Geographic variation of diet and habitat of the Mexican populations of Columbian Mammoth (Mammuthus columbi)

Quaternary International 276-277 (2012) 8e16

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Geographic variation of diet and habitat of the Mexican populations of Columbian Mammoth (Mammuthus columbi) Víctor Adrián Pérez-Crespo a, *, Joaquín Arroyo-Cabrales b, Mouloud Benammi c, d, Eileen Johnson e, Oscar J. Polaco b, Antonio Santos-Moreno f, Pedro Morales-Puente g, Edith Cienfuegos-Alvarado g a

Posgrado en Ciencias, CIIDIR-Oaxaca-IPN. Calle Hornos 1003. Sta. Cruz Xoxocotlán, Oaxaca, México Laboratorio de Arqueozoología “M. en C. Ticul Álvarez Solórzano”, Subdirección de Laboratorios y Apoyo Académico, INAH. Moneda 16 Col. Centro, 06060, México, D.F., México Laboratorio de Paleomagnetismo, Instituto de Geofísica, UNAM. Ciudad Universitaria, Del. Coyoacán, 04150, México, D.F., México d Institut International de Paléoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironnements (IPHEP)-UMR CNRS 6046, SFA-Université de Poitiers, Bât. De Sciences Naturelles (3ème étage), 40 avenue du Recteur Pineau, F86022 Poitiers Cedex, France e Museum of Texas Tech University, Box 43191, Lubbock, TX 79409, USA f Laboratorio de Ecología Animal, CIIDIR-Oaxaca-IPN. Calle Hornos 1003. Sta. Cruz Xoxocotlán, Oaxaca, México g Instituto de Geología, Universidad Nacional Autónoma de México, Circuito de la Investigación Científica S/N, Ciudad Universitaria, Del. Coyoacán, 04150 México, D.F., México b c

a r t i c l e i n f o

a b s t r a c t

Article history: Available online 14 March 2012

Isotopic data (d13C and d18O) for 25 enamel samples from Mammuthus columbi for 13 Mexican localities are provided. On average, the samples provide evidence of a mixed C3/C4 diet. The population consists of six individuals with an exclusive C4 plant diet, and 19 with some consumption of C3 plants. Latitude, longitude, and elevation do not have an affect on the average diet. Comparisons of data from the Mexican specimens with those values in the literature for samples from California, Arizona, Florida, Nevada, New Mexico, and Texas (USA) show that food habits in North America were similar. Comparisons of d13C and d18O values with those of javelinas, mastodonts, tapirs, and white-tailed deer from the Floridan Late Pleistocene confirm that mammoths primarily were inhabitants of open areas, indicating a probable case of biomic specialization. Ó 2012 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction During the Late Pleistocene, three families from the Order Proboscidea co-inhabited México: Gomphotheriidae, Mammutidae, and Elephantidae (Arroyo-Cabrales et al., 2002). The last family was represented only by the genus Mammuthus with a single species, the Columbian Mammoth Mammuthus columbi that was distributed throughout most of the country (Arroyo-Cabrales et al., 2007a). Although mammoth remains are abundant in México, most of the studies about this animal have been focused on specimens description and identification, as well as taxonomic discussion of the species (Arroyo-Cabrales et al., 2007b). A few studies have

* Corresponding author. UNAM, Posgrado en Ciencias Biologícas, Circuito de la Investigación Cien., 04150 Distrito Federal, México, Mexico. E-mail addresses: [email protected] (V.A. Pérez-Crespo), arromatu@ hotmail.com (J. Arroyo-Cabrales), [email protected] (M. Benammi), [email protected] (E. Johnson), [email protected] (A. Santos-Moreno), [email protected] (P. Morales-Puente), [email protected] (E. Cienfuegos-Alvarado). 1040-6182/$ e see front matter Ó 2012 Elsevier Ltd and INQUA. All rights reserved. doi:10.1016/j.quaint.2012.03.014

addressed taphonomical and ecological questions (Morett et al., 1998; Johnson et al., in press). The food habit for Mexican mammoths has been defined as a grazer (Ferrusquía-Villafranca, 1978; Morett et al., 2003). This inference has been supported based on molar morphological features: hypsodont molars, similar to those from present elephants; and specialized for an abrassive diet (Maglio, 1972; McDonald and Pelikan, 2006). On the other hand, coprolite studies of Columbian mammoth feces have shown mainly grasses, along with tree, shrub, and cacti leaves (Davis et al., 1985; Agenbroad and Mead, 1996). This browsing aspect has been tested through the use of d13C and d18O biochemical markers (Connin et al., 1998; Koch et al., 1998, 2004), assaying specimens from Arizona, California, Florida, Nevada, New Mexico, and Texas. Results demonstrate that the use of C3 and CAM plants was an important portion of the diet, accounting for as much as 20% of the intake. Pérez-Crespo (2007) and Pérez-Crespo et al. (2009) find a similar pattern, using specimens from Cedral and Laguna de las Cruces, San Luis Potosí, México. On average, the diets for the individuals from both localities could be assigned as mixed C3/C4 diets. Topography and climate in México are quite variable. Assayed

V.A. Pérez-Crespo et al. / Quaternary International 276-277 (2012) 8e16

9

samples, however, come only from those two localities. Whether mammoths had similar diets and habitat preferences all over México cannot be assumed solely based on samples from two localities. Geographic provenance of the samples (i.e., diet was independent from location) or variations according to sample provenance (Montellano-Ballesteros and Jiménez-Hidalgo, 2006) also need to be considered. Such is the case with antelopes, zebras, elephants, and rhinos in Africa (McNaughton and Georgiadis, 1986; Owen-Smith, 1988), Argentinan guanacos (Puig et al., 2008), South American gomphotheres (Sánchez et al., 2004), and Central and South American toxodonts (MacFadden, 2005). The objective of this study is to define the diet and habitat preferences for Columbian mammoths. Several localities throughout México are used, employing 13C/12C and 18O/16O ratios found in the apatite carbonates from molar enamel. These data are examined to determine if the food habits and habitats varied in accordance to the geographic region where the animals lived.

at low altitudes, d18O values are more positive than those at higher altitudes (Mook, 2002). Also, plants from warm and arid regions show a 18O enrichment due to evapo-transpiration in comparison to those living in cold and humid areas (Yakir, 1992; Quade et al., 1995). Herbivores inhabiting humid and closed (forest) zones show lower d18O values than those living in arid and open (grassland) zones (Feranec and MacFadden, 2006; Zanazzi and Kohn, 2008; Domingo et al., 2009). Because of that situation, d18O dental enamel can be used to infer climatic conditions that existed at a location in the past, and some species ecological characteristics also may be obtained (Bryant et al., 1994; Sánchez et al., 1994; Kohn, 1996; Kohn et al., 1996; Sponheirmer and Lee-Thorp, 1999; Schoeninger et al., 2000).

1.1. Carbon and oxygen isotopes

Twenty-five specimens pertaining to Columbian mammoth M. columbi have been selected from 13 localities (Fig. 1). Most of the assayed samples are from specimens on deposit at the Paleontological Collection of the Subdirección de Laboratorios y Apoyo Académico, National Institute of Anthropology and History. Four individuals are housed at the Paleontological Museum in Tocuila, State of México. Few of the localities are dated and in general the age is Late Pleistocene (Table 1). Only adult specimens have been used to avoid further biases. Localities have been chosen to account for latitudinal (northesouth), longitudinal (eastewest), and elevational (100e2240 msnm) gradients. The specimen localities with geographic coordinates, catalog numbers (DP for the INAH’s Paleontological Collections), and age are in Table 1.

The use of carbon stable isotopes to infer diets of Pleistocene herbivore and carnivore mammals has been an important tool, allowing an independent assessment of hypotheses based on morphological data (Bocherens et al., 1996; Koch, 1998; Palmqvist et al., 2003; MacFadden et al., 2004; Kohn et al., 2005). Carbon is fixed through plant photosynthesis that has three pathways: C3 (HatcheSlack cycle); C4 (CalvineBenson cycle); and CAM (Crassulacean Acid Metabolism) (Smith and Epstein, 1971; Dawson et al., 2002). The C3 pathway is found mainly in dicotyledoneous trees and shrubs, as well as some temperate grasslands. The first metabolic product from the process molecule is the rubisco (1, 5 ribulosebiphosphate carboxylase-oxygenase), with d13C values from
22 to
35&, and an average value around
27.8&  1.5& (O’Leary, 1981; Ehleringer and Cerling, 2002). On the other hand, the C4 pathway is typical of monocotyledonean grasses, as well as some trees and shrubs from warm regions. The first product molecule is phosphoenolpyruvate carboxylase (PEPC), with d13C values between
10 and
14&, with an average around
13.5&  1.5& (Cerling et al., 1997; Keeley and Rundel, 2003). The third pathway, CAM, is found in succulent plants, like cacti and bromelids, with values between
10& and
30&. These values are not useful in distinguishing either C3 or C4 plants (Gröcke, 1997). Carbon in plants becomes incorporated into herbivorous tissue, such as dental enamel apatite, when those plants are eaten (Feranec, 2007). Because of that situation, herbivores will have similar plant d13C values, but enriched at 14& (Gannes et al., 1997; Cerling and Harris, 1999; Balasse, 2002). Based on classifications proposed by Hofmann and Stewart (1972) and MacFadden and Cerling (1996), C4 plant eaters (grazers) show values from
2 to 2&; C3 plant eaters (browsers) have values from
9 to 19&; and C3/ C4 mixed-diet herbivores show values between
2 and
9&. The oxygen isotopic composition, however, for medium and large size mammals depends on the metabolic equilibrium between oxygen that enters the body, including water ingested from drinking, that from food, and the inhaled oxygen, and that from oxygen that exists throughout exhalation of CO2 and H2O, feces, urine, and sweat (Koch et al., 1994). Such equilibrium may be modified by the organism’s physiology, climate, and habitat (Sánchez, 2005). Ingested water is a major oxygen source for the body. Possible changes need to be considered due to altitude, latitude, longitude, and particularly temperature. At warm temperatures, oxygen isotopic values from water are more positive than those found at low temperatures (Dansgaard, 1964; Castillo et al., 1985). Similarly

2. Materials and methods 2.1. Study localities

2.2. Material extraction and statistical analyses A technique proposed by Koch et al. (1997) was followed for enamel extraction and pretreatment. As such, diagenetic alterations were not assayed. Using a Dremel power drill with a dentist bit, 10 mg of enamel was obtained from each molar. The enamel sample was dusted with an agate mortar with pistil, and sieved to get the finest dust. Hydrogen peroxide at 30% (10 ml) was added and the sample left standing for two hours. The peroxide then was decanted and the sample was washed three times with distilled water. Once the washing was concluded, a 1 M acetic acid and sodium acetate solution was added, left to stand for nine hours. The solution then was decanted and the sample again washed three times with distilled water. Finally, to eliminate any remaining water, ethyl alcohol was added and the sample left to dry in an oven at 90  C for 12 h. Samples were sent to the Laboratorio Universitario de Geoquímica Isotópica at the Geology Institute at UNAM, and assayed with a Finnigan MAT 253 mass spectrometer. The spectrometer had an autosampler GC Pal self-sampler that has a temperaturecontrolled aluminium plate adjoined to the mass spectrometer (Révész and Landwehr, 2002). Duplicate analysis standards were assayed to accomplish precision. Recording both d18OVPDB and d13CVPDB (Viena Pee Dee Belemnite) from the carbonates was undertaken following the procedure described by Révész and Landwehr (2002), utilizing the Bench Gas at 25  C. A 0.6 mg portion of carbonates was weighted in an exentainer tube, using a Mettler Toledo MX5 microscale with a precision of 0.000001 g. The tubes were set in an aluminium plate at 25  C. Each tube was injected with helium (99.995% pure) utilizing a two-way needle, for 10 min to eliminate any air. Then,

10

V.A. Pérez-Crespo et al. / Quaternary International 276-277 (2012) 8e16

Fig. 1. Localities with mammoth remains utilized for d13C and d18O assays. 1: Ciudad Acuña (Coahuila); 2: El Mezquital (Baja California Sur); 3: Monterrey (Nuevo León); 4: El Cedral (San Luis Potosí); 5: Laguna de las Cruces (San Luis Potosí); 6: Cuitzeo (Michoacán); 7: El Mirador (Hidalgo); 8: Santa Lucia (State of México); 9: Tocuila (State of México); 10: Santa Isabel (State of México); 11: Metepec (State of México); 12: Culhuacan (Distrito Federal); and 13: Jicotlán (Oaxaca).

the sample was left to stand for 55 h after 15 drops of 100% ortophosporic acid were injected using a syringe. The objective was to change the carbonates in a sample into CO2, using a reaction with ortophosphoric acid, in order to identify the chemical composition of the enamel. The d13CVPDB value was the reported unit. It was measured by using the carbon isotopic relationships 13C/12C and 18O/16O of CO2 from the assayed samples run through the Stable Isotopes mass spectrometer in comparison to the carbon 13C/12C and oxygen 18 16 O/ O isotopic relationships from the CO2, International standard PDB (Pee Dee Belemnite Limestone). The International standard is

Table 1 Altitude, latitude, and longitude for Mexican localities from where specimens were studied; m asl: meters above sea level. B. P.: before present. Altitude Latitude Longitude Age (m asl) Culhuacan, México City Cuitzeo, Michoacan Ciudad Acuña, Coahuila Cedral, San Luis Potosí El Mezquital, Baja California Sur El Mirador, Hidalgo Laguna de las Cruces, San Luis Potosí Metepec, State of Mexico Monterrey, Nuevo León Santa Maria Jicotlán, Oaxaca Santa Lucia I, Zumpango, State of México Santa Lucia II, Zumpango, State of México Santa Isabel Iztapa I, State of México Tocuila, State of México

2110 1840 280 1700 10

19 19 29 23 27

200 580 190 490 100

99 050 101 080 100 550 100 430 112 510

Rancholabrean Rancholabrean Rancholabrean 2480e33,000 B. P. Rancholabrean

2679 2070

19 500 22 430

98 200 102 010

Rancholabrean Rancholabrean

2670 537 2180

19 150 25 400 17 180

99 360 100 180 97 280

Rancholabrean Rancholabrean Rancholabrean

2243

19 440

98 590

23,900e26,300 B. P.



2243

19 44

0



0

98 59

2239

19 580

98 930

11,003e16,000 B. P.

2240

19 310

98 540

11,188 B. P.

11,170 B. P.

a calcium carbonate originated from belemnite (Belemnitella americana) from the Peede Sea of the Cretaceous Formation in South Carolina (Craig, 1957). The d18OVPDB and d13CVPDB values were calculated in accordance with the formulas: d13C ¼ (13C/12Csample/13C/12CVPDB-1)  1000 and d18O ¼ (18O/16Osample/ 18 16 O/ OVPDB-1)  1000. As a reference pattern, a CO2 (99.998% pure) tank was used, and carbonates d18OVPDB and d13CVPDB results were normalized using NBS 19, NBS-18, and LSVEC, with the VPDB scale in accordance with the corrections described by Coplen (1988) and Werner and Brand (2001). For this technique, a standard deviation of 0.2% for the oxygen and 0.2% for the carbon was used. At the IUPAC’s 43rd General Assembly in Beijing (2005), the Commission on Isotopic Abundances and Atomic Weights accepted the recommendation of the IAEA panel. The d13C values of all carbon-bearing materials would be measured and expressed relative to VPDB on a scale normalized by assigning consensus values of
46.6& to LSVEC lithium carbonate and þ1.95& to NBS 19 calcium carbonate. The samples were analyzed using LSVEC and NBS 19. Values for d13C and d18O from assayed specimens from Cedral and Laguna de las Cruces, San Luis Potosí, and Tocuila, State of México were included in the study (Pérez-Crespo, 2007; PérezCrespo et al., 2009; 2010) (Fig. 1). 2.3. Statistical analyses Sample data were analyzed using an analysis of variance (ANOVA) and TukeyeKrammer test by groups, using the assays mean values to infer differences among individuals. The same analysis was assayed between individuals from those localities that have been dated. Because several localities in the study are represented only by one specimen, a non-parametric KruskalleWallis test was used as it is a robust test for smallsized samples (Hammer and Harper, 2006). Less variation among individuals from the same locality could be hypothesized

V.A. Pérez-Crespo et al. / Quaternary International 276-277 (2012) 8e16

than those between locations because animals at the same locality would have been exposed to the same climatic conditions. Due to the small sample size in most of the studied localities, however, any regional trend could not be verified. Regression models were assayed along with altitude, longitude, and elevation data to test any existing pattern. The formula proposed by Koch et al. (2004) was used for having a percentage approximation to a C3 or C4 diet. Comparisons among the results of the current study and those reported by Connin et al. (1998) and Koch et al. (1998, 2004) were undertaken. These comparisons examined differences and similarities in the diet of the Mexican mammoths and USA mammoths. Data were merged into two groups (American and Mexican groups), and analyzed via an ANOVA (Tables 2e4). An ANOVA was used for comparing more than two samples as it is more robust than a T-Student test (Hammer and Harper, 2006). In order to calculate the d18O water value, Faure’s (1977) equation was used to transform the d18OVPDB values into d18Ovsmow values. Once such a transformation was assayed, Iacumin et al.’s (1996) formula was used for determining d18O water. For inferring habitat type, d13C and d18O values for Mexican mammoths were graphed, following Feranec and MacFadden (2006), in comparison with North American mastodont Mammut americanum, javelina Mylohyus fossilis, tapir Tapirus veroensis, and white-tailed deer Odocoileus virginianus from the Floridan Late Pleistocene (Koch et al., 1998). The d13C values were compared to test differences and similarities among the groups. Probability level for the statistical test was 95% (p < 0.05); software programs NCCS and PASS 2002 were utilized (Hintze, 2004). 3. Results For the d13C values, the mean value for the Mexican mammoths was
3.5& (%C4, 59.6), ranging from
7.5& to 0.3& (%C4: 33.4e85.4) (Table 5). The statistical analyses showed significant differences (ANOVA: p < 0.038681, F ¼ 2.47, df ¼ 24; KruskalleWallis: p < 0.288432, H ¼ 15.3095, df ¼ 13), while the TukeyeKramer test points out that the El Mezquital specimen statistically is different from those of Laguna de Cuitzeo and Metepec. Correlation coefficients for elevation (r ¼ 0.3499), Table 2 Mean values for d13C and d18O for Mammuthus columbi, Mammut americanum, Mylohyus fossilis, Odocoileus virginianus, and Tapirus veroensis from Florida, USA. Source: Koch et al. (1998); n: individual number. The original values of d18Ovsmow d18OVPDB using Faure’s (1977) equation: were transformed at d18OVPDB ¼ 0.97002*d18Ovsmow
29.98. Species

Locality

n

d13CVPDB

d18OVPDB

Mammuthus columbi Mylohyus fossilis Odocoileus virginianus Mammuthus columbi Mammut americanum Tapirus veroensis Mammuthus columbi Mammut americanum Odocoileus virginianus Tapirus veroensis Mammuthus columbi Mammut americanum Tapirus veroensis Mammuthus columbi Mammut americanum Mylohyus fossilis Odocoileus virginianus Mammuthus columbi Mammut americanum

Cuttler Hammock Cuttler Hammock Cuttler Hammock Hornsby Springs Hornsby Springs Hornsby Springs Page Ladson Page Ladson Page Ladson Page Ladson Rock Springs Rock Springs Rock Springs Vero Beach 2 Vero Beach 2 Vero Beach 2 Vero Beach 2 West Palm Beach West Palm Beach

6 3 2 1 5 1 2 4 2 2 4 3 2 4 3 2 2 2 9


0.9
9.8
12.6
5.6
11.9
12.3 0.1
10.9
12.4
11.7
3.7
11.6
13.4
1.9
11.8
10.9
14.3
0.6
10.1


0.2
2.2 0.4 0.006
0.006
1.07 0.04
1.3
3.4
4.0 1.1
0.7
3.0 0.6
1.4
2.2 0.4 1.5
1.8

11

Table 3 Average values for d13C and d18O for Mammuthus columbi from New Mexico and Texas. Source: Koch et al. (2004); n: number of individuals. The original values of d18Ovsmow were transformed at d18OVPDB using Faure’s (1977) equation: d18OVPDB ¼ 0.97002*d18Ovsmow
29.98. Locality

n

d13CVPDB

d18OVPDB

Ben Franklin Blackwater Draw Bonfire Shelter Clear Creek Congreso Avenue Easely Ranch Friesenhahn Cave Ingleside Kincaid Shelter Leo Boatright Pit Moore Pit Shulze Cave level C2 Waco Mammoth Site

3 9 1 2 1 1 16 8 1 4 9 1 14


2.1
3.2
2.8
1.8
1.0
0.8
1.8
1.5
1.8
3.8
2.7
4.2
2.7


1.2
4.2
1.3
3.3
2.1 0.7
1.1
1.2
0.8
2.2
2.0
1.7
0.9

latitude (r ¼
0.3446), and longitude (r ¼
0.2949) indicated that no pattern is evident, showing no diet change due to the effects of the three factors (Figs. 2e4). The comparison between data from localities that have been dated did not show any difference at a chronological level (ANOVA: p < 0.564088, F ¼ 0.91, df ¼ 12; KruskalleWallis: p < 0.426595, H ¼ 7.021978, df ¼ 7). On the other hand, d18O values had a range from
13.3& to
2.3&, with a mean value at
5.20&. Statistical analyses (ANOVA and KruskalleWallis test) did not indicate any significant difference among localities (p ¼ 0.841628, F ¼ 0.48, df ¼ 24; p < 0.439425, H ¼ 13.10904, df ¼ 13). When comparing the Mexican mammoths d13C values with those calculated for the existing USA samples, no significant differences were found (p < 0.187877, F ¼ 1.75, df ¼ 128). Significant differences (p ¼ 0.0000001, F ¼ 52.13, df ¼ 63), however, emerged when comparing d13C values for specimens pertaining to M. americanum, M. fossilis, O. virginianus, and T. veroensis, with the Mexican mammoths. Graphing d13C and d18O values between Florida animals and mammoths resulted in the groups being separated, with clear differences among them (Fig. 5). 4. Discussion 4.1. d13C, elevation, latitude, longitude, and diet On average, Mexican M. columbi had a mixed C3/C4 diet, with an average C4 plant consumption percentage (%C4approx) at 57% (
3.7%). These results were much higher for C3/CAM ingestion than for USA mammoths. Some extreme individuals occurred, like the one from Metepec with %C4approx 83% (d13C ¼ 0.3&) or the one from Laguna de Table 4 Average values for d13C and d18O for Mammuthus columbi from Arizona, California, Nevada, and New Mexico. Source: Connin et al. (1998); n: number of individuals. The original values of d18Ovsmow were transformed at d18OVPDB using Faure’s (1977) equation: d18OVPDB ¼ 0.97002*d18Ovsmow
29.98. Locality

n

d13CVPDB

d18OVPDB

Cactus Springs Howell’s Ridge Cave Murray Springs Pahrump Valley Rye Patch Sandia Cave Seff A Tule Springs Valley Wells

1 1 2 2 1 1 1 4 1


10.7
5.6
2.0
8.4
10.7
5.0
0.9
7.5
7.2


7.4
7.7
4.1
4.4
11.7
7.8
3.69
9.7
8.7

12

V.A. Pérez-Crespo et al. / Quaternary International 276-277 (2012) 8e16

Table 5 d13C and d18O values for the assayed specimens pertaining to Mammuthus columbi from México. þ Values provided by Pérez-Crespo (Unpublished Master’s Thesis) and PérezCrespo et al. (2009). The value (* %C4) was calculated based on the following equation: (100)d13C sample ¼ (100
x)d13C100%C3enamel þ (X)d13C100%C4enamel, enamel d13C100%C3 value is
12.5& and enamel d13C 100%C4 for 2.5&, corresponding to estimates for the Late Pleistocene (Koch et al., 2004; Koch, 2007). And d18O water was calculated based on the following equations: d18OvsmowCO3 ¼ 1.030901*d18OVPDB þ 30.91 (Faure, 1977) d18O& water ¼ d18OvsmowCO3
33.63/0.998 (Iacumin et al., 1996). Catalog Number

d13CVPDB &

%C4* approx.

d18OVPDB &

d18O water &

Locality

DP 4342 DP 4340 DP 1947 DP 1948 DP 1949 DP 1280 DP 626 DP 1194 DP 409 DP 412 DP 1824 DP 414 DP 1182 S/N S/N S/N S/N S/N S/N S/N DP 1975þ DP 1976þ DP 1978þ DP 1979þ DP 3729þ


3.0
3.5
1.7
5.5
1.7
5.1 0.1
3.9
4.9
4.8
7.5
4.3
2.3
3.9 0.3
5.7
3.5
1.4
4.4
5.1
3.5
3.7
3.2
1.9
3.8

63.2 60.2 72.1 46.6 72 49.5 83.7 57.5 51.4 51.0 43.0 54.6 68.3 57.0 85.4 45.1 59.8 74.3 54 49. 59.8 58.4 62.2 70.6 58


4.6
4.9
4.2
3.7
3.9
4.9
5.0
4.7
4.6
4.0
4.9
4.7
5.0
3.7
2.3
6.4
8.2
13.3
5.0
5.6
6.1
5.6
3.5
6.2
5.1


7.5
7.8
7.1
6.5
6.8
7.8
7.8
7.5
7.5
6.9
7.8
7.6
7.9
6.5
5.1
9.3
11.5
16.5
7.9
8.5
9.0
8.5
6.3
9.1
7.9

Santa Lucía II, State of México Santa Lucía II, State of México Santa Lucía I, State of México Santa Lucía I, State of México Santa Lucía I, State of México Jicotlán, Oaxaca Laguna de Cuitzeo, Michoacán Monterrey, Nuevo León Santa Isabel Ixtapa I, State of México Santa Isabel Ixtapa I, State of México El Mezquital, BCS. Ciudad Acuña, Coahuila Culhuacan, D.F Tocuila, State of México Metepec, State of México El Mirador, Hidalgo Tocuila, State of México Tocuila, State of México Tocuila, State of México Tocuila, State of México Laguna de las Cruces, S.L.P. Laguna de las Cruces, S.L.P. Laguna de las Cruces, S.L.P. Laguna de las Cruces, S.L.P. Cedral, S.L.P.

Cuitzeo (d13C ¼ 0.1&, %C4approx 83%). The one from El Mezquital had a significant contribution from C3 plants (%C4approx 43%, d13C ¼
7.5&). Because the statistical analyses considered the overall locality samples, those values could cause the significant difference found with the ANOVA, KruskalleWallis, and TukeyeKramer tests. Those unique localities, however, should not drive the interpretation as they appear to be outliers. Available data are lacking for Mexican plants in regard to C3, C4, and CAM composition among the different vegetation types. Because of that lack, it is not possible to undertake a comparison of modern and past variations of %C4 across the country. Nevertheless, Rubestien and Hobson (2004) point out that elevation is one of the factors affecting the d13C percentage. At higher elevations, temperature starts to go down, and concomitantly, C3 plants become more abundant while the presence of C4 plants decreases (Medrano and Flexas, 2000). Animals living at higher elevations

would be expected to have C3 plant values larger than those from lower elevations. In the case of the Mexican mammoths, however, such an inference was not found. The El Mezquital specimen had a mixed C3/C4 diet, with an %C4approx at 43%, and an elevation at the locality of 10 mosl. Meanwhile, the Metepec specimen was found above 2610 mosl, and had a %C4approx at 83% (d13C ¼ 0.3&). A similar pattern is found by the assays in relation to latitude. MacFadden et al. (1999) point out that when latitude increases, C4 plants diminish in abundance and C3 plants increase in number. This pattern is due to the temperature decrease as latitude increases. The individual from Jicotlán (a southern locality), however, shows a d13C value of
5.1& (%C4approx 50%), while the one from Ciudad Acuña (northernmost locality) has a d13C value of
4.7& (%C4approx 57%). It seems that d13C is not affected by the latitude factor. The same is the case for longitude. Samples from Laguna de Cuitzeo and El Mezquital (westernmost localities) do not show any diet pattern change compared with the one from the eastern locality of Jicotlán.

Fig. 2. Linear regression between Mexican mammoth localities altitudes and d13C values, with altitude shown as “meters above sea level”. d13C ¼ 0.0010*altitude
5.4525.

Fig. 3. Linear regression between Mexican mammoth localities latitudes and d13C values. d13C ¼
0.2270*latitude þ 1.1905.

V.A. Pérez-Crespo et al. / Quaternary International 276-277 (2012) 8e16

Fig. 4. Linear regression between Mexican mammoth localities longitudes and d13C values. d13C ¼
0.1839*longitude þ 14.8309.

These results are different from those reported by Connin et al. (1998) and Koch et al. (1998, 2004) for the studied species in most of the USA localities. An increment in C4 plants consumption is notable for individuals inhabiting the southeast US in comparison to those that lived in the Southwest. All localities in central México (El Cedral, Laguna de las Cruces, El Mirador, Metepec, Santa Isabel Iztapa, Santa Lucia I and II, Tocuila) are dated. The d13C values of sampled individuals do not show differences. This correspondence is due to the lacustrine system in the Basin of México that had similar environmental conditions throughout the entire basin during the Late Pleistocene (Bradbury, 1989; Caballero et al., 2010). Animals living in nearby areas should have d13C values similar to each other, rather than to individuals from other parts of the country. Because dates are not available for other localities, however, diet differences cannot be associated to climatic conditions prior, throughout, and after the Glacial Maximum. Modern elephants have been used for inferring mammoth diet (Haynes and Klimowicz, 2003). Observations of living elephant populations (Owen-Smith, 1988; Greyling, 2004) indicate that they

13

are more generalists than specialists, independently from the hypsodont molars that suggest a grazing feeding behavior (Haynes, 1991). Isotopic values for carbon suggest that the food habits from Mexican mammoths were similar to those of living elephants. Few studies are available on oxygen isotopic values of Mexican waters. Because of that situation, data for the studied mammoth localities as well as the Late Pleistocene in general are limited. The d18O values do not show any effect due to elevation. Individuals that inhabited Tocuila exhibit the lowest value (
7.1&), yet the locality is at 2240 mosl. The result could support the assumption that an elevation effect exists because d18O values diminish at a higher elevation (Sánchez et al., 2004). Nevertheless, in the same Tocuila population, one specimen shows a very high d18O (
3.7&), and another a very low value (
13.3&). As such, the variation cannot be due to elevation. Differences among population d18O values could be due to individuals drinking water from different locations while they were searching for food. Molars also may have grown in different time periods, indicating distinct oxygen isotopic values (Hoppe, 2004). Another case in which elevation is not a defining factor is the comparison between Metepec, with the highest d18O value (
2.3&) for México and at 2670 mosl, and El Mezquital, with a d18O value of
4.9& and at 10 mosl. Differences among d18O values may be due to migration movements. Not enough dates are available for the different mammoths, however, that would allow patterns to be defined. Castillo et al. (1985) analyzed d18O meteoric water composition at 18 different weather stations in México. San Carlos, Baja California, at an elevation of 170 msnm, had a value of
7.0& and Pueblo Nuevo, Tabasco, at an altitude of 10 mosl, had a value of
6.1&. In the Distrito Federal at 2400 mosl, the value was
6.7& and Suchixtlahuaca, Oaxaca at 2120 mosl, had a value of
9.7&. Those results indicated that besides temperature, the complex topography in México greatly influences precipitation. The very complex rainy season pattern resulted in some regions in the country getting much more rain than others. Temperature and humidity of two nearby locations also could be different (Metcalfe, 2006). Furthermore, such differences created local variations in the amount of precipitation that, in conjunction with distance from land to the sea, may affect the d18O values in México (Wassenaar et al., 2009). It is possible, then, that d18O mammoth dental enamel values may represent such issues, and reflect values similar to others found for d18O from nearby locations. The water d18O range for the Basin of México currently is from
9.5& to
10& (MoralesPuentes, personal communication, 2011). The water d18O values inferred for the Basin mammoths are
7.9& (Culhuacan),
7.2& (Santa Isabel Iztapa),
7.1& (Santa Lucia), and
10.1& (Tocuila). For two localities not far from the Basin of México, the values are
9.3& to
11.5& (Morelia) and
7.9& (Cuitzeo). 4.2. Habitat

Fig. 5. Results and isotopic composition variation of carbonates (d13C) and oxygen (d18O) from analyzed samples from México, in comparison with those obtained for Late Pleistocene fauna from the United States (Koch et al., 1998): M. Mammut americanum; My: Mylohyus fossilis; O: Odocoileus virginianus; T:Tapirus veroensis; CT: Cuitzeo; CU: Culhuacan; EC: Cedral; EM: El Mezquital; JI: Jicotlán; LC: Laguna de las Cruces; ME: Metepec; MI: El Mirador; MO: Monterrey; NM: New Mexico; SI: Santa Isabel Iztapa; SL: Santa Lucía; and TO: Tocuila.

Mexican mammoths are able to browse on C3 plants, probably trees and shrubs, and they may have preferred open habitats. This situation is in contrast to the available palynological record for Central and Northern México (Metcalfe, 2006; Caballero et al., 2010) as forested open areas existed where now a xerophillous scrub is in place similar to Southern México. Overall, Mexican Columbian mammoths appear to have inhabited open vegetation areas preferentially. A separation exists between browsing species from Florida that inhabited closed areas and Mexican mammoth values (Fig. 5). Feranec and MacFadden’s (2006) model, however, suggests that a clear separation between those animals from closed zones from those from open areas is due to the isotopic values of carbon and oxygen that are more negative than those

14

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from open areas. As such, d13C values of Floridan browsing species are more negative than those for mammoths, signifying distinct diets but not necessarily distinct d18O. This situation could be due to differences in altitude, longitude, and latitude at the Mexican sites as opposed to those from Florida that, in turn, affects the oxygen isotopic values. The separation of species by habitat is provided more by the d13C values than those for d18O. Finally, mammoths prefer living in open vegetation areas, similar to grasslands or savannas. The distinction of open vegetation areas primarily is related to carbon isotope values rather than oxygen isotope values due to the variation of the USA localities that primarily are from below 1000 mosl, and those from México that primarily are over 1000 mosl. It is possible that different climatic regimes produce similar d13C values at different locations. This situation may be the case in México for the Late Pleistocene. Conditions range between cold and dry periods to warm and humid ones, all of which produced expansion and contraction of forest and grasslands. Yet, the mammoth data show the consumption of C4 plants similar to those found in the USA. The presence of open vegetation areas found through this study based on stable isotopes is useful for comparison with other studies. For example, the Cedral palynological record points to the existence of large quantities of herbaceous plants but few trees, inferring the presence of a grassland at the end of the Pleistocene (Sánchez-Martínez and Alvarado, in press). Similarly, the palynological record for the Basin of México shows the existence of open forest and grasslands between 20,000 and 18,000 years BP (Lozano, 1996; Caballero et al., 2010), that later were reduced and a closed forest took over. For Laguna de las Cruces and Ciudad Acuña, pollen records are not available that would indicate the presence of grasslands during the Late Pleistocene. Johnson (2001) and Johnson et al. (2006) note, however, that during that time, a large savanna extended from central Canada to central México, including both localities, along with those from the Basin of México and San Luis Potosí. In El Mezquital, located in the Baja California Peninsula, the climate more than 10,000 years ago is more temperate than humid (the current one), allowing the presence of a subtropical vegetation that was replaced by xerophilous scrub (Lozano-García et al., 2002; Caballero et al., 2005). Jicotlán, Oaxaca, located in the Mixteca region, currently has an open vegetation, composed mainly of xerophilous scrubs, but with an abundance of cacti and Quercus. Pérez-Crespo et al. (2008), however, report the existence of Bison remains, a species that currently does not occur in this region. Bison is an indicator for the presence of grassland or savanna (Johnson et al., 2006), and infers the existence of such vegetation in the region during the Late Pleistocene. The palynological study by Velásquez et al. (2004) for Laguna de Cuitzeo shows the existence of a mountanous area of pine-oak forest and Cupressus-Juniperus, with an undergrowth dominated by poacid grasses. At lower elevations, a deciduous tropical forest is mixed with grasslands. In these three cases, however, the d13C and d18O data come from single individuals. The data need to be taken at face value. The existence of open areas in the locality cannot be generalized beyond the localities. Previous evidence suggested that the diet of M. columbi in México (Pérez-Crespo et al., 2010) was more flexible, consuming an amount of C3 plants, including trees and shrubs, but that flexibility did not extend to habitat preference. Mammoth, then, could be an example of biomic specialization. Hernández and Vrba (2005) defined biomic specialization as the capacity of a species to inhabit different biomes. Species defined as eurobymics could inhabit different biome types and a wide range of vegetation types

in contrast to stenebiomic species that are restricted to a unique biome and only one to a few vegetation types (Moreno et al., 2008). This situation may help explain mammoth extinction during the Pleistocene/Holocene transition. Climate conditions in México turned drier, and that affected the vegetation composition. The great savanna that used to be in central México was changed into a xerophylous scrub. The Baja Californian subtropical vegetation was fragmented and most of the region covered by xerophylous scrub. In Oaxaca, only a very small grassland patch remained (Rzedowski, 1981). Koch and Barnosky (2006) mention habitat lost as one of the extinction causes for several species during the Pleistocene/Holocene transition, including mammoths, but also cite human activity as another extinction cause. In México, some controversial evidence is noted for human-extinct fauna interactions, including mammoths (Mirambell, 1982; Lorenzo and Mirambell, 1986; Arroyo-Cabrales et al., 2006). Because of that situation, the direct impact of humans on extinction should not be discounted. The evidence, however, does not indicate any active hunting, but rather scavenging (Arroyo-Cabrales et al., 2006). New biochemical studies of d13C and d18O with more Mexican specimens could strengthen the argument that mammoth was specialized to live in open vegetation areas. It also would address whether environmental change provoked the extinctions, or if it was the result of human activities that drove the megafauna into extinction not just in North America but globally. The situation with ancient bison Bison antiquus may be pertinent to the extinction of mammoth and biomic specialization. Ancient bison makes it through the extinction filter at the end of the Pleistocene even though it was hunted by humans (e.g., Frison, 1996; Bement and Carter, 2003; Haynes and Huckell, 2007). Its changeover to the modern form (Bison bison) appears correlated with the changeover in the grassland from a mixed to a short-grass prairie (Lewis et al., 2007, 2010). Although an obligate grazer, both its genome and grass type on which it fed are flexible enough to allow adaptation to the new grassland. This flexibility apparently is not the case for mammoth. They are specialized not only to grassland but apparently a particular type of grassland. 5. Conclusions Isotopic analyses indicated that Mexican M. columbi are not solely or obligate grazers, but had a mixed C3/C4 diet. Some individuals had a significant consumption of C3 plants, reflecting an important browsing component. Some were exclusively grazers and eating only C4 plants. All of them lived in open areas of grasslands or savannas. Their diet and habitat were independent from altitude, latitude, and longitude of the place where they were living. Mammoths were flexible in their diet, but not in habitat type. In future studies, dated materials would be critical in order to undertake precise temporal comparisons, and determine if any pattern is constant through time. Acknowledgments The National Council for Science and Technology (CONACYT) and Instituto Politécnico Nacional provided a graduate scholarship (223602, SIP20050200, and SIP20060322200441) to the senior author. The Laboratorio Universitario de Geoquímica Isotópica (LUGIS) from the Institute of Geology, UNAM, as well as F. J. Otero and R. Puente M. are thanked for analyzing the samples. An early presentation of the results during the Vth International Conference on Mammoths and their relatives was supported in part by Johnson’s Horn Professorship research fund at Texas Tech University. This manuscript represents part of the ongoing Lubbock Lake

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