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Diet and habitat definitions for Mexican glyptodonts from Cedral (San Luis Potosí, México) based on stable isotope analysis

Published online by Cambridge University Press:  18 October 2011

VICTOR ADRIÁN PÉREZ-CRESPO ,
JOAQUÍN ARROYO-CABRALES ,
LUIS M. ALVA-VALDIVIA ,
PEDRO MORALES-PUENTE  and
EDITH CIENFUEGOS-ALVARADO
VICTOR ADRIÁN PÉREZ-CRESPO*
Affiliation:
Posgrado en Ciencias Biológicas, UNAM, Ciudad Universitaria, Del. Coyoacán, 04150, México, D. F.
JOAQUÍN ARROYO-CABRALES
Affiliation:
Laboratorio de Arqueozoología ‘M. en C. Ticul Álvarez Solórzano’, Subdirección de Laboratorios y Apoyo Académico, INAH, Moneda 16 Col. Centro, 06060, México, D. F.
LUIS M. ALVA-VALDIVIA
Affiliation:
Laboratorio de Paleomagnetismo, Instituto de Geofísica, UNAM, Ciudad Universitaria, Del. Coyoacán, 04150, México, D. F.
PEDRO MORALES-PUENTE
Affiliation:
Instituto de Geología, Universidad Nacional Autónoma de México, Circuito de la Investigación Científica S/N, Ciudad Universitaria, Del. Coyoacán, 04150, México, D. F.
EDITH CIENFUEGOS-ALVARADO
Affiliation:
Instituto de Geología, Universidad Nacional Autónoma de México, Circuito de la Investigación Científica S/N, Ciudad Universitaria, Del. Coyoacán, 04150, México, D. F.
*
†Author for correspondence: vapc79@gmail.com
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Abstract

Values for δ13C and δ18O obtained from molar samples from three individuals pertaining to Glyptotherium sp. from Cedral (San Luis Potosí, México) are provided and are utilized to infer general aspects of glyptodont diet and habitat. On average this animal showed a C3/C4 mixed diet, with a high consumption of C4 plants. Comparisons of the δ13CVPDB and δ18OVPDB values for glyptodonts with horses, mastodons, mammoths and tapirs from the same locality show that glyptodonts from Cedral lived in an open habitat.

Keywords

Méxicoglyptodontsdiethabitatδ13Cδ18O
Type
Rapid Communication
Information
Geological Magazine , Volume 149 , Issue 1 , January 2012 , pp. 153 - 157
Copyright
Copyright © Cambridge University Press 2011

1. Introduction

Cingulata is an order of mammals (Mammalia) originating in South America, which dispersed into North America during the Great American Biotic Interchange (Tonni & Pasquali, Reference Tonni and Pasquali2002; MacFadden, Reference MacFadden2006). In México, the oldest remains of the order Cingulata are pampatheres found in Lower Pliocene sediments with an estimated age of between 4.8 and 4.7 Ma, while the earliest record of glyptodonts was found in Upper Pliocene sediments dated at around 2.8 Ma (Carranza-Castañeda & Miller, Reference Carranza-Castañeda and Miller2004; Woodburne, Cione & Tonni, Reference Woodburne, Cione, Tonnin, Carranza-Castañeda and Lindsay2006).

In the Pleistocene of México there were three families within the order Cingulata: armadillos (Dasypodidae, Cabassous centralis and Dasypus novemcinctus), glyptodonts (Glyptodontidae, Glyptotherium cylindricum, G. floridanum and G. mexicanus) and pampatheres (Pampatheriidae, Holmesina septentrionales and Pampatherium mexicanum) (Arroyo-Cabrales, Polaco & Johnson, Reference Arroyo-Cabrales, Polaco and Johnson2007). Currently, armadillos are the only surviving family in the Americas (Wilson & Reeder, Reference Wilson and Reeder2005). Diet and general habitat for the two extinct families of Cingulata are the focus of great debate. Presently, armadillos are considered omnivores, having a quite varied diet including insects and fruits, and live in a great variety of habitats (McDonough & Loughry, Reference McDonough, Loughry, Vizcaíno and Loughry2008); as for the extinct families, pampatheres have been considered insectivores or open-zone grazers (De Iuliis, Bargo & Vizcaíno, Reference De Iuliis, Bargo and Vizcaíno2000), while glyptodonts are considered either browsers, inhabiting areas near water springs, similar to the preferred habitat of extant capybaras (Gillette & Ray, Reference Gillette and Ray1981), or grazers utilizing open areas, as suggested by others (Vizcaíno, Reference Vizcaíno2000; Vízcaíno et al. Reference Vizcaíno, Fariña, Bargo and De Iuliis2004). The above inferences were proposed based on the dental morphology, of which there is no equivalent in any modern mammal (Fariña & Vizcaíno, Reference Fariña and Vizcaíno2001). The objective of this study is to determine the diet and habitat of Glyptotherium sp. based on the analysis of δ13C and δ18O in three specimens from the archaeological–palaeontological site at Cedral (San Luis Potosí, México). We analysed the stable isotopes of carbon, reported as δ13C, and oxygen, δ18O, from the osteodentine carbonate (Ferigolo, Reference Ferigolo1985) obtained from the molars of three individuals.

1.a. Stable isotopes δ13C and δ18O

There are three photosynthetic pathways in plants, which are distinguished by differences in their δ13C values. C3 plants (−22 ‰ to −30 ‰) are the most abundant and include most dicotyledonous trees and shrubs, and a few temperate grasses. C4 plants (−10 ‰ to −14 ‰) include monocotyledonous grasses, pterydophytes and a few dicotyledonous trees and shrubs from tropical habitats. The CAM pathway is found in bromeliads, cacti, orchids and other succulent plants. The δ13C values are between −10 ‰ and −30‰, and therefore are not easily separated from the other two pathways (Smith & Epstein, Reference Smith and Epstein1971; Vogel, Reference Vogel1978; Ehleringer et al. Reference Ehleringer, Field, Liz and Kuo1986; Cerling et al. Reference Cerling, Harris, MacFadden, Leakey, Quade, Eisenman and Ehleringer1997; Keeley & Rundel, Reference Keeley and Rundel2003). These values are then passed onto herbivorous animals, with 14% enrichment with respect to the plant's original values (Cerling & Harris, Reference Cerling and Harris1999; Sánchez, Reference Sánchez, Alcorno, Redondo and Toledo2005). These final values can be assigned to the different feeding habits: browser species from −9 to −19 ‰; grazers, −2 to +2 ‰; and mixed diet organisms from −2 to −9 ‰ (MacFadden & Cerling, Reference MacFadden and Cerling1996).

While oxygen is incorporated into a mammal's bones through food, the main source is ingested water, and its composition of δ18O is affected mainly by environmental temperature (Dansgaard, Reference Dansgaard1964; Sánchez et al. Reference Sánchez-Chillón, Alberdi, Leone, Bonadonna, Stenni and Longinelli1994; Bryant & Froelich, Reference Bryant and Froelich1995; Kohn, Reference Kohn1996). Based on the previous statement, δ18O values are mainly used for palaeoclimatic inferences (Ayliffe, Lister & Chivas, Reference Ayliffe, Lister and Chivas1992; Iacumin et al. Reference Iacumin, Bocherens, Mariotti and Longinelli1996; Kohn, Schoeninger & Valley, Reference Kohn, Schoeninger and Valley1998; Grimes et al. Reference Grimes, Collinson, Hooker and Mattey2008).

2. Materials and methods

2.a. Study area

The Cedral archaeological–palaeontological site is located in the state of San Luis Potosí, México, at 23° 49′ N and 100° 43′ W, at 1700 m asl (Fig. 1). This site contains several ancient springs, which could have been used for drinking water by Late Pleistocene mammals, including the glyptodont, Glyptotherium sp.; mylodont, Paramylodon harlani; tapir, Tapirus haysii; wolf, Canis dirus; lion, Panthera atrox; camel, Camelops hesternus; mastodon, Mammut americanum; mammoth, Mammuthus columbi; and horses, Equus mexicanus, E. conversidens and Equus sp., as well as smaller mammals and other vertebrates (Álvarez & Polaco, Reference Álvarez and Polaco1982; Lorenzo & Mirambell, Reference Lorenzo, Mirambell and Bryan1986). Stratigraphically controlled excavations at the site were able to identify the presence of three fossiliferous levels, based on radiocarbon dates (modified from Lorenzo & Mirambell, Reference Lorenzo, Mirambell and Bryan1986). These levels are: (1) between 30000 and 25000 years bp (before present); (2) between 17000 and 11000 years bp, and (3) between 10000 and 8000 years bp (Fig. 2). It is important to recognize that two of the three glyptodont samples are from unknown layers, while the third one was collected in Layer XIV (Fig. 2).

Figure 1. Geographic location of the Pleistocene fossiliferous locality at El Cedral, San Luis Potosí, México (after Pérez-Crespo et al. Reference Pérez-Crespo, Sánchez-Chillón, Arroyo-Cabrales, Alberdi, Polaco, Santos-Moreno, Benammi, Morales-Puente and Cienfuegos-Alvardo2009).

Figure 2. Stratigraphic column for El Cedral. In the column, the level where excavations found the remains of glyptodonts is indicated with a bold box (modified from Lorenzo & Mirambell, Reference Lorenzo, Mirambell and Bryan1986).

2.b. Sample extraction and preparation

Samples from tooth osteodentine were taken from the following isolated teeth: DP-2489 (Layer XIV), DP-2490 and DP-2491 (backdirt), each of them representing a unique individual. They are housed at the Palaeontological Collection of the Archaeozoology Lab ‘M. en C. Ticul Álvarez Solórzano’, Subdirección de Laboratorios y Apoyo Académico del Instituto Nacional de Antropología e Historia. Osteodentine is the main component of glyptodont teeth (Ferigolo, Reference Ferigolo1985), and it has a similar chemical composition to dental enamel, but in different proportions, since enamel has 3% water, 1% organic matter (collagen) and 96% hydroxyapatite (Hillson, Reference Hillson1986; Koch, Reference Koch, Micherner and Lajtha2007), and osteodentine is composed of 4–20% water, 18–21% organic matter and 75% hydroxyapatite (Hillson, Reference Hillson1986; MacFadden et al. Reference MacFadden, Desantis, Hochstein and Kamenov2010), being more susceptible to diagenetic processes than the enamel. However, recent analyses on molars from different extinct ‘Xenarthrans’ suggested that their osteodentine could provide δ13C and δ18O signals that are reliable enough to propose inferences on food habits and palaeoclimates (MacFadden et al. Reference MacFadden, Desantis, Hochstein and Kamenov2010).

The preparation of the samples and analyses were performed in the Stable Isotopes Mass Spectrometry Lab at the Geology Institute, National University of México. The preparation procedure follows the method proposed by Koch, Tuross & Fogel (Reference Koch, Tuross and Fogel1997). First, 20 mg of osteodentine was ground and screened with a 125 μm mesh to obtain a fine and uniform dust. Then 10 ml of 30% distilled water (H2O) was added to eliminate the organic matter and left for a period of 2 hours; later the samples were centrifuged and the distilled water decanted. This procedure was executed three times. Once the washing was finished, 5 ml of a buffer solution made of CaCH3CO2–CH3COOH 1M, pH = 4.75, was added and allowed to rest for nine hours. Later the buffer solution was discarded, and samples were washed three times again with distilled water.

Finally, to eliminate any remaining water, ethanol was added, and the solution was left to rest for 12 hours in an oven at 90°C. Determination of simple isotopic abundance was executed in a Finnigan MAT 253 mass spectrometer with a dual inlet system, and GasBench auxiliary equipment with a GC Pal autosampler that has a temperature-controlled aluminium plate adjoined to the mass spectrometer (Révész & Landwehr, Reference Révész and Landwehr2002). Results were reported as δ18OVPDB and δ13CVPDB, and they were normalized using NBS-19, NBS-18 and LSVEC to the Vienna Pee Dee Belemnite (VPDB) scale in accordance with the corrections described by Coplen (Reference Coplen1988) as well as Werner & Brand (Reference Werner and Brand2001). For this technique, the standard deviation was 0.2 ‰ for oxygen and 0.2 ‰ for carbonates.

2.c. Statistical analysis of the results

The mean and standard deviation were obtained for the δ13C and δ18O values of the three individuals. Also, the type of diet was assigned in accordance with the δ13C values by comparison with the proposed classification of MacFadden & Cerling (Reference MacFadden and Cerling1996).

To infer the habitat type, first a variance analysis for the glyptodont δ13CVPDB values was performed against both typical browser species from closed areas, like mastodons (Mammut americanum) and tapirs (Tapirus haysii), as well as grazing species that inhabited open areas, like horses (Equus sp.) and the Columbian mammoth (Mammuthus columbi), from Cedral (Pérez-Crespo et al. Reference Pérez-Crespo, Sánchez-Chillón, Arroyo-Cabrales, Alberdi, Polaco, Santos-Moreno, Benammi, Morales-Puente and Cienfuegos-Alvardo2009; Pérez-Crespo, unpub. data). A comparison between the isotopic data from Cedral using a Tukey-Kramer test (Hammer & Harper, Reference Hammer and Harper2006) showed statistical differences between these groups. The glyptodont δ13CVPDB and δ18OVPDB values were compared to other members of the Cedral fauna, and plotted on a graph to visually display the analysis results from the analysis of variance (ANOVA) and Tukey-Kramer tests. The probability level for the statistical samples was p < 0.05, and the software used was NCCS and PASS (Hintze, Reference Hintze2004).

3. Results

The δ13CVPDB values were for specimen DP-2489, −4.65 ‰, DP-2490, −4.59 and DP-2491, −3.73 ‰, with a mean of −4.32 ‰ and a standard deviation of 0.51 ‰. The δ18O values had a mean of −6.85 ‰ and a standard deviation of 0.90 ‰, with the individual values as follows: DP-2489, −4.65 ‰; DP-2490, −7.62 ‰ and DP-2491, −7.08 ‰. An ANOVA test was performed between glyptodonts and the remaining assayed mammal herbivores from Cedral, showing significant differences (p < 0.000000*, F: 22.80, DF: 26), while the Tukey-Kramer test showed that glyptodonts were statistically different from the mastodons and tapirs, but similar to the horses and mammoths (Table 1). A graph showing δ13CVPDB v. δ18OVPDB values for the glyptodonts and remaining Cedral fauna confirms such analysis results (Fig. 3).

Table 1. Result of the Tukey-Kramer test between the glyptodonts and the El Cedral fauna

* Groups with significant differences. E – Equus sp., G – Glyptotherium sp., Ma – Mammut americanum, Mc – Mammuthus columbi and T – Tapirus haysii.

Figure 3. Graph of the δ13C v. δ18O values for Glyptotherium sp. and the faunal complex of El Cedral, México. E – Equus sp., G – Glyptotherium sp., Ma – Mammut americanum, Mc – Mammuthus columbi and T – Tapirus haysii.

4. Discussion

4.a. Diet

Glyptodont δ13CVPDB values show a mixed C3/C4 diet, with large quantities of C4 plants being consumed. Gillette & Ray (Reference Gillette and Ray1981) had previously proposed that the animal was a preferred browser. Fariña & Vizcaíno (Reference Fariña and Vizcaíno2001) questioned such a proposal since glyptodont molars are hypselenodont, with morphofunctional adaptations indicative of a grazer (Vizcaíno, De Iuliis & Bargo, Reference Vizcaíno, De Iuliis and Bargo1998; Vizcaíno et al. Reference Vizcaíno, Fariña, Bargo and De Iuliis2004; Vízcaíno, Reference Vizcaíno2009). The isotopic data obtained from the Cedral glyptodonts suggest that this animal ate mainly grasses.

Data provided by this study in regard to δ13CVPDB values supports the latter proposal, showing that the three sampled individuals had a mixed diet, but ate a large amount of C4 plants. This is also supported by the statistical analyses, since ANOVA and Tukey-Kramer test results for glyptodont δ13CVPDB values and those of mastodons and tapirs are significantly different, while the glyptodont values are similar to those of mammoths and horses from Cedral, which also show a C3/C4 mixed diet, but with a larger consumption of C4 plants. The palynological history for the region, recorded by Sánchez-Martínez & Alvarado (in press), shows the existence of herbaceous plants from the families Poacea, Amaranthacea and Quenopodiacea, all of which are C4 plants (Keeley & Rundel, Reference Keeley and Rundel2003), and could have been consumed by the glyptodonts.

4.b. Habitat

Based on the remains of these animals being found in lacustrine sediments, Gillette & Ray (Reference Gillette and Ray1981) proposed that they occurred in habitats associated with rivers, lakes and other water sources, similar to those used by living capybara. Our comparison of the δ13CVPDB and δ18OVPDB values of the studied glyptodonts and browsing species from Cedral shows quite different values, with glyptodonts being more similar to the grazing Cedral species. This is similar to the suggestions by Fariña & Vizcaíno (Reference Fariña and Vizcaíno2001) and Rincón, White & McDonald (Reference Rincón, White and McDonald2008), who have indicated that this species inhabited savannas or grassland; however, the presence of springs in Cedral, as well as near other glyptodont findings in México (Mead et al. Reference Mead, Swift, White, McDonald and Baez2007; Bravo-Cuevas, Ortíz-Caballero & Cabral-Perdomo, Reference Bravo-Cuevas, Ortíz-Caballero and Cabral-Perdomo2009), could point out that Cedral glyptodonts were living in open areas close to water sources, matching what Gillette & Ray (Reference Gillette and Ray1981) mentioned, with a diet mainly based on C4 plants rather than C3 plants.

5. Conclusions

Glyptodonts (Glyptotherium sp.) from Cedral had a C3/C4 mixed diet, dominated by the consumption of C4 plants, shown by the δ13CVPDB values. This species in Cedral was an inhabitant of open areas close to water sources, similar to extant capybaras. However, this hypothesis would need to be tested with a larger number of specimens in order to predict any pattern in their food habits, as well as in the kind of habitat. Furthermore, the studied specimens need to be specifically identified and dated.

Acknowledgements

We thank the Consejo de Arqueología from INAH for granting the permit to obtain the osteodentine samples from the studied glyptodonts. Also, the senior author thanks CONACYT and Posgrado en Ciencias Biologícas, UNAM for the graduate-studies scholarship (# 200441), and the Laboratorio Universitario de Geoquímica Isotópica (LUGIS) from the Institute of Geology, UNAM, as well as F. J. Otero and R. Puente M. for analysing the samples. Dr Michael Pasenko, University of Arizona, kindly reviewed an earlier version of this manuscript, and provided useful comments to improve it. Drs Begoña Sanchez Chillón, Sergio Vizcaíno and two anonymous reviewers also contributed with useful comments.

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Figure 1. Geographic location of the Pleistocene fossiliferous locality at El Cedral, San Luis Potosí, México (after Pérez-Crespo et al. 2009).

Figure 1

Figure 2. Stratigraphic column for El Cedral. In the column, the level where excavations found the remains of glyptodonts is indicated with a bold box (modified from Lorenzo & Mirambell, 1986).

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Table 1. Result of the Tukey-Kramer test between the glyptodonts and the El Cedral fauna

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Figure 3. Graph of the δ13C v. δ18O values for Glyptotherium sp. and the faunal complex of El Cedral, México. E – Equus sp., G – Glyptotherium sp., Ma – Mammut americanum, Mc – Mammuthus columbi and T – Tapirus haysii.