in abrasive particles on the occlusal surface (Daegling et al., 2013). This this issue)). This implies a generalized exploitation of the envi- angle is related to hardness of food and abrasive particles adhering ronment, which could be due to cultural or environmental factors to it, but also to the chewing biomechanics. Mahoney (2006c) (Perez-P erez et al., 2003; El-Zaatari and Hublin, 2014). Dietary pointed out that there is a close association between dental variability related with environmental conditions has been microwear and three metric variables (mandibular length and confirmed for Lower Magdalenian times through isotopic analysis. corpus width and depth) related to jaw biomechanics. Mandibles The El Miron individual is not the earliest human from Europe to with a narrow corpus undergo lesser compression loadings than show similar amounts of marine foods in their diets (the Gravettian those with broad a broad corpus, independent of the diet. This individuals from Arene Candide and La Rochette have similar values decrease in compression affects mainly the first molar, which pre- (Richards, 2009)). However, comparison to contemporary in- sents a dental microwear pattern characterized by small pits and dividuals from France shows that marine foods were important in narrow scratches, relative to second and third molars. Therefore, semi-coastal locations like El Miron (ca. 25 km to the Oldest Dryas although the Red Lady's mandible can be classified as a mandible shore, but close to the Río Ason, an historically salmon-rich river), with a narrow corpus (Carretero et al., 2015), it was not possible to although terrestrial foods (mainly red deer and ibex (see Marin- analyze microwear on the M1 due to heavy wear. Thus, it is not clear Arroyo and Geiling, in this issue)) were the overwhelmingly whether the pattern on the M3 is a result of a decrease in dominant protein sources. Future isotopic analyses of contempo- compressive loadings. Nonetheless, it does not seem likely that rary fauna from the El Miron site, as well as analyses of more these factors are responsible for the incongruent combination of humans from this time period in northern Spain are needed to large pits and narrow scratches present on the occlusal surface of the confirm this interpretation of a mixed, but ungulate meat- El Miron M3, since the size of both features depends on the same dominated diet. kind of forces exerted during the chewing cycle. Another possible explanation for the presence of large pits and Acknowledgments narrow scratches, is that these two microwear features show a different turnover rate. Wood and Schroer (2012) showed that deep We are very grateful to Lawrence G. Straus and Manuel Gonzalez pits will endure longer than shallow ones, and this can lead to an Morales for inviting us to participate in this special issue. We would overestimation of hard food consumption. 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