Partición de recursos dietéticos en los caballos del Pleistoceno Tardío de Cedral, centro-norte de México: evidencia del estudio de desgaste dental

Christian R. Barrón-Ortiz^1*, Jessica M. Theodor¹, and Joaquín Arroyo-Cabrales²

¹ Department of Biological Sciences, University of Calgary, 2500 University Dr. NW, Calgary, AB, T2N1N4, Canada. *crbarron@ucalgary.ca; chbarron45@yahoo.com

² Laboratorio de Arqueozoología, Instituto Nacional de Antropología e Historia, Moneda # 16, Col. Centro, C.P. 06060, México, D.F. Mexico.

ABSTRACT

The Late Pleistocene (late Wisconsinan glacial stage) deposits of the archeological-paleontological site of Cedral, north-central Mexico, have yielded abundant fossil remains of three horse species: Equus mexicanus, E. conversidens, and E. sp. These horses appear to have been sympatric, not only at this locality but in different sites in Mexico and the southwestern United States, posing the possibility that they partitioned available food resources in order to coexist. In this study, we investigated the feeding ecology of the Cedral horses through the analysis of dental wear (i.e., mesowear and microwear). The extended mesowear and low magnification microwear methods were used to infer the paleodiet of each species. The analysis of mesowear reveals significant differences in cusp shape between E. mexicanus and the other two equid species, with the former showing a higher percentage of rounded cusps and lower percentages of sharp and blunt cusps. These differences are consistent with those reported in a recent study of stable isotopes. Furthermore, the analysis of dental microwear indicates significant differences between the microwear patterns of the three equids. The results of the microwear analysis suggest that each species tended to feed on different foodstuffs with varying physical properties, supporting the hypothesis of dietary resource partitioning. Integrating the results derived from the examination of mesowear and microwear, as well as those gathered from the study of stable isotopes, it is suggested that E. conversidens and E. sp. were predominantly grazers, which may have fed at different feeding heights and/or in different microhabitats. Equus mexicanus also appears to have grazed to a large extent, but possibly with a more generalist dietary behavior.

Key words: paleodiet; mesowear; microwear; Equus; Cedral; Mexico.

RESUMEN

Los sedimentos del Pleistoceno Tardío (etapa glacial del Wisconsiniano tardío) del sitio arqueológico-paleontológico de Cedral, centro-norte de México, han producido abundantes restos fósiles de tres especies de équidos, los cuales han sido identificados como Equus mexicanus, E. conversidens y E. sp. Estos caballos al parecer fueron simpátricos, no solamente en esta localidad, sino también en diferentes sitios de México y el suroeste de Estados Unidos, lo que plantea la posibilidad de que presentaban una partición de los recursos alimenticios disponibles para coexistir. En el presente estudio, se investigaron los hábitos alimenticios de los caballos de Cedral a través del análisis del desgaste dental. Se emplearon los métodos de mesodesgaste y microdesgaste de baja magnificación para inferir la paleodieta de cada especie de caballo. El análisis de mesodesgate muestra diferencias significativas en la forma de las cúspides de los molares entre E. mexicanus y las otras dos especies, ya que E. mexicanus presenta un mayor porcentaje de cúspides redondeadas y menores porcentajes de cúspides aguzadas y romas. Estas diferencias son consistentes con los resultados reportados en un estudio reciente de isótopos estables. Por otra parte, el análisis de microdesgaste dental indica diferencias significativas en el patrón de microdesgaste de los tres équidos. Los resultados del análisis de microdesgaste sugieren que cada especie tendía a ingerir materiales con diferentes propiedades físicas, lo cual apoya la hipótesis de que presentaban una partición de recursos alimenticios. Integrando los resultados derivados del estudio de mesodesgaste y microdesgaste con aquéllos reportados en un estudio de isótopos estables, se sugiere que E. conversidens y E. sp. presentaban una dieta predominantemente pacedora y posiblemente se alimentaban a diferentes alturas del suelo y/o en diferentes microhábitats. Equus mexicanus parece también haber incorporado en su dieta una gran proporción de pastos, pero con un hábito alimenticio más generalista que los otros dos équidos.

INTRODUCTION

Three equid species are currently recognized from the Late Pleistocene deposits of Cedral, San Luis Potosí, Mexico, which have been tentatively identified as: Equus mexicanus Hibbard, 1955; E. conversidens Owen, 1869; and E. sp. (Figure 1c; Alberdi et al., 2003; Melgarejo-Damián and Montellano-Ballesteros, 2008; Barrón-Ortiz and Theodor, 2011; Marín Leyva, 2011). In this article, we follow these taxonomic designations noting that there is still no consensus regarding to the taxonomy of North American Pleistocene equids (e.g., Winans, 1989; Azzaroli, 1998; Weinstock et al., 2005; Pichardo, 2006; Scott et al., 2010). Nevertheless, regardless of the taxonomic names applied to the Cedral fossil horses, the distinction between the three species is well supported by differences in size (Alberdi et al., 2003; Melgarejo-Damián and Montellano-Ballesteros, 2008; Barrón-Ortiz and Theodor, 2011; Marín Leyva, 2011), metapodial proportions (Melgarejo-Damián and Montellano-Ballesteros, 2008; Marín Leyva, 2011), and features of the occlusal enamel pattern of the cheek teeth (Barrón-Ortiz and Theodor, 2011).

The frequent association of these three equid species in the same stratigraphic levels, not only at Cedral, but in different sites throughout central and northern Mexico as well as the southwestern United States (e.g., Hibbard, 1955; Harris, 1985, 1993; FAUNMAP, 1994; Barrón-Ortiz et al., 2009) suggests that, at least in these regions, they were sympatric. The question therefore arises: did these horses partition the available food resources in order to minimize competition and facilitate coexistence?.

In this study, we investigate the paleodiets of the Late Pleistocene (late Wisconsinan glacial stage) horses from Cedral, north-central Mexico, by examining dental wear (i.e., mesowear and microwear), which has been shown to correlate with diet (e.g., Walker et al., 1978; Fortelius and Solounias, 2000; Solounias and Semprebon, 2002). We test for significant differences in dental wear patterns between equid species that would indicate dietary resource partitioning. Thus far, the only other study that has examined the paleodiets of the Cedral horses corresponds to a stable isotope analysis conducted by Pérez-Crespo et al. (2009). Although sample sizes were admittedly reduced, this study hinted at the presence of dietary resource partitioning between E. mexicanus and the two other species. The results suggest an isotopically mixed C₃-C₄ diet for E. mexicanus and a diet composed largely of C₄ plants for E. conversidens, and E. sp.

STUDY AREA

The Cedral archeological-paleontological site is located in the state of San Luis Potosí, north-central Mexico, at 23^o 49' N and 100^o 43' W and at an altitude of 1,700 m a.s.l. (Figure 1a). The site was excavated by scholars from the Instituto Nacional de Antropología e Historia (INAH) from 1977 to 1984 (Lorenzo and Mirambell, 1986; Mirambell, 2012). Vertebrate fossil remains were collected from different stratigraphic levels in sediments that were deposited in a system of springs. A large portion of the equid remains recovered come from sedimentary layers (strata X-XII) that are bracketed by radiocarbon dates of 21,960 ± 540 and 31,850 ± 1,600 ¹⁴C years before the present (Figure 1b; Alberdi et al., 2003); however, assignment of any particular specimen to a specific stratum cannot be made, as this information is presently missing. Our study, thus, represents a time-averaged assessment of the diets of the Cedral equids at a temporal scale of approximately ten thousand years. The associated mammalian assemblage includes, among other vertebrates, Columbian mammoth (Mammuthus columbi), mastodon (Mammut americanum), mylodont (Paramylodon harlani), glyptodont (Glyptotherium sp.), Western camel (Camelops hesternus), tapir (Tapirus haysii), American lion (Panthera atrox), and dire wolf (Canis dirus) (Alvarez et al., 2012). The assemblage of herbivore mammals is suggestive of an open habitat with forest patches.

The extended mesowear (Kaiser and Solounias, 2003) and low magnification microwear (Solounias and Semprebon, 2002) methods were used to infer the paleodiets of the Cedral horses. A total of 104 specimens were analyzed (Tables 1A and 2A of the Appendix) all of them housed at the Paleontological Collection of the Archeozoology Laboratory 'M. en C. Ticul Alvarez Solórzano', Subdirección de Laboratorios y Apoyo Académico, Instituto Nacional de Antropología e Historia (INAH), Mexico City, catalogued under the acronym DP. Quantification and scoring of the variables investigated were carried out by the first author, as inter-observer error has been shown to be a concern, particularly for low magnification microwear (Mihlbachler et al., 2012). All statistical tests were conducted in PAST 2.17 (Hammer et al., 2001) and STATISTICA v. 9 (StatSoft*, 2009) software packages. The significance level for all tests was set to a p-value of 0.05.

Extended mesowear method

We collected mesowear data following the extended mesowear method proposed by Kaiser and Solounias (2003) for teeth in middle stages of wear (i.e., heavily worn as well as little worn teeth were not included in the analysis). The mesowear method was originally developed for the second upper molars (M2) to reconstruct ungulate diets based on the analysis of the buccal cusps (Fortelius and Solounias, 2000). It was subsequently extended in equids by Kaiser and Solounias (2003) to include the last four upper tooth positions: P4, M1, M2, and M3. The variables considered include the degree of relief of the cusps, high or low, and the shape of the sharpest cusp (whether anterior or posterior), which can be scored as sharp, round, or blunt (Figure 2; Fortelius and Solounias, 2000). Ungulates with a browsing diet tend to have molars with high relief and sharp cusps, whereas grazing ungulates tend to show molars with low relief and round/blunt cusps, and mixed feeders tend to present intermediate cusps morphologies.

In this study, digital photographs of the buccal side of each specimen were taken using a Sony Cybershot DSC-H9 digital camera. Prior to data collection, the order of the photographs was randomized to ensure observer blindness. Subsequently, the computer software ImageJ 1.47 (Rasband, 2013) was used to measure the depth of the valley between the paracone and metacone cusps as well as the anteroposterior length of each tooth, in order to determine cusp relief. These measurements were taken three separate times and an average was calculated with the objective of reducing measurement error. The teeth were scored as possessing low cusps if the cusp height index, determined by dividing the valley depth by the anteroposterior length, was lower than 0.1 (Fortelius and Solounias, 2000). Cusp shape was scored by direct observation of the specimens. The frequency of the mesowear variables was recorded for each equid species. In addition, we calculated the mesowear score (e.g., Rivals and Semprebon, 2006; Rivals et al., 2007), which combines cusp relief and shape into a single value that ranges from 0 (high relief and sharp cusps) to 3 (low relief and blunt cusps).

A Kruskal-Wallis test and randomization tests of independence (Monte Carlo simulations using 100,000 replicates) were used to test, respectively, for significant differences between equid species in mesowear score and frequency distributions of the mesowear variables. In addition, a discriminant function analysis (DFA) was conducted using the dataset of extant ungulates published by Fortelius and Solounias (2000), with the exclusion of the minute abraded brachydonts and species with a sample size lower than ten specimens. The variables percent high, percent sharp, and percent blunt cusps were employed in the DFA analysis. These variables were normalized using the arcsine transformation prior to performing the analysis. We followed the conservative dietary classification in Fortelius and Solounias (2000). The DFA was performed assuming equal prior classification probabilities for all groups. The classification functions derived from the DFA were subsequently used to classify the Cedral horses into one of the extant ungulate dietary categories: browsers, mixed feeders, and grazers.

Low magnification microwear

Several methodologies exist for the study of dental microwear of which low magnification microwear (e.g., Solounias and Semprebon, 2002; Semprebon et al., 2004; Merceron et al., 2004, 2005; Nelson et al., 2005; Gomes Rodrigues et al., 2009) and microwear texture analysis (e.g., Ungar et al., 2003, 2010; Scott et al., 2005, 2006; Merceron et al., 2010) are currently the most widely applied. In this study, we examined dental microwear at a low magnification (35 X) using high-resolution clear epoxy casts. Microwear features were counted on photographs (Figure 3) prepared following the methodology in Fraser et al. (2009), using a Nikon D200 digital camera and a Nikon SMZ1500 stereomicroscope; the digital resolution of the images obtained is 0.6 pixels/µm. Cleaning, molding, and casting of the teeth studied were done according to Solounias and Semprebon (2002). As for the mesowear method, only teeth in middle stages of wear were used. In addition, to minimize measurement error, the order of the photographs was randomized prior to data collection to ensure observer blindness (Mihlbachler et al., 2012), and microwear variables were quantified three separate times per specimen with the resulting average values used in further calculations.

We used the data collected following the methodology outlined above for comparison with the extant ungulate dataset gathered by Solounias and Semprebon (2002) using a principal component analysis (PCA) on the correlation matrix. We also conducted a DFA on the Solounias and Semprebon (2002) dataset, assuming equal prior classification probabilities for all groups, and used the classification functions generated to classify the Cedral equids into one of their dietary categories: browsers, fruit browsers, grazers, meal-by-meal mixed feeders, and seasonal mixed feeders. It should be noted that comparison of our microwear data with the Solounias and Semprebon (2002) dataset is considered tentative, as some recent studies have found high inter-observer error in the scoring of microwear features using low magnification procedures (e.g., Mihlbachler et al., 2012).

In order to test for significant differences between the three equid species, we modified the scoring procedure described above and included additional variables, with the objective of obtaining a finer characterization of dental microwear. In addition to the average number of scratches and pits, the number of exceptionally wide scratches (at least twice the width of coarse scratches) on the visible enamel band of the photograph was counted. The variables more than four cross scratches and more than four large pits were quantified for each counting area, providing a score of 1 if the features are present or 0 if they are absent, and calculating the average of the two counting areas to obtain an average score for these variables. The presence or absence of gouges on the enamel band visible in the photograph was scored as 1 and 0, respectively. Finally, we also scored scratch texture (e.g., Rivals et al., 2007; Rivals and Athanassiou, 2008). For each counting area, we gave a score of 0 if it consisted of fine scratches, 1 if it consisted of fine and coarse scratches, and 2 if it consisted of coarse scratches; the average score of the two counting areas was then calculated for each specimen.

A PCA employing the correlation matrix was used for visualization of each equid specimen in microwear multivariate space. In order to test for significant differences between species, we conducted a non-parametric multivariate analysis of variance test (NP-MANOVA), in which significance is estimated by permutation, using 100,000 replicates and the Mahalanobis distance measure. Bonferroni corrected pairwise comparisons were used to identify which species are significantly different from each other. We also examined the distribution of individual scratch counts for each species to assess if there is seasonality in the diet; seasonal mixed feeding taxa tend to display a bimodal distribution of scratches (Solounias and Semprebon, 2002). A Shapiro-Wilk test of normality was employed to test whether the distributions of individual scratch counts depart significantly from a normal distribution.

RESULTS

Mesowear

The results of the mesowear analysis are summarized in Table 1. Equus mexicanus shows the lowest mesowear score of the three equids, whereas E. sp. has the highest mesowear score, with E. conversidens occupying an intermediate position (Figure 4; Table 1); however, these differences are not statistically significant (Kruskall-Wallis test, H = 3.516, p = 0.1066). Likewise, the distribution of the variables relating to cusp relief are not significantly different (Monte Carlo simulations, p > 0.05), with all three equids showing a high frequency of low cusps (Figure 5). In contrast, there is a significant difference between E. mexicanus and the two other species in the distribution of the variables concerning cusp shape (Monte Carlo simulations, p < 0.05), with the former showing a higher percentage of rounded cusps and lower percentages of sharp and blunt cusps (Fig 5).

The DFA conducted on a subset of the extant ungulate dataset of Fortelius and Solounias (2000) correctly classifies 75.6 % of the species by diet; 77.8 % for browsers, 76.0 % for mixed feeders, and 72.7 % for grazers. The discriminant functions generated classify the three fossil equids within the grazers (posterior probabilities greater than 0.95), such as the white rhinoceros (Ceratotherium simum) and the plains zebra (Equus quagga).

Microwear

Analysis of the low magnification microwear indicates significant differences between the three horse species. Examination of the first two components of a PCA analysis (Figure 6; Table 2) calculated using the modified microwear variables (Table 2A of the Appendix), shows that each species tends to occupy a different region of the microwear multivariate space. Based on the PCA factor loadings (Table 2), Equus mexicanus separates from the other equids along the first principal component by possessing a greater number of pits, a lower scratch texture score, and a lower number of wide scratches. E. conversidens separates from E. sp. along the second principal component by presenting a greater number of scratches, a higher incidence of cross scratches and gouges, and a lower incidence of large pits. Moreover, the NP-MANOVA test reveals that there are significant differences in the multivariate means of the three horse species (F = 2.707, p < 0.001). Bonferroni corrected pairwise comparisons demonstrate significant differences between E. mexicanus and the other species (p < 0.02), as well as a marginally significant difference between E. conversidens and E. sp. (F = 2.204, p = 0.0419).

The distribution of individual scratch counts (not shown) for each species does not follow a bimodal distribution. Fur rmore, application of the Shapiro-Wilk test indicates that none of the distributions depart significantly from normality (p > 0.05), suggesting a lack of seasonality in the diet of the specimens studied. However, these results do not demonstrate that the Cedral equids did not have seasonally variable diets as it is not known, at present, whether animal remains at Cedral tended to accumulate on a particular season. If accumulation of animal remains tended to be seasonally concentrated, for instance during the dry season, then microwear would be reflecting the dry season diet, but not the diet during the rainy season.

DISCUSSION

The analyses of dental microwear and, to a lesser extent, mesowear support the hypothesis of dietary resource partitioning in the horses from Cedral. Microwear is significantly different in all three species, whereas mesowear (specifically cusp shape) is only significantly different in E. mexicanus.

The discrepancy in the results between mesowear and microwear is not surprising and has been reported in other extinct ungulate species (e.g., Fortelius and Solounias, 2000; Rivals and Semprebon, 2006; Merceron et al., 2007; Rivals et al., 2008; Rivals et al., 2010). Mesowear and microwear provide insights into dietary preferences at different scales. Mesowear reflects the overall abrasive nature of the diet over a relatively long period of an individual's lifetime, whereas microwear represents distinct microscopic features produced within weeks or days prior to death, by the food and/or exogenous grit ingested (Teaford and Oyen, 1989; Fortelius and Solounias, 2000; Solounias and Semprebon, 2002). Taking this distinction into account, the results for the analysis of mesowear indicate that the three equid species had an overall highly abrasive diet comparable to that seen in extant grazers; however, E. mexicanus appears to have had a somewhat less abrasive diet than the other equids. A similar highly abrasive diet was recently reported for samples of E. mexicanus and E. conversidens from Tlaxcala (Bonilla-Toscano et al., 2013), as well as for samples of E. conversidens from Hidalgo (Bravo-Cuevas et al., 2011) and Chiapas, Mexico (Carbot-Chanona and Gómez-Pérez, 2013). This may not have been the case, however, for a sample of E. conversidens from Michoacán, Mexico, where a mixed feeding diet has been reported on the basis of the study of dental microwear (Marín Leyva et al., 2013).

On a finer scale, the results of the microwear analysis for the Cedral specimens indicate that individual equids of each species tended to feed on different foodstuffs and/or ingested different types of grit, with varying physical properties, which produced distinctive microwear patterns. Although these results support the hypothesis of dietary resource partitioning, the analysis of dental microwear provides little insight into the mechanism by which this division of resources might have taken place. Extant ungulates partition dietary resources in a variety of ways, such as feeding on different plant species, feeding on different plant parts of the same species, feeding at different heights and/or in distinct microhabitats (e.g., Bell, 1971; Jarman and Sinclair, 1979; McNaughton and Georgiadis, 1986; du Toit, 1990; Spencer 1995; Stewart et al., 2002). Which of these alternatives for partitioning food resources was employed by the Cedral equids cannot be presently determined from the microwear data alone. This is partly because, despite extensive research, there is still no consensus about the primary agent responsible for the formation of microwear features. Phytoliths, lignin and cellulose, as well as exogenous grit have each been proposed as the primary factor producing microwear features (Walker et al., 1978; Ungar et al., 1995; Sanson et al., 2007; Merceron et al., 2007; Lucas et al., 2013; Schulz et al., 2013; Tütken et al., 2013). Determining whether microwear primarily records the type of vegetation eaten by a herbivore or whether it mainly records the amount and type of grit ingested, may allow for the formulation of more specific dietary hypotheses. Nevertheless, drawing from ecomorphological studies, it seems likely that the Cedral equids segregated according to microhabitat use and/ or feeding height, as evidenced by differences in limb proportions as well as differences in body size (Marín Leyva, 2011).

Equus mexicanus also appears to have grazed substantially, but with a greater degree of dietary flexibility, and there are alternative scenarios for the reconstruction of the dietary preferences of this equid. The isotope analysis demonstrates that E. mexicanus was an isotopically C₃-C₄ mixed feeder, with a mean δ¹³C value of -4.9 % (Pérez-Crespo et al., 2009). This may indicate that it fed on a combination of C₄ grasses and C₃ forbs growing close to the ground, accounting for its more generalist microwear pattern and its abrasive mesowear signal. Alternatively, this equid might have periodically incorporated in its diet woody browse and forbs, possibly during dry periods, as it has been reported in some extant equid species (Grubb, 1981; St-Louis and Côté, 2009). Serial isotope analyses and, perhaps, determining the season of death through the study of dental cementum (e.g., Burke and Castanet, 1995) of a sample of the teeth from which microwear was obtained, could elucidate this matter. In addition, feeding on a portion of C₃ grasses for this and the other equids is a possibility that cannot be ruled out, according to the results presented here and those from the analysis of stable isotopes. Many teeth of E. mexicanus and a few specimens of the other equids show high numbers of fine scratches. Different authors have noted that many C₃ grazers tend to have occlusal enamel surfaces covered by numerous, fine scratches, suggesting that this attribute could be used to differentiate C₃ from C₄ grazing (Solounias and Semprebon, 2002; Merceron et al., 2004; Rivals et al., 2007). However, as indicated by Merceron et al. (2004), more studies, especially experimental studies with controlled diets, are needed to confirm this.

Instances of dietary resource partitioning among sympatric equid taxa have been previously reported through the analysis of dental wear, ecomorphological, and/or geochemical data (e.g., MacFadden and Shockey, 1997; MacFadden et al., 1999; Barrón Ortiz and Guzmán Gutiérrez, 2009). As presented in this study, the Cedral equids also follow this pattern. Nonetheless, there are reports where the data do not clearly support dietary resource partitioning among sympatric equid species (e.g., Sánchez et al., 2006; MacFadden, 2008; Bonilla-Toscano et al., 2013). In any case, continued study of the feeding ecology of equids as well as other herbivores will open the way to better understand the feeding structure of herbivore communities, and elucidate shifts as well as restructuring brought about by large scale changes in vegetation over time. Of particular relevance to these studies is the integration of different dietary proxies, which, despite some of the shortcomings discussed above, ultimately allows for a finer reconstruction of feeding ecology than using each proxy in isolation.

CONCLUSIONS

Considering the results here presented and those of a previous analysis of stable isotopes (Pérez-Crespo et al., 2009), we conclude that E. conversidens and E. sp. from Cedral had a primarily grazing diet. The results also suggest that E. mexicanus grazed considerably, but it may have had a more generalized dietary behavior. Moreover, the study of dental wear, particularly microwear, provides evidence of dietary resource partitioning, as there are statistically significant differences in the microwear patterns of the three equid species. Feeding at different heights and/or in distinct microhabitats may have been the manner by which the Cedral equids partitioned available food resources. The present study highlights that finer reconstructions of feeding ecology may be obtained by integrating a variety of dietary and ecomorphological proxies.

APPENDIX. SUPPLEMENTARY MATERIAL

Tables 1A and 2A can be found at the journal website <http://rmcg.unam.mx/>, in the table of contents of this issue.

We would like to thank the Consejo de Arqueología, INAH, for granting permission to study the equid material from Cedral. Thanks are also extended to the INAH staff for their hospitality when visiting the collection. We also extend our gratitude to Elizabeth Romo Rábago for her assistance in data collection and molding of the teeth studied. Danielle Fraser and Víctor Adrián Pérez Crespo provided useful suggestions and comments during the development of the project. Funding for this study was provided by a graduate scholarship to CRBO from the Consejo Nacional de Ciencia y Tecnología de México (CONACYT scholarship No. 310423) and a graduate scholarship from the University of Calgary, as well as a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to JMT. Finally, we thank the reviewers, Víctor M. Bravo Cuevas and Florent Rivals, for their comments which helped improve an earlier version of this manuscript.

REFERENCES

Alberdi, M.T., Arroyo-Cabrales, J., Polaco, O.J., 2003, ¿Cuántas especies de caballo hubo en una sola localidad del Pleistoceno Mexicano?: Revista Española de Paleontología, 18(2), 205-212.         [ Links ]

Alvarez, T., Ocaña-Marín, A., Arroyo-Cabrales, J., 2012, Restos de mamíferos, in Mirambell, L.E. (ed.), Rancho "La Amapola", Cedral, un sitio arqueológico-paleontológico pleistocénico-holocénico con restos de actividad humana: México, D.F., Colección Interdisciplina, Serie Memorias, Instituto Nacional de Antropología e Historia, 147-194.         [ Links ]

Azzaroli, A., 1998, The genus Equus in North America - The Pleistocene species: Paleontographia Italica, 85, 1-60.         [ Links ]

Barrón Ortiz, C.R., Guzmán Gutiérrez, J.R., 2009, Hábitos alimenticios de los caballos Dinohippus mexicanus y Neohipparion eurystyle del Hemphiliano tardío de Tecolotlán, Jalisco, México: Investigación y Ciencia de la Universidad Autónoma de Aguascalientes, 17(45), 24-29.         [ Links ]

Barrón-Ortiz, C.R., Theodor, J., 2011, A geometric morphometric study of North American late Pleistocene equid upper premolars and its potential significance for equid systematics: Current Research in the Pleistocene, 28, 147-149.         [ Links ]

Barrón-Ortiz, C.R., González-Sánchez, V.H., Guzmán-Gutiérrez, J.R., 2009, Mastofauna de Chupaderos (Pleistoceno tardío), municipio de Villa de Cos, Zacatecas, in Memoria XI Congreso Nacional de Paleontología, Juriquilla: Universidad Nacional Autónoma de México, Centro de Geociencias, 88.         [ Links ]

Bell, R.H.V., 1971, A grazing ecosystem in the Serengeti: Scientific American, 224(1), 86-93.         [ Links ]

Bonilla-Toscano, L.R., Marín Leyva, A.H., Madurell, J., DeMiguel, D., 2013, Aproximación paleoambiental y dietaria de los équidos de Huexoyucan, México y Carihuela, España, in VIII Congreso Latinoamericano de Paleontología & XIII Congreso Mexicano de Paleontología, programa y resúmenes, Guanajuato: Guanajuato, México, Sociedad Mexicana de Paleontología A. C., Museo Dugès, Universidad de Guanajuato, 39-40.         [ Links ]

Bravo-Cuevas, V.M., Jiménez-Hidalgo, E., Priego-Vargas, J., 2011, Taxonomía y hábito alimentario de Equus conversidens (Perissodactyla, Equidae) del Pleistoceno Tardío (Rancholabreano) de Hidalgo, centro de México: Revista Mexicana de Ciencias Geológicas, 28(1), 65-82.         [ Links ]

Burke, A., Castanet, J., 1995, Histological observations of cementum growth in horse teeth and their application to archaeology: Journal of Archaeological Science, 22(4), 479-493.         [ Links ]

Carbot-Chanona, G., Gómez-Pérez, L.E., 2013, Use of mesowear análisis for inferring paleodietary habits of Equus conversidens (Perissodactyla: Equidae) from the Late Pleistocene of Chiapas, México, in VIII Congreso Latinoamericano de Paleontología & XIII Congreso Mexicano de Paleontología, programa y resúmenes, Guanajuato: Guanajuato, México, Sociedad Mexicana de Paleontología A. C., Museo Dugès, Universidad de Guanajuato, 41.         [ Links ]

du Toit, J.T., 1990, Feeding-height stratification among African browsing ruminants: African Journal of Ecology, 28(1), 55-61.         [ Links ]

FAUNMAP Working Group, 1994, FAUNMAP: a database documenting late Quaternary distributions of mammal species in the United States: Illinois State Museum Scientific Papers, 25(1-2), 1-690.         [ Links ]

Fortelius, M., Solounias, N., 2000, Functional characterization of ungulate molars using the abrasion-attrition wear gradient: a new method for reconstructing paleodiets: American Museum Novitates, 3301, 1-36.         [ Links ]

Fraser, D., Mallon, J.C., Furr, R., Theodor, J.M., 2009, Improving the repeatability of low magnification microwear methods using high dynamic range imaging: Palaios, 24(12), 818-825.         [ Links ]

Gomes Rodrigues, H., Merceron, G., Viriot, L., 2009, Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia): ecological implications: Naturwissenschaften, 96, 537-542.         [ Links ]

Grubb, P., 1981, Equus burchelli: Mammalian Species, 157, 1-9.         [ Links ]

Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001, PAST: Paleontological Statistics Software Package for Education and Data Analysis: Palaeontologia Electronica, 4(1), 4A.         [ Links ]

Harris, A.H., 1985, Late Pleistocene vertebrate paleoecology of the West: Austin, University of Texas Press, 293 pp.         [ Links ]

Harris, A.H., 1993, Quaternary vertebrates of New Mexico: Vertebrate Paleontology in New Mexico, New Mexico Museum of Natural History, Bulletin 2, 179-197.         [ Links ]

Hibbard, C.W., 1955, Pleistocene Vertebrates from the Upper Becerra Formation, Valley of Tequixquiac, Mexico, with notes on other Pleistocene Forms: University of Michigan, Contributions from the Museum of Paleontology, 12, 47-96.         [ Links ]

Hoppe, K.A., Koch, P.L., 2006, Chapter 13: The biochemistry of the Aucilla river fauna, in Webb, S.D. (ed.), First floridians and last mastodons: The Page-Ladson site in the Aucilla River: Dordrecht, Springer, 379-401.         [ Links ]

Jarman, P.J., Sinclair, A.R.E., 1979, Feeding strategy and the pattern of resource-partitioning in ungulates, in Sinclair, A.R.E., Norton-Griffiths, M. (eds.), Serengeti, dynamics of an ecosystem: Chicago, University of Chicago Press, 130-163.         [ Links ]

Kaiser, T.M., Solounias, N., 2003, Extending the tooth mesowear method to extinct and extant equids: Geodiversitas, 25(2), 321-345.         [ Links ]

Koch, P.L., Hoppe, K.A., Webb, S.D., 1998, The isotopic ecology of late Pleistocene mammals in North America: Part 1. Florida: Chemical Geology, 152(1-2), 119-138.         [ Links ]

Lorenzo, J.L., Mirambell, L., 1986, Preliminary report on archeological and paleoenvironmental studies in the area of El Cedral, San Luis Potosí, México, in Bryan A.L. (ed.), New evidence for the Pleistocene peopling of the Americas: Orono, Maine, Center for the Study of the Early Man, University of Maine, Peopling of the Americas Symposia Series, 107-113.         [ Links ]

Lucas, P.W., Omar, R., Al-Fadhalah, K., Almusallam, A.S., Henry, A.G., Michael, S., Arockia Thai, L., Watzke, J., Strait, D.S., Atkins, A.G., 2013, Mechanisms and causes of wear in tooth enamel: implications for hominin diets: Journal of the Royal Society Interface, 10, 20120923.         [ Links ]

MacFadden, B.J., 2008, Geographic variation in diets of ancient populations of 5-million-year-old (early Pliocene) horses from southern North America: Palaeogeography, Palaeoclimatology, Palaeoecology, 266(1-2), 83-94.         [ Links ]

MacFadden, B.J., Shockey, B.J., 1997, Ancient feeding ecology and niche differentiation of Pleistocene mammalian herbivores from Tarija, Bolivia: Morphological and isotopic evidence: Paleobiology, 23(1), 77-100.         [ Links ]

MacFadden , B.J., Solounias, N., Cerling, T.E., 1999, Ancient diets, ecology, and extinction of 5-million-year old horses from Florida: Science, 283, 824-827.         [ Links ]

Marín Leyva, A.H., 2011, Caballos del Pleistoceno y su paleoambiente en dos cuencas de Michoacán, México: Morelia, México, Universidad Michoacana de San Nicolás de Hidalgo, M.Sc. thesis, 156 pp.         [ Links ]

Marín Leyva, A.H., Alberdi, M.T., García-Zepeda, M.L., Ponce Zaavedra, J., Arroyo-Cabrales, J., Schaaf, P., De Miguel, D., 2013, Dieta de Equus conversidens durante el Pleistoceno tardío, en el centro occidente de México, in VIII Congreso Latinoamericano de Paleontología & XIII Congreso Mexicano de Paleontología, programa y resúmenes, Guanajuato: Guanajuato, México, Sociedad Mexicana de Paleontología A. C., Museo Dugès, Universidad de Guanajuato, 61-62.         [ Links ]

McNaughton, S.J., Georgiadis, N.J., 1986, Ecology of African grazing and browsing mammals: Annual Review of Ecology and Systematics, 17, 39-65.         [ Links ]

Melgarejo-Damián, M.P., Montellano-Ballesteros, M., 2008, Quantitative differentiation of Mexican Pleistocene horses: Current Research in the Pleistocene, 25, 184-186.         [ Links ]

Merceron, G., Blondel, C., Brunet, M., Sen, S., Solounias, N., Viriot, L., Heintz, E., 2004, The Late Miocene paleoenvironment of Afghanistan as inferred from dental microwear in artiodactyls: Palaeogeography, Palaeoclimatology, Palaeoecology, 207(1-2), 143-163.         [ Links ]

Merceron, G., Blondel, C., de Bonis, L., Koufos, G.D., Viriot, L., 2005, A new method of dental microwear analysis: application to extant primates and Ouranopithecus macedoniensis (Late Miocene of Greece): Palaios, 20(6), 551-561.         [ Links ]

Merceron, G., Schulz, E., Kordos, L., Kaiser, T.M., 2007, Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: evidence from dental meso-and micro-wear analyses of large vegetarian mammals: Journal of Human Evolution, 53(4), 331-349.         [ Links ]

Merceron, G., Escarguel, G., Angibault, J.M., Verheyden-Tixier, H., 2010, Can dental microwear textures record inter-individual dietary variations? PLOS ONE, 5(3), e9542.         [ Links ]

Mihlbachler, M.C., Beatty, B.L., Caldera-Siu, A., Chan, D., Lee R., 2012, Error rates and observer bias in dental microwear analysis using light microscopy: Palaeontologia Electronica, 15(1), 12A.         [ Links ]

Mirambell, L.E., 2012, Las excavaciones, in Mirambell, L.E. (ed.), Rancho "La Amapola", Cedral, un sitio arqueológico-paleontológico pleistocénico-holocénico con restos de actividad humana: México, D.F., Colección Interdisciplina, Serie Memorias, Instituto Nacional de Antropología e Historia, 31-69.         [ Links ]

Murray, M.G., Brown, D., 1993, Niche separation of grazing ungulates in the Serengeti: an experimental test: Journal of Animal Ecology, 62, 380-389.         [ Links ]

Nelson, S.V., Badgley, C., Zakem, E., 2005. Microwear in modern squirrels in relation to diet: Palaeontologia Electronica, 8(1), 14A.         [ Links ]

Pérez-Crespo, V.A, Sánchez-Chillón, B., Arroyo-Cabrales, J., Alberdi, M.T., Polaco, O.J., Santos-Moreno, A., Benammi, M., Morales-Puente, P., Cienfuegos-Alvarado, E., 2009, La dieta y el hábitat del mamut y los caballos del Pleistoceno tardío de El Cedral con base en isótopos estables (δ¹³C, δ¹⁸O): Revista Mexicana de Ciencias Geológicas, 26(2), 347-355.         [ Links ]

Pichardo, M., 2006, Update of equids in paleoindian time, in Mashkour, M. (ed.), Equids in time and space, papers in honour of Véra Eisenmann: Oxford, Oxbow Books, 31-48.         [ Links ]

Rasband, W., 2013, ImageJ, Image Processing and Analisys in Java, version 1.47: National Institutes of Health, U.S.A. <http://imagej.nih.gov/ij/index.html>         [ Links ].

Rivals, F., Athanassiou, A., 2008. Dietary adaptations in an ungulate community from the late Pliocene of Greece: Palaeogeography, Palaeoclimatology, Palaeoecology, 265(1-2), 134-139.         [ Links ]

Rivals, F., Semprebon, G.M., 2006, A comparison of the dietary habits of a large sample of the Pleistocene pronghorn Stockoceros onusrosagris from the Papago Springs Cave in Arizona to the modern Antilocapra americana: Journal of Vertebrate Paleontology, 26(2), 495-500.         [ Links ]

Rivals, F., Solounias, N., Mihlbachler, M.C., 2007, Evidence for geographic variation in the diets of late Pleistocene and early Holocene Bison in North America, and differences from the diets of recent Bison: Quaternary Research, 68(3), 338-346.         [ Links ]

Rivals, F., Schulz, E., Kaiser, T.M., 2008. Climate-related dietary diversity of the ungulate faunas from the middle Pleistocene succession (OIS 14-12) at the Caune de l'Arago (France): Paleobiology, 34(1), 117-127.         [ Links ]

Rivals, F., Mihlbachler, M.C., Solounias, N., Mol, D., Semprebon, G.M., de Vos, J., Kalthoff, D.C., 2010, Palaeoecology of the Mammoth Steppe fauna from the late Pleistocene of the North Sea and Alaska: Separating species preferences from geographic influence in paleoecological dental wear analysis: Palaeogeography, Palaeoclimatology, Palaeoecology, 286(1-2), 42-54.         [ Links ]

Sánchez, B., Prado, J.L., Alberdi, M.T., 2006, Ancient feeding, ecology and extinction of Pleistocene horses from the Pampean Region, Argentina: Ameghiniana, 43(2), 427-436.         [ Links ]

Sanson, G.D., Kerr, S.A., Gross, K.A., 2007, Do silica phytoliths really wear mammalian teeth: Journal of Archaeological Science, 34(4), 526-531.         [ Links ]

Schulz, E., Piotrowski, V., Clauss, M., Mau, M., Merceron, G., Kaiser, T.M., 2013, Dietary abrasiveness is associated with variability of microwear and dental surface texture in rabbits: PLOS ONE, 8(2): e56167.         [ Links ]

Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Grine, F.E., Teaford, M.F., Walker, A., 2005, Dental microwear texture analysis shows within-species diet variability in fossil hominins: Nature, 436, 693-695.         [ Links ]

Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Childs, B.E., Teaford, M.F., Walker, A., 2006, Dental microwear texture analysis: technical considerations: Journal of Human Evolution, 51(4), 339-349.         [ Links ]

Scott, E., Stafford, T.W., Jr., Graham, R.W., Martin, L.D., 2010, Morphology and metrics, isotopes and dates: determining the validity of Equus laurentius Hay, 1913: Journal of Vertebrate Paleontology, 30(6), 1840-1847.         [ Links ]

Semprebon, G.M., Godfrey, L.R., Solounias, N., Sutherland, M.R., Jungers, W.L., 2004, Can low-magnification stereomicroscopy reveal diet? Journal of Human Evolution, 47(3), 115-144.         [ Links ]

Solounias, N., Semprebon, G., 2002, Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids: American Museum Novitates, 366, 1-49.         [ Links ]

Spencer, L.M., 1995, Morphological correlates of dietary resource partitioning in the African Bovidae: Journal of Mammalogy, 76(2), 448-471.         [ Links ]

StatSoft, 2009, STATISTISCA, version 9.0: StatSoft Inc. Tulsa, Oklahoma, U.S.A.         [ Links ]

Stewart, K.M., Bowyer, R.T., Kie, J.G., Cimon, N.J., Johnson, B.K., 2002, Temporospatial distributions of elk, mule deer and cattle: Resource partition and competitive displacement: Journal of Mammalogy, 83(1), 229-244.         [ Links ]

St-Louis, A., Côté, S.D., 2009, Equus kiang (Perissodactyla: Equidae): Mammalian Species, 835, 1-11.         [ Links ]

Teaford, M.F., Oyen, O.J., 1989, In vivo and in vitro turnover in dental microwear: American Journal of Physical Anthropology, 80(4), 447-460.         [ Links ]

Tütken, T., Kaiser, T.M., Vennemann, T., Merceron, G., 2013, Opportunistic feeding strategy for the earliest old world hypsodont equids: Evidence from stable isotope and dental wear proxies: PLoS ONE, 8(9), e74463.         [ Links ]

Ungar, P.S., Teaford, M.F., Glander, K.E., Pastor, R.F., 1995, Dust accumulation in the canopy: a potential cause of dental microwear in primates: American Journal of Physical Anthropology, 97(2), 93-99.         [ Links ]

Ungar, P.S., Brown, C.A., Bergstrom, T.S., Walker, A., 2003, Quantification of dental microwear by tandem scanning confocal microscopy and scale-sensitive fractal analyses: Scanning, 25(4), 185-193.         [ Links ]

Ungar, P.S., Scott, R.S., Grine, F.E., Teaford, M.F., 2010, Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis: Philosophical Transactions of the Royal Society of London B, 365, 3345-3354.         [ Links ]

Voeten, M.M., Prins, H.H.T., 1999, Resource partitioning between sympatric wild and domestic herbivores in the Tarangire region of Tanzania: Oecologia, 120, 287-294.         [ Links ]

Walker, A., Hoeck, H.H., Perez, L., 1978, Microwear of mammalian teeth as an indicator of diet: Science, 201, 908-910.         [ Links ]

Weinstock, J., Willerslev, E., Sher, A., Tong, W., Ho, S.Y.W., Rubenstein, D., Storer, J., Burns, J., Martin, L., Bravi, C., Prieto, A., Froese, D., Scott, E., Xulong, L., Cooper, A., 2005, Evolution, systematics, and phylogeography of Pleistocene horses in the New World: A molecular perspective: PLoS Biology, 3(8), e241.         [ Links ]

Winans, M., 1989, A quantitative study of North American fossil species of the genus Equus, in Pothrero, D.R., Schoch, R.M. (eds.), The evolution of perissodactyls: Oxford, Clarendon Press, 262-297.         [ Links ]