Feeding ecology, dispersal, and extinction of South American Pleistocene gomphotheres (Gomphotheriidae, Proboscidea)

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Feeding ecology, dispersal, and extinction of South American Pleistocenegomphotheres (Gomphotheriidae, Proboscidea)Author(s): Begoña Sánchez, José Luis Prado, María Teresa AlberdiSource: Paleobiology, 30(1):146-161. 2004.Published By: The Paleontological SocietyDOI: http://dx.doi.org/10.1666/0094-8373(2004)030<0146:FEDAEO>2.0.CO;2URL: http://www.bioone.org/doi/full/10.1666/0094-8373%282004%29030%3C0146%3AFEDAEO%3E2.0.CO%3B2

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Paleobiology, 30(1), 2004, pp. 146–161

Feeding ecology, dispersal, and extinction of South AmericanPleistocene gomphotheres (Gomphotheriidae, Proboscidea)

Begona Sanchez, Jose Luis Prado, and Marıa Teresa Alberdi

Abstract.—To reconstruct the paleodiet and habitat preference of gomphotheres, we measured thecarbon and oxygen isotope composition of 68 bone and tooth samples for three species of Gom-photheriidae from 24 different localities (Argentina, Bolivia, Ecuador, Chile, and Brazil). Addi-tionally, we measured the isotopic oxygen in the phosphate of 30 samples to control diageneticalteration. We calculated the correlation between pairs of d18Op–d18Oc values for enamel, dentine,and bone, taken from the same individual in order to verify whether the oxygen of structural ap-atite carbonate was in equilibrium with body water. Because of the good correlation obtainedamong pairs of the three skeletal components, we considered the d13C results of all components tobe equally representative of both gomphothere groups, and we used them collectively in the anal-ysis of the data.

To compare the different groups of specimens, we divided the samples into six groups, takinginto account their taxonomy as well as their geographic and stratigraphic distribution. Cuvieroniusspecimens from Chile were exclusively C3 plants eaters, whereas specimens from Bolivia and Ec-uador had a mixed C3-C4 diet. Stegomastodon showed a wider range of dietary adaptations. Speci-mens from Quequen Salado in Buenos Aires Province were entirely C3 feeders, whereas the diet ofspecimens from La Carolina Peninsula (Ecuador) was exclusively C4. The remaining South Amer-ican groups analyzed were C3-C4 mixed-feeders. Carbon isotope composition of bone and teethdecreased as latitude increased. We found evidence of an exclusively C3-dominated diet at approx-imately 35–418S. This result confirms that ancient feeding ecology cannot always be inferred fromdental morphology or extant relatives. Data from middle and late Pleistocene indicated that, overtime, there was an adaptive change in paleodiet from predominantly mixed-feeders to more spe-cialized feeders. We propose that this dietary evolution was one of the causes that forced gom-photheres to extinction in South America. In addition, the data presented in this paper suggest thatbecause of the different feeding preferences among mastodons, mammoths, and gomphotheres,only the bunodont gomphotheres reached South America.

Begona Sanchez and Marıa Teresa Alberdi. Museo Nacional de Ciencias Naturales, CSIC, Jose GutierrezAbascal 2, Madrid 28006, Spain. E-mail: [email protected], E-mail: [email protected]

Jose Luis Prado. INCUAPA, Universidad Nacional del Centro, Del Valle 5737, Olavarrıa B7400JWI, Argen-tina. E-mail: [email protected]

Accepted: 23 July 2003

Introduction

The Gomphotheriidae of South America isconsidered to have descended from NorthAmerican gomphothere stock. Members ofthis family dispersed into Asia, Europe, andNorth America during the late African Eocenethrough the late Pleistocene and arrived inSouth America during the early Pleistocene(Simpson and Paula Couto 1957; Webb 1991).Gomphotheres experienced an enormous di-versification similar to that for all ungulates inNorth America during the Clarendonian. Thediversity of gomphotheres then decreased,with a major drop during the latest Hemphil-lian (Webb 1983). Gomphotheres are known inSouth America from the early Pleistocene (En-senadan South American Land Mammal Age,

hereafter SALMA) to the late Pleistocene, Lu-janian SALMA (Alberdi and Prado 1995). Be-cause there are only few and slight differencesamong these animals, Simpson and PaulaCouto (1957) concluded that it was best eitherto tentatively refer all South American formsto the subfamily Anancinae, or to ‘‘simplyabandon subfamilies within the Gomphoth-eriidae’’ (Simpson and Paula Couto 1957: p.181). In our opinion, and given current knowl-edge, the latter is the best postulate.

During the Pleistocene, two corridors de-veloped in South America. These two corri-dors shaped the paleobiogeographic historyof most North American mammals in SouthAmerica. The most viable model postulatedfor the gomphothere dispersal process seemsto indicate that the small Cuvieronius utilized

147ISOTOPIC EVIDENCES ON THE PALEODIET

the Andes corridor, whereas the large Stego-mastodon dispersed through the Eastern routeand some coastal areas. The dispersal of bothgenera in South America seems to reflect anadaptive shift in their feeding ecology (Webb1991).

In this paper we compare the results of car-bon and oxygen isotopic data from toothenamel, dentine, and bone of Pleistocene gom-photheres from South America. The purposeof this study was to investigate gomphotherepaleodiet and habitat preference, and to showhow these are related to the dispersion and ex-tinction of these groups in South America. Wealso present the first set of d18Op and d18Oc

measured on the tooth and bone of SouthAmerican Pleistocene gomphotheres. Anotheraim of this study was to confirm whether theoxygen of structural apatite carbonate is inequilibrium with body water in South Amer-ican gomphotheres, as is the phosphate oxy-gen. Finally, we sought to verify whether it ispossible to obtain information about postmor-tem modification effects in fossils by usingcoupled isotope measurements of oxygen incarbonate and phosphate.

Isotopic Ecology of Fossil Mammals. In recentdecades, oxygen and carbon isotope analyseshave been increasingly used to reconstruct pa-leoenvironmental and paleoclimatical condi-tions. In the case of homeothermic animals ingeneral, the oxygen isotope composition ofapatite depends primarily on the oxygen bal-ance of the animal (Longinelli 1984; Luz et al.1984). Influxes of oxygen include ingested wa-ter (drinking water 1 water from plants) aswell as inspired O2 gas; oxygen is lost from thebody as liquid water in urine, sweat, and feces,and as CO2 and H2O in respiratory gases. Fac-tors acting on this balance are both internal(related to the physiology of the animal) andexternal (related to ecology and to climate).Oxygen isotope variations in large mammalsdepend largely on external factors such as thed18O of ingested water. Because the oxygenisotopic composition of phosphate in mam-malian bones and teeth (d18Op) is related tothat of ingested water, and ingested watercomes ultimately from precipitation, the d18Oof enamel and bone phosphate can be used toinfer climatic conditions in the past (Longi-

nelli and Nuti 1973; Kolodny et al. 1983;D’Angela and Longinelli 1990; Bryant et al.1994; Sanchez-Chillon et al. 1994; Bryant andFroelich 1995; Delgado et al. 1995; Kohn 1996;Kohn et al. 1996, 1998).

Previous studies have also shown that thecarbon isotope ratio (d13C) of fossil teeth andbones can be used to obtain dietary informa-tion about extinct herbivores (De Niro and Ep-stein 1978; Vogel 1978; Sullivan and Krueger1981; Lee-Thorp et al. 1989, 1994; Koch et al.1990, 1994; Quade et al. 1992; Cerling et al.1997; MacFadden 2000a). This carbon isotoperatio is influenced by the type of plant mate-rial ingested, which is in turn influenced bythe photosynthetic pathway utilized by theplants. During photosynthesis, C3 plants interrestrial ecosystems (trees, bushes, shrubs,forbs, and high elevation and high latitudegrasses) discriminate more markedly againstthe heavy 13C isotope during fixation of CO2

than do tropical grasses and sedges (C4

plants). Thus C3 and C4 plants have distinctd13C values. C3 plants have d13C values of 222per mil (‰) to 230‰, with an average of ap-proximately 226‰, whereas C4 plants haved13 C values of 210‰ to 214‰, with an av-erage of about 212‰ (Smith and Epstein1971; Vogel et al. 1978; Ehleringer et al. 1986,1991; Cerling et al. 1993). Animals then incor-porate carbon from food into their tooth andbone with an additional fractionation of about12–14‰. Mammals feeding on C3 plants(fruit, leaves, etc.) characteristically have d13Cvalues between about 210‰ and 216‰,whereas animals that eat C4 tropical grasses(including blades, seeds, and roots) have d13Cvalues between 12‰ and 22‰. A mixed-feeder would fall somewhere in between thesetwo extremes (Lee-Thorp and van der Merwe1987; Quade et al. 1992). Hence, the relativeproportions of C3 and C4 vegetation in an an-imal diet can be determined by analyzing itsteeth and bone d13C.

A number of previous studies have used thecarbon and oxygen isotopic abundance of fos-sils and paleosols from South America to re-construct both the diets of extinct herbivoresas well as the paleoenvironmental parametersof ancient terrestrial communities and ecosys-tems (Latorre et al. 1997; MacFadden et al.

148 BEGONA SANCHEZ ET AL.

1996, 1999; MacFadden 1998, 2001). In recentyears, carbon isotopic data for gomphotheresfrom South America have been presented inseveral papers (MacFadden et al. 1994;MacFadden and Shockey 1997; MacFadden2000b).

Materials and Methods

We recognize two genera of gomphotheres:Cuvieronius, represented by the species Cuvi-eronius hyodon; and Stegomastodon, representedby two species, Stegomastodon waringi and Ste-gomastodon platensis (Alberdi and Prado 1995;Prado et al. 2003). Cuvieronius hyodon is geo-graphically restricted to the Andean region inEcuador, Peru, Bolivia, Chile, and northwestArgentina (Hoffstetter 1952; Casamiquela etal. 1996; Frassinetti and Alberdi 2000). Stego-mastodon waringi has been found in the SantaElena peninsula in Ecuador (Hoffstetter 1952),and in the non-Andean tropical regions of theSouth America such as Colombia and Brazil(Hoffstetter 1952; Simpson and Paula Couto1957; Correal Urrego 1981; Ficcarelli et al.1993). Stegomastodon platensis has a moresouthern distribution from the middle to thelate Pleistocene of Argentina, principally inthe Pampean Region (Prado et al. 2002), aswell as in Uruguay (Mones and Francis 1973)and possibly Paraguay (Cabrera 1929; Simp-son and Paula Couto 1957).

Sixty-eight skeletal samples of Cuvieroniushyodon, Stegomastodon platensis, and Stegomas-todon waringi from 24 different South Ameri-can middle and late Pleistocene localities inArgentina, Bolivia, Brazil, Chile, and Ecuador(Fig. 1) were measured to obtain the oxygenand carbon isotopic composition of bone andtooth enamel carbonate. Fossil samples werecollected from specimens stored at the follow-ing institutions: Museo de La Plata (MLP) andMuseo Argentino de Ciencias Naturales ‘‘Ber-nardino Rivadavia,’’ Buenos Aires (MACN),Argentina; Museo de Upsala and StockholmNatural History Museum, Sweden; Lund col-lection at Zoological Museum of Copenhagen(ZMK), Denmark; Museo Nacional de Rıo deJaneiro, Brazil; Museo de Historia Natural dela Universidad Federal de Minas Gerais inBelo Horizonte, Brazil (MHN); Museo de laPontificia Universidad Catolica de Minas Ger-

ais in Belo Horizonte, Brazil; Museo de la Es-cuela Politecnica Nacional de Quito (MEPN),Ecuador; Museo Nacional de Historia Natural,Santiago, Chile (SGO). The museum collectionnumber and the locality of each sample are re-ported in Table 1.

To compare the different specimens, we di-vided the samples into six groups, taking intoaccount the species, the geographic location,and the age of the corresponding deposit. Thesix groups are listed in Table 1: (1) Cuvieroniushyodon from the late Pleistocene of Ecuador;(2) Stegomastodon waringi from the late Pleis-tocene of Santa Elena Peninsula in Ecuador;(3) Stegomastodon platensis from the Pleistoceneof Argentina; (4) Cuvieronius hyodon from themiddle Pleistocene of Bolivia; (5) Stegomasto-don waringi from the late Pleistocene of Brazil;and (6) Cuvieronius hyodon from the Pleisto-cene of Chile. In Table 1, we also included re-sults previously published by Bocherens et al.(1996) for the modern elephant Loxodonta af-ricana from the Amboseli Park (Kenya).

In a majority of specimens, we extractedenamel and dentine samples from the anteriorbasal edge of the first loph of the M3. In pop-ulations where no M3 was available, sampleswere extracted from the same location of theM2. Gomphotheriid teeth are brachyodontand emerge at different stages during the an-imal’s life (Roth and Shoshani 1988; Roth1992; Kohn et al. 1998). The largest inter- andintratooth variation in the oxygen isotopecomposition of mammalian tooth enamelphosphate is in hypsodont teeth (Fricke andO’Neil 1996; Fricke et al. 1998; Koch et al.1998). Fox (2000) indicates that the large var-iations of d18O and d13C observed in gom-phothere tusks are an accurate reflection ofseasonal temperature changes. However, thegrowth and structure of the tusks differ com-pletely from those of the teeth. Tusks growcontinuously throughout the life of the animalin incremental, concentric bands or rings.Teeth, on the other hand, continually erupt,progress, wear down, and are shed (Roth1992), a process that makes the detection ofclear seasonal changes impossible. Eventhough the analyzed teeth may be somewhatvariable, most samples were taken from the


FIGURE 1. A, Geographical distribution and dispersal routes of different species of the family Gomphotheriidae inSouth America. Pointed arrow: possible dispersion route of the genus Cuvieronius. Solid arrow: possible dispersionroute of species from genus Stegomastodon. B, Geographical distribution of analyzed samples areas from Argentina(Ar), Bolivia (Bo), Brazil (Br), Chile (Ch), and Ecuador (Ec).


TABLE 1. d18O and d13C isotopic values for skeletal elements of South American fossil gomphotheres and the modernLoxodonta africana from Amboseli Park (Kenya). late Pl 5 late Pleistocene; mid Pl 5 middle Pleistocene. e 5 enamel;d 5 dentine; b 5 bone; t 5 tooth (enamel 1 dentine). Ec 5 Ecuador; Ar 5 Argentina; Bo 5 Bolivia; Br 5 Brazil;Ch 5 Chile; K 5 Kenya. Skeletal samples with the same specimen number correspond to the same individuals.

Species (age)Specimennumber

Skeletaltissue Locality (country)

Alti-tudem.asl

Lati-tude

8Sd13C (CO3)

‰ PDB

d18O(CO3) ‰V-SMOW

C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)

V-1248V-1239V-1238V-1238V-3038V-1254

bedeee

Quebrada Colorada (Ec)Alangası (Ec)Alangası (Ec)Alangası (Ec)Alangası (Ec)Punın (Ec)

277827782778277827782778

000002

27.3227.3829.3929.5928.0425.66

21.2122.523.7622.5823.5222.12

C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)

V-1254V-1254V-164V-1251V-164V-164

dbbbde

Punın (Ec)Punın (Ec)Punın (Ec)Punın (Ec)Punın (Ec)Punın (Ec)

277827782778277827782778

222222

25.126.8828.5526.8829.5629.71

22.1821.5521.9922.0822.2423.01

S. waringi (late Pl)S. waringi (late Pl)S. waringi (late Pl)S. waringi (late Pl)

V-2010V-1269V-1269V-160

bdee

La Carolina (Ec)La Carolina (Ec)La Carolina (Ec)La Carolina (Ec)

0000

2222

21.525.7225.9720.78

31.6236.6130.7730.9

S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)

40-XII-17.140-XII-17.140-XII-17.140-XII-17.140-XII-17.1

eebbb

Quequen Grande (Ar)Quequen Grande (Ar)Quequen Grande (Ar)Quequen Grande (Ar)Quequen Grande (Ar)

100100100100100

3838383838

210.42210.53210.8329.6929.69

29.1928.9129.628.9228.25

S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)

40-XII.17.340-XII.17.344-XII.29.144-XII.29.1

bbde

Quequen Salado (Ar)Quequen Salado (Ar)Tapalque (Ar)Tapalque (Ar)

100100

5050

38383636

212.11211.9528.2629.02

33.1930.8229.1531.21

S. platensis (mid Pl)S. platensis (mid Pl)S. platensis (mid Pl)S. platensis (mid Pl)

68-X.31.168-X.31.171-II.14.171-II.14.1

eeee

Ensenada (Ar)Ensenada (Ar)La Plata (Ar)La Plata (Ar)

10101010

34343434

27.2827.3729.0628.99

28.7328.629.0729.0

S. platensis (mid Pl)S. platensis (mid Pl)S. platensis (mid Pl)

71-II.14.1288b1785 30.11

eee

La Plata (Ar)La Plata (Ar)A8 Pavon (Ar)

101010

343434

29.0325.927.0

30.2530.6029.98


31-VII.16.131-VII.16.131-VII.16.131-VII.16.131-VII.16.1

eeddb

Magdalena (Ar)Magdalena (Ar)Magdalena (Ar)Magdalena (Ar)Magdalena (Ar)

5050505050

3535353535

27.427.4628.128.2528.02

30.1230.0630.4930.3729.41


31-VII.16.187-XII.35.187-XII.35.187-XII.35.190-VIII.1.1

bdeed

Magdalena (Ar)Cant. Sr. Landa (Ar)Cant. Sr. Landa (Ar)Cant. Sr. Landa (Ar)Cant. Hdez. Orazi (Ar)

5010101010

3534343434

28.2626.0928.028.0529.08

29.4230.3130.7230.3629.99

S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)S. platensis (late Pl)

90-VIII.1.190-VIII.1.190-VIII.1.1MLP 505MLP8-407MLP 8-62

deeeed

Cant. Hdez. Orazi (Ar)Cant. Hdez. Orazi (Ar)Cant. Hdez. Orazi (Ar)Mercedes (Ar)Mercedes (Ar)Ayacucho (Ar)

101010505075

343434343437

28.6527.327.3828.7428.729.56

29.6330.4229.7630.4430.3232.76

C. hyodon (mid Pl)C. hyodon (mid Pl)C. hyodon (mid Pl)C. hyodon (mid Pl)C. hyodon (mid Pl)

MACN 505MACN 509MACN 509MACN 503MACN 503

btbbt

Tarija (Bo)Tarija (Bo)Tarija (Bo)Tarija (Bo)Tarija (Bo)

18661866186618661866

2121212121

27.2325.2526.0927.9528.05

26.1425.925.6524.925.72

C. hyodon (mid Pl)C. hyodon (mid Pl)C. hyodon (mid Pl)C. hyodon (mid Pl)

M4545M4569M4568SGO PV 145

eeee

Tarija (Bo)Tarija (Bo)Tarija (Bo)Ulloma (Bo)

1866186618663775

21212118

24.029.929.329.4

27.3023.3722.8621.52

S. waringi (late Pl)S. waringi (late Pl)

ee

Toca dos Ossos (Br)Toca dos Ossos (Br)

200200

1515

28.225.0

30.8028.95


TABLE 1. Continued.

Species (age)Specimennumber

Skeletaltissue Locality (country)

Alti-tudem.asl

Lati-tude

8Sd13C (CO3)

‰ PDB

d18O(CO3) ‰V-SMOW

C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)

SGO PV 17aSGO PV 15SGO PV 44SGO PV 235SGO PV 43

eeeee

El Parral (Ch)El Parral (Ch)Rio Bueno (Ch)Tierras Blancas (Ch)Tralmahue (Ch)

350350150300100

3636403340

212.5212.0213.1212.1213.9

26.0626.8826.1628.0226.88

C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)C. hyodon (late Pl)

SGO PV 40SGO PV 47aSGO PV 47j

eeee

ChileLimahuida (Ch)Tagua-tagua (Ch)Tagua-tagua (Ch)

500200200

323434

211.8211.3211.6212.8

26.4727.3026.8826.78

L. africana (extant)L. africana (extant)L. africana (extant)L. africana (extant)L. africana (extant)L. africana (extant)

Bocherens et al. 1996Bocherens et al. 1996Bocherens et al. 1996Bocherens et al. 1996Bocherens et al. 1996Bocherens et al. 1996

eeeeee

Amboseli (K)Amboseli (K)Amboseli (K)Amboseli (K)Amboseli (K)Amboseli (K)

115511551155115511551155

333333

27.325.7

210.2210.726.6

210.0

30.429.328.330.031.029.8

same type of tooth and from the same area, toavoid possible random results.

The samples (bones included) were finelyground in an agate mortar. The chemical pre-treatment of the samples was performed asdescribed by Koch et al. (1997) in order toeliminate secondary carbonate. About 40–50mg of powdered dentine and bone sampleswere soaked in 2% NaOCl for three days atroom temperature to oxidize organic matter.Residues were rinsed and centrifuged fivetimes with deionized water, and later treatedwith 1M acetic acid for one day to remove dia-genetic carbonates. Pretreatment of the enam-el differed slightly—samples were soaked in2% NaOCl for one day only. Carbon dioxidewas obtained by reacting approximately 40–50 mg of treated powder with 100% H3PO4 forfive hours at 508C. This CO2 was then isolatedcryogenically in a vacuum line. Results are re-ported as d 5 ([Rsample/Rstandard] 2 1) 3 1000,where R 5 13C/12C or 18O/16O, and the stan-dards are PDB for carbon and V-SMOW for ox-ygen. We applied data corrections for calciteto calculate the magnitude of the oxygen iso-topic fractionation between apatite CO2 andH3PO4 at 508C (Koch et al. 1989). Analyticalprecision for repeated analyses was 0.1‰ ford13C and 0.2‰ for d18O.

Recent studies by Bryant et al. (1996), Kohn(1996), and Kohn et al. (1998) have shown thatthe d18O isotopic values of phosphate (d18Op)and carbonate (d18Oc) in equid enamel are

strongly correlated and that the d18O of car-bonate is approximately 8.6‰ more positivethan the d18O of phosphate. In South America,Sanchez-Chillon and Alberdi (1996) found agood relationship between d18O results in car-bonate and phosphate apatite for gompho-theres and equids. In this present study, weanalyzed oxygen ratios in the phosphate andcarbonate phases of 30 new samples. For theanalysis of phosphate we followed the pre-chemical treatment procedure described byTudge (1960), which resulted in the precipi-tation of oxygen in the form of BiPO4. CO2 wasobtained by reacting BiPO4 with BrF5 as de-scribed by Longinelli (1965). All the sampleswere run in duplicate and the reported resultsare the mean of at least two consistent results.The isotopic results were reported against theV-SMOW standard and the analytical preci-sion for repeated analyses was 0.2‰. We per-formed both parametric (t-test) and nonpara-metric (Wilcoxon Signed-Rank) statisticaltests to evaluate d13C and d18O differences inmiddle and late Pleistocene populations. SPSS10.0 software was used for the statistical anal-ysis.

Analytical Results

When the PO432 and structural CO3

22 arecogenetic and the oxygen-bearing phases arein isotopic equilibrium with the same oxygenreservoir at the same temperature (for mam-mals the reservoir is body water at approxi-


mately 378C) a linear correlation should existbetween the d18Op and d18Oc values. In SouthAmerica, the equation obtained for Stegomas-todon from Argentina was (Sanchez-Chillonand Alberdi 1996): d18Oc 5 16.74 d18Op 1 0.64;R2 5 0.91. In our study, we calculated the cor-relation between pairs of d18Op–d18Oc valuesfor the enamel, dentine, and bone, taken fromthe jaw or maxilla of the same individual. Re-sults are reported in Table 2. The correlationsbetween the different PO4-CO3 pairs are:

Enamel18 18d O(PO ) 5 1.0348d O(CO ) 2 10.6574 3

2R 5 0.93

Dentine

18 18d O(PO ) 5 1.3048d O(CO ) 2 17.9274 3

2R 5 0.93

Bone

18 18d O(PO ) 5 1.6935d O(CO ) 2 0.71854 3

2R 5 0.99

The difference between d18Oc and d18Op val-ues is about 9.7‰ for enamel, 9.4‰ for den-tine, and 9.2‰ for bone. The calculated meanfor all three skeletal components is 9.5‰,which is the same as previously reported forArgentina by Sanchez-Chillon and Alberdi(1996).

Given the strong correlation among thethree skeletal phases, we believe that if dia-genetic modifications had occurred, all threeskeletal components would have been affectedequally. Like the isotopic composition of ox-ygen in phosphate, the isotopic compositionof oxygen in enamel, tooth, and bone carbon-ate for South American gomphotheres is inequilibrium with body fluid. Differences ob-served in the isotopic composition of d18O invarious gomphotheres groups were due to ad-aptations to climatic conditions and not to dia-genetic factors.

The positive correlations among both d13Cand d18O values demonstrate that the originalisotopic composition was well preserved inthe samples analyzed. The d13C isotopic valuesamong skeletal components (bone, dentine,and enamel) of the same fossil specimen were

generally very similar but did not always fol-low the same pattern of variation (Table 2).Value differences between dentine and enamelwithin the same individual were generallysmall, although in some cases the enamel pre-sented slightly more negative values (dentine5 0.8855enamel 1 2.8815; R2 5 0.9331). Byand large, bone results were similar to thoseof dentine (bone 5 0.9532dentine 1 0.4096; R2

5 0.9998), and in only one instance (31-VII-16-1) were bone isotopic values lower than thoseof the enamel (1.91‰). Given the strong, pos-itive correlation among pairs of the three skel-etal components, we considered the d13C re-sults of all components to be equally repre-sentative of both gomphothere groups, andwe used them collectively in the analysis ofthe data.

General Discussion and Interpretation

Initial evaluation and analysis showed thatd13C and d18O isotopic compositions were sig-nificantly different between Stegomastodon andCuvieronius. Further study also revealed thatover the middle and late Pleistocene the twogenera developed different feeding patterns aswell as different adaptations to climatic con-ditions. In addition, a relationship betweend13C and latitude was observed. This relation-ship was more evident for Stegomastodon thanit was for Cuvieronius. Isotopic oxygen valuesalso varied according to latitude and were fur-ther influenced by altitude.

Overall, the range of d13C values in Cuvieron-ius samples indicates that members of this ge-nus were mixed-feeders (Fig. 2). Carbon iso-topic data from Cuvieronius from Bolivia(MacFadden et al. 1994; MacFadden and Shock-ey 1997) suggest an adaptation from mixed-feeder to grazer. One notable exception was Cu-vieronius from Chile. The d13C values from thislocality were more homogeneous (rangingfrom 211.3‰ to 213.9‰), indicating thatspecimens of this group were exclusively C3

feeders (Table 3). The ecological pattern of thepopulations of Cuvieronius from Ecuador andBolivia agrees with the results described forthe modern elephant Loxodonta africana fromAmboseli Park (Bocherens et al. 1996).

Stegomastodon shows two different adapta-tions. Samples from Buenos Aires Province (ex-


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FIGURE 2. d18O versus d13C values of enamel, dentine, and bone for six groups of South American gomphotherescompared with results obtained by Bocherens et al. (1996) for the extant Loxodonta africana from Amboseli Park inKenya.

TABLE 3. Descriptive statistics for eight compared groups of South American gomphotheres. A, Cuvieronius, allspecimens. B, C. hyodon from Ecuador. C, C. hyodon from Bolivia. D, Stegomastodon, all specimens. E, S. platensis, allspecimens. F, S. platensis from late Pleistocene. G, S. platensis from middle Pleistocene. H, S. waringi, all specimens.I, S. waringi from Ecuador. J, S. waringi from Brazil. K, C. hyodon from Chile.

Groups nMean d13C

(‰)PDB SD (‰) Range (‰)Mean d18O

(‰)V-SMOW SD (‰) Range (‰)

ABCDEF

3012

9383225

29.0827.8427.4627.9828.6328.86

2.641.572.012.281.471.46

213.9 to 2429.71 to 25.129.9 to 24

212.11 to 20.78212.11 to 25.9212.11 to 26.09

24.4522.4024.8230.2630.0030.15

2.190.741.851.491.071.10

21.21 to 28.0221.21 to 23.7621.51 to 27.3028.25 to 36.6128.25 to 33.1928.25 to 33.19

GHIJK

76429

27.8024.5323.4926.6

212.34

1.242.842.732.260.82

29.06 to 25.928.2 to 20.7825.97 to 20.7828.2 to 25

213.9 to 211.3

29.4631.6132.4829.8826.83

0.802.612.781.310.59

28.6 to 30.6028.95 to 36.6130.77 to 36.6128.9 to 30.8026.06 to 28.02

cept for Quequen Salado samples) and Brazilindicate that these species were mixed-feederswhereas those from La Carolina (Ecuador)were mostly C4 feeders. Parametric (t-test) andnonparametric (Wilcoxon) statistical tests con-firm significant differences between thesegroups (Table 4).

Ayliffe et al. (1992) analyzed the d18Op valuesfor the two species of modern elephants fromAsia and Africa, and found that a good corre-lation existed between the d18O of ingested wa-ter and the d18O of tooth and bone phosphate:d18Op 5 0.94d18Ow 1 23.3 (R2 5 0.85). Multi-

variate statistical analysis reveals that, in ele-phants in this humidity range, the fraction-ation mechanisms on phosphate due to the in-gestion of water from consumed vegetation donot have a significant influence on phosphated18O.

The distribution range of d18O values clearlydifferentiates Cuvieronius from Stegomastodon(Fig. 2). The former, which dispersed into highaltitudes through the Andes corridor, showsd18O values ranging from 21.6‰ to 28‰. Ste-gomastodon species that dispersed through theeastern route (Argentina and Brazil) and the


TABLE 4. Results of parametric (t-test) and nonpara-metric (Wilcoxon Signed Rank) tests performed on 12possible paired comparisons between two genera ofSouth American gomphotheres. For definition ofgroups, see Table 3.

VariableComparison

groups t-test pNonparametric

p

d13Cd13Cd13Cd13Cd13C

A vs. DC vs. FB vs. CE vs. FG vs. H

0.1390.0190.9240.3160.038

0.140.020.770.610.03

d13Cd13Cd13Cd13Cd18O

B vs. HB vs. KC vs. KI vs. JA vs. D

0.0602.35 3 1026

0.000.571.15 3 10211

0.050.010.010.65

1.73 3 1026

d18Od18Od18Od18O

C vs. FB vs. CE vs. FG vs. H

2.53 3 10210

0.000.100.15

0.010.010.130.07

d18Od18Od18Od18O

B vs. HB vs. KC vs. KI vs. J

0.008.95 3 1027

0.020.43

0.030.010.030.18

coastal area from Ecuador show a range of28.6–36.6‰. Statistical analyses reveal signifi-cant differences between both genera of gom-photheres (Table 4). The d18O range of Stego-mastodon from Brazil is similar to that of the ex-tant Loxodonta africana from Amboseli Park(Bocherens et al. 1996).

Substantial differences in isotopic compo-sition are also observed between these twogenera as they evolve from the middle to thelate Pleistocene (Fig. 3A). Stegomastodon fromthe middle Pleistocene of Buenos Aires fed ona mixed diet, as their isotopic values are morehomogeneous, ranging from 25‰ to 29‰.Alternatively, Stegomastodon from late Pleisto-cene exhibit a wider range of diet adaptationsthat includes an exclusively C3 diet (QuequenSalado), a mixed C3-C4 diet (Buenos Aires),and a diet completely composed of C4 plants(Ecuador). The dietary regimes of Cuvieroniussamples from middle and late Pleistocene, onthe other hand, show less variation. With theexception of the strictly C3 feeding Cuvieroniusof the late Pleistocene in Chile, mixed feedingpredominated in both the middle Pleistocene(Bolivia) and the late Pleistocene (Ecuador). Atrend from a mixed C3-C4 diet in the middlePleistocene to a more strictly C3 diet in the up-

per Pleistocene can be more clearly observedin the Buenos Aires remains.

MacFadden et al. (1999), using the distri-bution of Pleistocene Equus in America,showed a general d13C gradient that seems tobe symmetrical on either side of the equator.The isotopic transition between plants with C4

photosynthetic pathway to plants with C3

pathways is observed in the Northern Hemi-sphere at about 458N, with mean d13C valuesmore positive than 210‰. The proportion ofC3 and C4 grasses in modern ecosystemsvaries with latitude, and the crossover be-tween C3 versus C4 dominance in grasslandsoccurs at about 40–458 latitude in the NorthernHemisphere (Ehleringer et al. 1997; Epstein etal. 1997; Tieszen et al. 1997). In the SouthernHemisphere we observed the transition to C3

feeding at around 35–418S (Fig. 4). Samplesfrom Quequen Salado (Buenos Aires Prov-ince), at approximately 388S latitude show ad13C mean value of 212.03‰, whereas sam-ples from Chile (several localities at approxi-mately 35–418S) show a d13C mean value of212.3‰. The most southern locality (Tral-mahue, 408S) presents the most negative val-ues (213.9‰). This progression of more neg-ative values south of the equator confirms alatitudinal gradient for the Southern Hemi-sphere, similar to that observed by Mac-Fadden et al. (1999).

There are also significant differences be-tween d18O values for the two middle Pleisto-cene localities (Table 4, Fig. 3B). Cuvieroniussamples from Tarija, Bolivia (altitude 2000 masl) have clearly lower d18O values than do Ste-gomastodon samples from Buenos Aires (sealevel). For the late Pleistocene, the range of d18Ovalues in high-altitude and equatorial samples(16‰, 21.2–36.6) demonstrates the effects of analtitudinal gradient. Specimens from Chilepresent the lowest values (between 21‰ and24‰), which correspond to the lowest climaticrecord. Samples from La Carolina (Ecuador),on the other hand, present values that corre-spond with more temperate conditions (26‰to 20.8‰). In Ecuador, high continental Cu-vieronius samples, from altitudes of 3000 m asl,show a lower temperature record than Stego-mastodon samples from La Carolina peninsula.The effects of altitude and latitude on d18O may


FIGURE 3. Variation in d13C (A) and d18O (B) during the middle and late Pleistocene for South American Cuvieroniusand Stegomastodon. BBAA 5 Buenos Aires.

also explain the higher temperature climatic re-cords obtained for the Buenos Aires province(sea level, latitude 348 to 398S), where samplesshowed d18O values ranging from 28.6‰ to33.19‰. In quantifying these effects, we founda correlation between d18O values and altitude.The equation obtained was (Fig. 5): d18O 520.0026 · Altitude 1 29.93 (R2 5 0.79). Takinginto account all the samples of South Americangomphotheres analyzed, we obtained an alti-tudinal gradient of 20.28 d unit/100 meters.Results for samples of Buenos Aires Provinceappear to indicate that there was no substantialtemperature change from the middle Pleisto-cene to upper Pleistocene.

Both Buenos Aires and Brazil Stegomastodond18O values were in the range expected for ac-tual African herbivores inhabiting a semiarid

and seasonal rainfall climate (Koch et al. 1995;Bocherens et al. 1996).

Gomphothere Extinction in South America.Currently, two main theories are accepted aspossible explanations for the extinction ofSouth American gomphotheres. One theory at-tributes their extinction to the direct impact ofhumans through hunting activities. Martin(1984), the main advocate of this hypothesis,proposed that the extinction of large mammalsfrom North America, South America, and Aus-tralia was related to sudden human expansionon these continents. This ‘‘overkill’’ hypothesisis supported by the synchronism of extinctionwith the arrival of large numbers of humans tothese continents. The archaeological recordfrom South America shows that gomphothereswere common in Paleo-Indian sites. Gom-


FIGURE 4. Distribution of d13C results for South American gomphotheres with the corresponding latitude of thesites from which they came.

FIGURE 5. Correlation obtained from linear regression of d18O for South American gomphotheres with the corre-sponding latitude of the sites from which they came.


photheres appear to have been a human foodresource in central and southern Chile (Dille-hay and Collins 1988; Montane 1968), Colom-bia (Correal Urrego 1981), and Venezuela (Bry-ant et al. 1978) between ca. 13,000 and 11,000yr B.P. Gomphotheres are also present in thePampean Region during this time but no as-sociation with human remains has yet been re-corded. Therefore, it is possible that human ac-tivities, such as hunting pressure or habitat dis-turbance, affected the Pleistocene population ofgomphotheres (Politis et al. 1995).

Other authors suggest that climatic and eco-logical changes, particularly nutritional stressinduced by rapid change in plant communities,may have been the principal cause of gom-phothere extinction (Janzen and Martin 1982;Graham and Lundelius 1984; King and Saun-ders 1984). With this in mind, Guthrie (1984)hypothesized that plant diversity was greaterand the growing season was longer in the Pleis-tocene than in the Holocene.

Specimens from the middle Pleistocene inSouth America exhibit feeding strategies simi-lar to those of modern elephants, which live indiverse habitats, are opportunists, and there-fore are capable of living on nearly any dietarymixture (Bocherens et al. 1996). In contrast,populations from late Pleistocene show moreselective dietary adaptations, which suggestthat gomphotheres were driven to extinctionbecause they were specialized feeders, adaptedto a kind of plant that disappeared during theHolocene. The record from the Pampean Re-gion shows that large mammal extinctionswere correlated with climate change, a processthat began before the arrival of humans (Pradoet al. 2001).

Mammoths, Gomphotheres, and the Great Amer-ican Biotic Interchange. About 2.5 Myr ago,tectonic activities along the Pacific margincaused the connection of the American conti-nents. As a result, a habitat corridor openedthat facilitated the dispersal of terrestrial plantsand animals into and out of South America,precipitating an event known as the ‘‘GreatAmerican Biotic Interchange’’ (Webb 1976,1991). This land bridge functioned as an eco-logically selective dispersal corridor (Webb1978; Simpson 1980). Biogeographic data in-dicate that three major types of Plio-Pleistocene

habitat corridors existed on the Panamanianland bridge: mesic tropical forest, mesic savan-na, and xeric scrub savanna (Webb 1978). Dur-ing the humid interglacial phase, rain forestsdominated the tropics, and the principal bioticmovement was from Amazonia to CentralAmerica (south to north). During the more aridglacial phase, when savanna habitats predom-inated and extended well into tropical lati-tudes, the directional pattern reversed, and bi-otic forms moved from north to south (Webb1991).

Before the interchange, Cuvieronius (Gom-photheriidae), Mammuthus (Elephantidae),and Mammut (Mammutidae) were recorded inFlorida and Honduras. There appears to be nobiological explanation why Mammuthus andMammut, which might have been expected tocross the Panamanian land bridge, did notreach South America. The reason may befound in the diet and habitat preferences ofthese genera. Mammut have relatively low-crowned molars with cusps arrayed in widelyspaced lophs. This dental morphology led tothe recognition of mastodons as browsers(Webb et al. 1992). Mammoths (Mammuthus)have high-crowned molars with closelyspaced enamel lophs coated with cementum,a feature that identifies them as grazers (Daviset al. 1985). Isotopic analyses confirm this hy-pothesis (MacFadden and Cerling 1996). Thegomphotheres from West Palm Beach, Florida,and from middle Pleistocene of South Amer-ica have d13C values that are intermediate iso-topic values between browsers and grazers(Koch et al. 1998; Connin 1998). Mammothand mastodon species were more specializedfeeders than Cuvieronius, which was a mixed-feeder. We propose that the different feedingpreferences among mastodons, mammoths,and gomphotheres could explain why onlythe bunodont forms reached South America.

Concluding Remarks

The carbon and oxygen isotopic compositionof three skeletal elements (enamel, dentine, andbones) was studied in 68 samples of SouthAmerican gomphotheres. The high positivecorrelations among the three different skeletaltissues (enamel, dentine, and bone) and d18Op–d18Oc allowed us to use all the data to recon-


struct the paleoenvironment and paleoclimateof the area.

Carbon isotopic analysis (d13C) revealed var-ious types of dietary adaptations among Pleis-tocene gomphotheres from South America: Cu-vieronius from Chile fed on C3 plants exclusive-ly, whereas other specimens of the genus had amixed C3-C4 diet. The genus Stegomastodonshowed a broader range of dietary adaptations,including predominantly C3 feeders (QuequenSalado in Buenos Aires Province), exclusivelyC4 feeders (in La Carolina Peninsula, Ecuador),and mixed C3-C4 feeders (from the remainingSouth American localities analyzed).

The temporal evolution of the two genera in-dicates that during the middle and late Pleis-tocene genus Cuvieronius appeared to be iso-topically mixed-feeders, although samplesfrom Chilean populations appeared to be sole-ly C3 plant eaters. Stegomastodon seem to haveadapted from a C3-C4 diet in the middle Pleis-tocene to a broader dietary range in the latePleistocene, during which some populationswere exclusively C3 or C4 feeders, and otherswere mixed C3-C4 feeders.

The oxygen isotopic composition did notvary greatly between middle and late Pleisto-cene samples for either genera. The variation inthe range of temperatures presented by the twogenera corresponds to their different dispersalroutes. Cuvieronious dispersed at high altitudesvia the Andes route, whereas Stegomastodon fol-lowed an eastern route.

Generally, the genus Cuvieronius showedlower oxygen isotopic values than Stegomasto-don, a difference that can be explained by theformer’s geographical distribution at higher al-titudes.

Carbon isotopic values showed an adaptivechange to C3 feeding along a latitudinal gra-dient. This occurred at approximately 35–418S(mean value 212.3‰) in Chile, and at approx-imately 398S (mean value of 210.7‰) in Bue-nos Aires Province. We also obtained a meanaltitudinal gradient for South America of 20.28d unit/100 m from d18O values.

The early Cuvieronius and Stegomastodon ap-parently entered South America in early ormiddle Pleistocene during the more arid gla-cial phase, when savanna habitats extendedbroadly through tropical latitudes. The most

likely explanation for the absence of Mammutand Mammuthus in South America is that theywere highly specialized feeders with habitatpreferences not represented in the Panamanianland bridge.

Acknowledgments

We would like to thank the curators of theMuseo de La Plata and the Museo Argentino deCiencias Naturales ‘‘Bernardino Ribadavia,’’Argentina; the Museo de la Escuela PolitecnicaNacional de Quito, Ecuador, and especially S.Lopez, who was responsible for the samples; theIsotope Geochemistry Laboratory at the Univ-ersita di Trieste; and the Servicio de IsotoposEstables of the Universidad de Salamanca. Themanuscript was greatly improved by thoughtfulreview from E. Cerdeno, B. MacFadden, andtwo anonymous referees. J. Watkins revised theEnglish text. This work was supported by anEuropean Community project CI1*-CT90–0862(B. Sanchez Chillon contract no. ERBCH-BICT930742 at the University of Trieste); a jointResearch Project from the Agencia Espanola deCooperacion Iberoamericana, Spain–Argentina(1994–96 and 2001–2002); Projects PB94–0071and PB97–1250 from the Direccion General deInvestigacion Cientıfica y Tecnica of Spain;grants from the Universidad Nacional del Cen-tro and from the Project PID-CONICET, Argen-tina.

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Documents

Feeding ecology, dispersal, and extinction of South American Pleistocene gomphotheres (Gomphotheriidae, Proboscidea)