ORIGINAL PAPER

The South American Gomphotheres (Mammalia,Proboscidea, Gomphotheriidae): Taxonomy, Phylogeny,and Biogeography

Dimila Mothé & Leonardo S. Avilla & Mario A. Cozzuol

# Springer Science+Business Media, LLC 2012

Abstract The taxonomic history of South American Gom-photheriidae is very complex and controversial. Three speciesare currently recognized: Amahuacatherium peruvium,Cuvieronius hyodon, and Notiomastodon platensis. The for-mer is a late Miocene gomphothere whose validity has beenquestioned by several authors. The other two, C. hyodon andN. platensis, are Quaternary taxa in South America, and theyhave distinct biogeographic patterns: Andean and lowlanddistributions, respectively. South American gomphotheres be-came extinct at the end of the Pleistocene. We conducted aphylogenetic analysis of Proboscidea including the SouthAmerican Quaternary gomphotheres, which resulted in twomost parsimonious trees. Our results support a paraphyleticGomphotheriidae and a monophyletic South Americangomphothere lineage: C. hyodon and N. platensis. The lateMiocene gomphothere record in Peru, Amahuacatherium

peruvium, seems to be a crucial part of the biogeographyand evolution of the South American gomphotheres.

Keywords South American Gomphotheres . Systematicreview . Taxonomy. Proboscidea

Introduction

The family Gomphotheriidae is, so far, the only group ofProboscidea recorded in South America. Together with themegatheriid sloths Eremotherium laurillardi Lund, 1842,the Megatherium americanum Cuvier, 1796, and thenotoungulate Toxodon platensis Owen, 1840, they are themost common late Pleistocene representatives of the mega-fauna in South America (Paula-Couto 1979). Similar to thePleistocene and Holocene members of the family Elephan-tidae (e.g., extant elephants and extinct mammoths), theSouth American gomphotheres are characterized by havinga brachycephalic and brevirostrine skull, a short and curvedmandibular symphysis, and specialized dentition, whichconsists of a pair of upper tusks (second incisors) and sixpairs of upper and lower molars (Simpson and Paula-Couto1957; Paula-Couto 1979; Prado et al. 2001; Ferretti 2008a).

Taxonomy and Diversity of South AmericanGomphotheres

The taxonomic history of the South American gompho-theres is long and complex. Most authors consider that theywere represented by three genera: Cuvieronius Osborn,1923, Haplomastodon Hoffstetter, 1950, and StegomastodonPohlig, 1912 (Simpson and Paula-Couto 1957; Ficcarelli et al.1995; Ferretti 2008a, 2010). Later, some authors (Alberdi and

D. Mothé (*)Programa de Pós-graduação em Ciências Biológicas (Zoologia),Museu Nacional/UFRJ,Quinta da Boa Vista,20940-040, Rio de Janeiro, RJ, Brazile-mail: dimothe@hotmail.com

L. S. AvillaDepartamento de Zoologia, Instituto de Biociências,Laboratório de Mastozoologia,Universidade Federal do Estado do Rio de Janeiro,Avenida Pasteur, 458, Urca, 22290-240,Rio de Janeiro, RJ, Brazile-mail: leonardo.avilla@gmail.com

M. A. CozzuolDepartamento de Zoologia, Instituto de Ciências Biológicas,Universidade Federal de Minas Gerais,Avenida Antônio Carlos, 6627, Pampulha,31270-910, Belo Horizonte, Minas Gerais, Brazile-mail: cozzuol@icb.ufmg.br

J Mammal EvolDOI 10.1007/s10914-012-9192-3

Prado 1995; Alberdi et al. 2002, 2004, 2007; Prado et al.2005; Prado and Alberdi 2008) synonymizedHaplomastodonwith Stegomastodon, reducing the diversity of genera, butkeeping three species: Cuvieronius hyodon (Fischer, 1814),Stegomastodon platensis (Ameghino, 1888), and S. waringi(Holland, 1920). Very recently, Mothé et al. (in press)proposed to include the last two species in a single species,under the nameNotiomastodon platensis, as first suggested byMadden (1984).

The first report of gomphothere remains from SouthAmerica was made by Cuvier (1806), who analyzed anisolated left M2 from Imbabura, northern Ecuador, andnamed it as the “Mastodonte des Cordilliéres.” In 1824,Cuvier established the formal names Mastodon andium forthe Imbabura (Ecuador) gomphotheres and M. humboldtiifor a molar from Concepción (Chile). Before this study,Fischer (1814) analyzed the same specimen from Imbabura,and named it as Mastotherium hyodon, which has priorityover Mastodon andium (see Cabrera 1929). The genusCuvieronius was erected by Osborn (1923) and later,Cabrera (1929), in a revision of the Argentine gompho-theres, synonymized Mastodon argentinus Ameghino, 1888,under the name Cuvieronius hyodon (Fischer, 1814).

Ficcarelli et al. (1995), in a taxonomic revision of Cuvier-onius, validated C. tarijensis (Ameghino, 1902), and pro-posed the material referred to C. tarijensis from Tarija,Bolivia, as the topotype for the species. Recently, Lambertand Shoshani (1998) considered C. hyodon as the typespecies of Cuvieronius, but Lucas (2009) argued that thegenus is monospecific, considering C. tropicus Cope, 1884,from Mexico, as a junior synonym of C. hyodon. Lucas(2009), in order to solve the taxonomic problem of the nameMastotherium hyodon, suggested to keep the name Cuvier-onius and consider M. hyodon as its type species, by desig-nating a neotype toM. hyodon (the skull and lower jaw fromTarija, Bolivia originally described and illustrated by Bouleand Thevenin (1920)).

The diagnostic material of C. hyodon comes from Tarija,Bolivia, where several skulls and postcranial remains werefound (Marshall and Sempere 1991; Coltorti et al. 2007).Cuvieronius hyodon is a short-jawed gomphothere charac-terized by having a depressed and elongated cranium, a pairof twisted upper tusks, which have a spiraled enamel bandalong their entire length, and lower deciduous incisors insome juveniles (Prado et al. 2005; Ferretti 2008a, b).

The first one to review the taxonomy of South Americanlowland gomphotheres was Florentino Ameghino (1888,1889, 1891), who defined four species that he placed inthe genusMastodon. After that, the Argentinean fossils wereagain reviewed by Cabrera (1929), who synonymized somespecies described by Ameghino (1889) and transferred themto the North American genus Stegomastodon, recognizingonly two species: S. platensis and S. superbus. He also

proposed a new genus and species, Notiomastodon ornatus,based on a short, massive tusk and a dentary from Playa delBarco, Argentina. Hoffstetter (1950) proposed Haplomasto-don as a subgenus of Stegomastodon and, in 1952, elevatedHaplomastodon to full generic status, based on the absenceof transverse foramina in the atlas (1st cervical vertebra). Healso included all Brazilian gomphotheres in a new speciesStegomastodon brasiliensis Hoffstetter, 1952. The trans-verse foramen of the axis was recognized as a variablecharacter by Simpson and Paula-Couto (1957), and theyplaced all Brazilian gomphotheres in Haplomastodon war-ingi (Holland, 1920). Ficcarelli et al. (1995), based ondiagnostic gomphothere remains from northern Ecuador,synonymized all Haplomastodon species with H. chimbor-azi (Proaño, 1922). Alberdi and Prado (1995) included thespecies S. superbus (Ameghino, 1888), and N. ornatus in S.platensis. The genus Haplomastodon was later synony-mized with the genus Stegomastodon, generating the newcombination S. waringi (Alberdi et al. 2002). Lucas andAlvarado (2010) used the combinations Notiomastodon pla-tensis, in replacement of S. platensis, which was previouslysuggested by Madden (1984) and Ferretti (2008a). Ferretti(2010) used the combination Haplomastodon chimboraziand employed quote marks for “Stegomastodon” platensis,arguing that the South and North American species attribut-ed to this genus are not congeneric with S. mirificus (Leidy,1859), the type species of the genus, from North America.Mothé et al. (in press) reviewed the Pleistocene SouthAmerican lowland gomphotheres and concluded that theybelong to a single species for which the valid name is Notio-mastodon platensis. Consequently, only two gomphotherespecies were present in the Quaternary of South America:the Andean Cuvieronius hyodon, and the lowland Notiomas-todon platensis (Fig. 1).

The holotype of Notiomastodon ornatus (Museo Argen-tino de Ciencias Naturales “Bernardino Rivadavia,” collec-tion number MACN 2157) is described by Cabrera (1929),and it is a mandible with a short symphysis, without lowerincisors, bunolophodont molars with several accessory con-ules (double trefoil wear pattern), and short, massive andupper curved tusk with lateral enamel band (Cabrera 1929:Figs. 2-4). Furthermore, Stegomastodon platensis is de-scribed as having a variable wear pattern on the molars,more complex than Haplomastodon chimborazi, andstraight to slightly upper curved tusks, without enamel band(Prado et al. 2005). Both genera show a similar tusk mor-photype and should represent the same taxon, in whichNotiomastodon has priority and Stegomastodon is not ap-plicable to the South American species (Mothé et al. inpress). A brachycephalic skull with a high parieto-occipitalregion, a pair of straight or curved upper tusks with absenceof spiraled torsion, complex molar teeth with double-trefoiland simple-trefoil wear patterns (Mothé et al. in press)

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characterize the species N. platensis. Cabrera (1929) indi-cates that Cuvieronius hyodon have a low and long skull,large upper tusks with twisted enamel band, lack of lowertusks in adults, and short dentary symphysis. Otherwise, thegenus Stegomastodon is represented in North America bythree species: S. primitivus, S. mirificus, and S. aftoniae(Lucas et al. 2011). The genus is characterized by a skullwith a tall frontal and parietal region, long and relativelystraight tusks that lack enamel, no lower tusks, the mandib-ular symphysis is relatively short and tall, and the m3 hasfive lophids and double trefoils. It differs from Notiomasto-don in some structures of the scapula, humerus, pelvis, andfemur, and it seems to have a greater degree of graviportalitythan South America gomphotheres (Lucas et al. 2011).

The discovery and description of Amahuacatherium peru-vium (Romero-Pittman, 1996), a gomphothere with vestigiallower incisors from the late Miocene (approximately 9.5–9.0MyBP) of the Peruvian Amazonia, has inspired a great con-troversy (Campbell et al. 2000, 2006, 2009, 2010; Alberdi etal. 2004; Woodburne 2010). Some authors have stated that theholotype of A. peruvium is, actually, a specimen of Stegomas-todon (Alberdi et al. 2004), its proposed age is mistaken, andits primitive features (lower incisors and simpler molars withcomplexity similar to Haplomastodon) were misinterpreta-tions caused by its fragmentary nature and taphonomomicprocesses (Alberdi et al. 2004; Woodburne 2010). Recently,Campbell et al. (2009, 2010) have refuted the critics on themorphological features and age of Amahuacatherium. The

presence of pre-Quaternary gomphotheres in South Americaremains an open issue and more studies are needed to eluci-date the evolutionary history of South American proboscideans.

The only consensus about proboscidean history in SouthAmerica is that they became extinct by the end of thePleistocene (Ficcarelli et al. 1997; Prado et al. 2001; Alberdiet al. 2002; Sánchez-Chillón et al. 2004; Prado et al. 2005),but the causes for their extinction are still unresolved.

Biogeography of South American Gomphotheres

Under the traditional view, gomphotheres arrived in SouthAmerica during the Great American Biotic Interchange(GABI), after the establishment of the Panamanian Isthmusat 3.1–2.8 MyBP (Coates and Obando 1996), a land-bridgethat connects North and South America through Central Amer-ica (Cione and Tonni 2001; Coltorti et al. 2007; Woodburne2010). However, the record of theAmahuacatherium peruviumfrom the lateMiocene Amazonian lowlands of Peru (Campbellet al. 2000, 2006, 2009) would indicate, if its morphologicalfeatures are accurately interpreted and its age is correct, thatproboscideans were present in South America prior to themainstream of the GABI. Besides Amahuacatherium, other speciesalso have an early “arrival” into South America, such asprocyonid carnivorans and sigmodontine rodents (Woodburne2010). Furthermore, ground sloths and terror birds reachedNorth America at the same time (Woodburne 2010 andreferences cited there). Consequently, the beginning ofthe GABI could have started approximately ten millionyears ago, with a brief period of global sea level drop thatallowed the emergence of a small land connection betweenCentral and South America. Between 10.71 and 9.36 MybP,calcareous nannofossils indicate a separation between theCaribbean and the east Pacific during this time, comparedwith the early and middle Miocene. This was followed bya reinstatement of a deeper connection between 8.35 and3.65 MybP between the Caribbean Sea and the eastern equa-torial Pacific, and a final closure of the Isthmus of Panamaby 2.76 MybP (Kameo and Sato 2000). About the samegeological variations are observed in the sedimentologicalrecord by Coates et al. (2004).

In North and Central America, the genus Cuvieronius has acontinuous distribution while the genus Stegomastodon has adiscontinuous distribution in Central America (Arroyo-Cabraleset al. 2007). This observation has led some authors to suggestthat a taxonomic review of the South American species referredto Stegomastodon is needed (Arroyo-Cabrales et al. 2007;Ferretti 2008a, 2010; Lucas et al. 2011).

During the Pleistocene, each of the South Americangomphotheres spread throughout the continent in two dif-ferent “corridors.” In the Andean or highland “corridor,”Cuvieronius hyodon was dominant, spreading in the present

Fig. 1 Main differences between the South American Quaternarygomphotheres. a anterior view of a Notiomastodon platensis highcranium (reconstructed, based on Cabrera 1929) with straight uppertusks from Arrecifes, Buenos Aires province, Argentina (MLP 8-1,Museo de La Plata paleontological collection). b anterior view of aCuvieronius hyodon low cranium with twisted upper tusks from Tarija,Bolivia (MACN Pv 1291, Museo Argentino de Ciencias Naturales“Bernardino Rivadavia” paleontological collection). c lateral view ofthe same specimen described in a. d lateral view of the same specimendescribed in b

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countries of Colombia, Ecuador, Bolivia, Peru, and Chile, andthe lowland “corridor,” where Notiomastodon platensisprevailed in Brazil, Ecuador, Venezuela, Colombia,Argentina, Uruguay, Paraguay, and the western coastalareas of Peru and Chile (Simpson and Paula-Couto1957; Alberdi and Prado 1995; Prado et al. 2001;Alberdi et al. 2002; Ferretti 2008a, 2010; Mothé et al. in press;Fig. 2). Cuvieronius hyodon seems to be adapted to live in thehighlands, which is supported not only by its geographicdistribution, but also by stable isotope analysis (Sánchez-Chillón et al. 2004). On the other hand, the lowland gompho-there, Notiomastodon platensis, seems to avoid drier environ-ments (Winck et al. 2010).

Phylogeny of South American QuaternaryGomphotheres

The phylogenetic relationships of South American gompho-theres are another controversial issue and it is directly

related to their unsolved taxonomic problems. Previousphylogenies by Shoshani et al. (2006) include 125 char-acters and 40 terminals at the generic level; however,they published only a simplified cladogram at the fam-ily level; Prado and Alberdi (2008) conducted a cladis-tic analysis of the trilophodont gomphotheres, withemphasis on the South American species. This phylog-eny is problematic in many points, which invalidateboth the phylogeny itself and the biogeographic analysisbased on it, as shown by Cozzuol et al. (in press).Furthermore, several recent studies of the group (Arroyo-Cabrales et al. 2007; Ferretti 2008a, 2010; Lucas andAlvarado 2010; Cozzuol et al. in press; Mothé et al. inpress) show the necessity of a systematic revision of theSouth American gomphotheres.

This study proposes a new systematic and biogeographicview for the South American Pleistocene gomphotheres andpresents inferences about the relation of these taxa withinthe family Gomphotheriidae that follows the taxonomicreview conducted in Mothé et al. (in press).

Fig. 2 Map of the geographicaldistribution of South Americangomphotheres during thePleistocene. The circlesrepresent Notiomastodonplatensis and the trianglesrepresent Cuvieronius hyodon.Modified from Simpson andPaula-Couto (1957), Alberdi etal. (2002), Cione et al. (2005),Ferretti (2008a), and Lucas(2008)

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Materials and Methods

A phylogenetic analysis was performed in order to elu-cidate the relationships of the South American gompho-theres. We modified the original matrix from Cozzuolet al. (in press, modified from Shoshani et al. 2006),by reviewing some features and merging “Stegomastodon”platensis and Haplomastodon waringi into Notiomastodonplatensis. We also recognized Stegomastodon only byNorth American species and we recoded the characterstates for this genus based only on these species (Arroyo-Cabrales et al. 2007; Ferretti 2008a, 2010; Lucas et al.2011). We are in agreement with Ferretti (2008a, 2010),Lucas et al. (2011), and Mothé et al. (in press), whoconsider that Stegomastodon is not present in SouthAmerica.

We ran the taxon-character matrix with TNT software(Goloboff et al. 2008) using the “Implied weighting” set-ting, with K06, and conducted the search using defaults of“xmult” command to finding optimal score 20 times inde-pendently, plus ten cycles of tree-drifting strategies (Goloboffet al. 2008). Group supports are calculated by TBR-swappingthe trees found, keeping note of the number of steps needed tocollapse each group.

Results and Discussion

The phylogenetic analysis conducted here resulted in twomost parsimonious trees with 7.31205 fit as the best scoreand the consensus of these two trees is represented in Fig. 3.Accordingly, the family Gomphotheriidae (sensu Shoshaniet al. 2006) is paraphyletic. This is not a new argument;Maglio (1972), Tassy (1996), and Arroyo-Cabrales et al.(2007) also rejected the monophyly of the family Gompho-theriidae. Moreover, Shoshani and Tassy (1996) also arguedthat it requires too many changes to group all taxa tradition-ally incorporated in “gomphotheres.” To consider this taxona natural group, it must include the monophyletic Elephan-tidae and Stegodontidae (Fig. 3, Clade 1). This clade, namedElephantida, was also recognized by Shoshani et al. (2006).In our results, the Elephantida includes several lineages(Fig. 3): a basal great polytomy compromising most of thetraditional gomphotheres, the monophyletic (Notiomastodonplatensis and Cuvieronius hyodon), and the four consecutivesister-taxa of Elephantoidea (Elephantidae plus Stegodontidaeby Shoshani et al. 2006), which are (Stegomastodon mirificus(Tetralophodon (Anacus (Paratetralophodon)))). The Ele-phantida is diagnosed here by the presence of a postcingulumon the lower third permanent molars (character 124, state 1).

Fig. 3 Resulting consensustree based on the matrixmodified from Shoshani et al.(2006) and Cozzuol et al. (inpress), including the new taxonNotiomastodon platensis. Theclade 1 represents Elephantidaand clade 4 represents the SouthAmerica Quaternarygomphotheres

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The development of the postcingulum in “gomphotheres” canbe associated with the increase in number of loph(id)s inElephantida, which are tetra, penta, or have more than fivelophids on the third lower molars. Tassy (1996) recognized anevolutionary trend for the Proboscidea toward the augmenta-tion on cusps due to the subdivision of the main mammaliancusps and by the increase in number of loph(id)s. The incre-ment in crown morphology in Elephantida, compared to otherProboscidea, was probably positively selected in response to amore abrasive and complex herbivorous diet in most of thecontinents after the spread of grasslands from the early Mio-cene on.

Themonophyletic clade 2 comprises clade 3, (Stegomastodonprimitivus (Tetralophodon (Anancus (Paratetralophodon (Ele-phantoidea))))), and the natural group Notiomastodon platensisplus Cuvieronius hyodon (clade 4) (Fig. 3). Clade 2 is diagnosedby M3 with postentoconule, pentaloph or with more than fivelophs on the molars (character 34, state 5), and a short and spout-like mandibular symphysis (character 94, state 2). With theexception of Cuvieronius hyodon and Tetralophodon, in which

some specimens bear vestigial (or reduced) and deciduous man-dibular tusks (Ferretti 2008b), all members of clade 2 lackmandibular tusks and are brevirostrine. This brevirostrine condi-tion, an extreme mandible shortening, was possible probablybecause of the horizontal teeth displacement condition evolvedin the Elephatimorpha (Shoshani et al. 2006). Therefore, in themembers of clade 2, the brevirostrine condition probably allowedthe reduction in the number of erupted molars, where only onemolar or one molar plus part of the successive adjacent tooth arein use at the same time on each half jaw.

The monophyletic clade 3 is diagnosed by m2 with fourdistinct lophids (character 33, state 3, tetralophodont) andM2 with four or more distinct lophs (character 40, state 2).Thus, the tendency for increase in the number of loph(id)s isalso observed in clade 3, but it occurs on the second upperand lower molars, which have more loph(id)s when com-pared to the other taxa in Elephantida. The most basal taxonof this clade, Stegomastodon mirificus, is represented hereby the genus Stegomastodon, which is endemic to NorthAmerica (Ferretti 2010; Lucas et al. 2011; Mothé et al. in

Fig. 4 Five possible systematic combinations involving Amahuacathe-rium peruvium and the gomphotheres recorded in South America, Cuvier-onius hyodon and Notiomastodon platensis. a the suggested clade is (C.hyodon and N. platensis), with South American arrival at the GreatAmerica Biotic Interchange. b the suggested clade is (C. hyodon and N.platensis) with A. peruvium synonymized with N. platensis. c the sug-gested clade is (Cuvieronius hyodon (Amahuacatherium peruvium andNotiomastodon platensis). d the suggested clade is (Amahuacatheriumperuvium (Notiomastodon platensis and Cuvieronius hyodon). e the sug-gested clade is (Notiomastodon platensis (Amahuacatherium peruviumand Cuvieronius hyodon). Important moments in the evolutionary and

biogeographic histories of gomphotheres in Americas: 1) Shortland connection between Central and South Americas at 10.71to 9.36 MyBP. 2) A. peruvium record in Peruvian Amazon atapproximately 9.5–9.0 MyBP. 3) Oldest record of Cuvieronius inNorth America, at 4.9 MyBP. 4) Isthmus of Panama formation at3.1 to 2.8 MyBP. 5) Total Andes uplift at 2.7 MyBP. 6) GreatAmerican Biotic Interchange at approximately 2.8 MyBP. 7) EarlyPleistocene gomphothere record in Argentina, at 2.5 MyBP. 8)Oldest record of C. hyodon in South America, middle/late Pleis-tocene from Tarija. 9) Pebas system formation, from 10 to 7MyBP

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press). This genus was previously misinterpreted to occuralso in South America, and two species were considered, S.waringi and S. platensis (Alberdi and Prado 1995; Alberdiet al. 2002). However, Mothé et al. (in press) consideredthese taxa as the same species and synonymyzed both undera new taxonomic combination, Notiomastodon platensis.Furthermore, Stegomastodon has four loph(id)s on m2/M2and five to six loph(id)s on m3/M3, while N. platensis hasonly three loph(id)s on m2/M2 and four to five on m3/M3(never six complete loph(id)s).

The South American Notiomastodon platensis and thePanamerican Cuvieronius hyodon form the monophyleticclade 4, which is diagnosed by upper tusks dorsally curvedin lateral view (character 7, state 2). Notiomastodon platensishas tusks in a variety of forms (Mothé et al. in press), but itcould be dorsally curved at a first stage, as does C. hyodon. Inthis way, clade 4 is supported by only one synapomorphy, andwe believe that Cuvieronius also needs taxonomic review, inagreement with Montellano-Ballesteros (2002).

The divergence of these clades probably occurred prior tothe early-middle Miocene (late Hemingfordian to early Bar-stovian) when the proboscideans arrived in North Americanfrom Asia (Vaughan et al. 2000). Therefore, the clade includ-ing Notiomastodon (the only Pleistocene genus endemic toSouth America) and Cuvieronius (North, Central, and SouthAmerican) should have originated in Central America. Herewe agree with Madden (1984), Ferretti (2008a, 2010), andLucas and Alvarado (2010), who supported the monophyly ofSouth American gomphotheres. The resulting topology sug-gests that the South American gomphotheres had a commonbiogeographical history.

In South America, the earliest well dated record ofGomphotheriidae, except for the A. peruvium record, isa fragmentary vertebra from the early Pleistocene ofArgentina (Uquian; López et al. 2001; Reguero et al.2007), while all other records are middle to late Pleis-tocene (Prado et al. 2005). The oldest record of C.hyodon in South America is from the early Pleistoceneof Tarija (Ensenadan; Prado et al. 2005). However, theage of the Tarija deposits is controversial (middle to latePleistocene; MacFadden et al. 1983; Coltorti et al.2007), and it might not represent the oldest C. hyodonrecord in South America (Ferretti 2008a). In CentralAmerica, the genus Notiomastodon is not recorded andCuvieronius is known from the early Irvingtonian (ElSalvador), although its arrival in the late Blancan is suggested(Montellano-Ballesteros 2002; Lucas and Alvarado 2010). InNorth America, Cuvieronius is recorded for the late Blancan inUnited States and Mexico (Lucas et al. 1999).

In this way, five hypotheses are proposed to explain theorigin and biogeographical history of South American gom-photheres. Three of them include Amahuacatherium peru-vium as a valid taxon; however, it was not included on our

systematic analysis because we did not analyze theseremains personally, and it was not included in the matriceswe revised here (see Materials and Methods section). Thequestion about the validity of A. peruvium is still open andneeds a systematic character review (presence of lower tuskand characters related to molar morphology), but we agreewith Campbell et al. (2000, 2009, 2010) in respect to the ageof this record, considered as the oldest gomphothere inSouth America.

The first premise is the “classical” hypothesis for thebiogeographical history of the South American gompho-theres (Fig. 4a), widespread in the literature (Alberdi andPrado 1995; Alberdi et al. 2002, 2004, 2007; Prado et al.2005; Prado and Alberdi 2008). In this case, both C. hyodonand N. platensis arrived in South America during the GreatAmerican Biotic Interchange, after the formation of theIsthmus of Panama (3.1 to 2.8 MyBP), and spread throughthe Andean and lowlands “corridors” in the Pleistocene.However, there are several issues that this does not explain:(1) the presence of A. peruvium in the late Miocene of Peru,(2) when and where the common ancestor of C. hyodon andN. platensis diverged (which must have occurred in Centralor North America before 4.9MyBP, the oldest record ofCuvieronius in North America), (3) how N. platensisreached the lowlands from both sides of the Andes aftertheir uplift (2.7 MyBP), and (4) why there is no record of N.platensis in Central and/or North America.

In the second hypothesis (Fig. 4b), we considered thetaxonomic revision made by Alberdi et al. (2004) for Perugomphotheres, in which A. peruvium was synonymized withStegomastodon and, later, it was synonymized with Notio-mastodon platensis by Mothé et al. (in press). Thus, thishypothesis suggests the existence of a Panamerican ancestorto the clade (Cuvieronius hyodon and Notiomastodon pla-tensis) at 10.71 to 9.36 MyBP, when South and CentralAmericas could be connected through a cluster of islands(Kameo and Sato 2000). After this period, when Central andSouth America became isolated, this ancestor could haveevolved into N. platensis in South America and C. hyodonin Central/North America. Between 9.36 and 3.1–2.8 MyBP,South America could be isolated (Kameo and Sato 2000),and N. platensis could reach the eastern lowlands before theColombian Andes became a biogeographical barrier (lessthan 2,000 m at 4 MyBP, Gregory-Wodzicki 2000) and toreach the South American western lowlands, at least at theearly Pleistocene (the second oldest gomphothere record inSouth America, 2.5 MyBP, from Argentina). In turn, C.hyodon was not present in South America until after theconnection with Central America and the uplift of theColombian Andes (2.8 and 2.7 MyBP, respectively; Coatesand Obando 1996; Gregory-Wodzicki 2000), spreadingthrough an Andean or highland “corridor” at the middle/latePleistocene (Fig. 4b).

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The third, fourth, and fifth hypotheses consider Amahua-catherium peruvium as a valid South American taxon andthose are based on all possible phylogenetic relationshipsbetween A. peruvium, C. hyodon, and N. platensis.

The third hypothesis suggests the clade (Cuvieroniushyodon (Amahuacatherium peruvium and Notiomastodonplatensis)), which had a common pan-American ancestorat 10.71 to 9.36 MyBP (Fig. 4c). When Central and SouthAmerica became isolated, this ancestor could originate C.hyodon in Central/North America and the South Americanancestor to the clade (Amahuacatherium peruvium andNotiomastodon platensis). This divergence event shouldoccur approximately at 9.5 MyBP (considering the ageof A. peruvium between 9.5 and 9.0 MyBP, Campbell etal. 2010) and this divergence might be related to theformation of the Pebas system and the Andes uplift(Hoorn et al. 2010). The Miocene gomphothere A.peruvium could be isolated in the southern region ofthe Pebas system, while N. platensis might perhaps beisolated in its northern and western regions, spreadingto western lowlands before the Andes uplift was at itshighest (until 2.7 MyBP) and to eastern lowlands afterthe establishment of the Amazon River (approximately7 MyBP; Hoorn et al. 2010). However, this hypothesisdoes not explain when A. peruvium went extinct and ifit dispersed through the South American eastern low-lands. If this was possible, the gomphothere vertebra remainsfrom the early Pleistocene of Argentina could be not identifiedat the generic level, because it could be a specimen of A.peruvium or N. platensis.

The fourth possibility suggests the clade (Amahuacatheriumperuvium (Notiomastodon platensis and Cuvieronius hyodon)),which had a common pan-American ancestor at 10.71 to 9.36MyBP (Fig. 4d). When Central and South America becameisolated, this ancestor could evolve into A. peruvium in SouthAmerica and the Central/North American ancestor to the clade(Notiomastodon platensis and Cuvieronius hyodon). Anotherspeciation event in Central or North America could explain theoccurrence of N. platensis and C. hyodon, before 4.9 MyBPand, later (after 2.8 MyBP), these taxa reached South Americaduring the GABI. This hypothesis does not explain how N.platensis crossed the Andes to reach the South Americaneastern lowlands in the Pleistocene and the absence of the N.platensis record in Central and/or North America. Also, it doesnot explain when A. peruvium went extinct and its dispersalthrough the South American eastern lowlands, raising the samegenus identification problem for the gomphothere vertebraremains found in the lower Pleistocene of Argentina.

The fifth possibility (Fig. 4e) suggests the clade (Notio-mastodon platensis (Amahuacatherium peruvium andCuvieronius hyodon)). However, to explain this systematicarrangement, it is necessary to assume several ad hoc hy-potheses that are not supported: (1) the existence of a

previous 10.71 to 9.36 MyBP land connection betweenSouth and Central America, (2) fast dispersal of gompho-theres throughout the Americas, and (3) two sympatricspecies of gomphotheres living in South America (least-ways in Colombia and western Amazonian regions ofBrazil) in the middle Miocene (when the speciationprocess could have happened) and the record of N.platensis since the middle Miocene (Fig. 4e). The lackof a land connection between Central and South Americafrom 15.83 to 10.71 MyBP (Kameo and Sato 2000) and thefact that the oldest record of gomphotheres in North Americais from 13.6 MyBP (Lambert 1996) argues against this idea.

We suggest the second and third hypothesis as themost parsimonious of all hypotheses presented here.Both depend on the validity of A. peruvium. No matterwhat, it suggests the need for a taxonomic revision ofthe South American gomphotheres, mainly by the inclu-sion of A. peruvium. However, all these hypotheses failto explain the long temporal gap between the late Mio-cene and late Pliocene gomphothere records in SouthAmerica. In Amazonia itself, this temporal gap extendsthrough the late Pleistocene (Cozzuol 2006). Thus, along part of the proboscidean history in South Americathat should had occurred in the northern part of thecontinent (nearby Colombian, Venezuelan, and Brazilianareas) is virtually unknown.

Conclusions

In agreement with several previous studies, our phylogenyresults in a paraphyletic Gomphotheriidae as a whole. Con-versely, the gomphotheres present in South Americanduring the Quaternary are grouped in the monophyleticclade (Notiomastodon platensis and Cuvieronius hyo-don). This clade is characterized by the presence ofdorsally curved upper tusks in lateral view, in agreementwith Madden (1984), Ferretti (2008a, 2010), and Lucasand Alvarado (2010). The genus Stegomastodon appearsas the basal member of a clade characterized by thepresence of m2 with four lophids and M2 with fourlophs or more. Biogeographically, several alternativehypotheses were suggested to explain the presence ofgomphotheres in South America. However, the mostparsimonious hypotheses depends on a diversificationof a South or pan-American ancestor in the Amazonianregion during the late Miocene. In this way, a thoroughtaxonomic analysis of Amahuacatherium peruvium andalso the quest for new proboscidean remains from late Mio-cene/Pliocene deposits in South America are crucial to fill thetemporal gap in the biogeography history of the Gomphother-iidae in the Americas.

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Acknowledgments The authors are grateful to C. Cartelle (PontifíciaUniversidade Católica de Minas Gerais, Brazil), R. Machado (Museude Ciências da Terra/Departamento Nacional de Produção Mineral,Brazil), A. M. Ribeiro (Fundação Zoobotânica do Rio Grande doSul, Brazil), J. Pereira (Museu Coronel Tancredo Fernandes de Mello,Brazil), N. Guidon and R. Casati (Fundação Museu do Homem Amer-icano, Brazil), A. Rojas (Faculdad de Ciencias, Universidad de LaRepublica, Uruguay), J. L. Román-Carrión (Escuela PolitecnicaNacional, Ecuador), J. E. A. Mosquera (Museo Geológico Nacional JoséRoyo y Gómez, Instituto Colombiano de Geología yMinería, Colombia),M. Reguero (Museo de La Plata, Argentina), A. Kramarz (MuseoArgentino de Ciencias Naturales, Argentina), P. Tassy (MuséumNational d’Histoire Naturelle, France), B. Macfadden and R. Hulbert(Florida Museum of Natural History, USA), and J. Galkin (AmericanMuseum of Natural History, USA) for allowing the access to the gom-phothere collections that supported this study. Conselho Nacional deDesenvolvimento Científico e Tecnológico (CNPq) granted master schol-arship fund to DM (process number 134905/2010-5).

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