J Mammal Evol DOI 10.1007/s10914-012-9192-3

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- peruvium, seems to be a crucial part of the biogeography photheriidae is very complex and controversial. Three species and evolution of the South American gomphotheres. are currently recognized: Amahuacatherium peruvium, Cuvieronius hyodon,andNotiomastodon platensis.Thefor- Keywords South American Gomphotheres . Systematic mer is a late Miocene gomphothere whose validity has been review. Taxonomy. Proboscidea questioned by several authors. The other two, C. hyodon and N. platensis, are Quaternary taxa in South America, and they have distinct biogeographic patterns: Andean and lowland Introduction distributions, respectively. South American gomphotheres be- came extinct at the end of the Pleistocene. We conducted a The family Gomphotheriidae is, so far, the only group of phylogenetic analysis of Proboscidea including the South Proboscidea recorded in South America. Together with the American Quaternary gomphotheres, which resulted in two megatheriid sloths Eremotherium laurillardi Lund, 1842, most parsimonious trees. Our results support a paraphyletic the Megatherium americanum Cuvier, 1796,andthe Gomphotheriidae and a monophyletic South American notoungulate Toxodon platensis Owen, 1840, they are the gomphothere lineage: C. hyodon and N. platensis. The late most common late Pleistocene representatives of the mega- Miocene gomphothere record in Peru, Amahuacatherium fauna in South America (Paula-Couto 1979). Similar to the Pleistocene and Holocene members of the family Elephan- tidae (e.g., extant elephants and extinct mammoths), the D. Mothé (*) South American gomphotheres are characterized by having Programa de Pós-graduação em Ciências Biológicas (Zoologia), a brachycephalic and brevirostrine skull, a short and curved Museu Nacional/UFRJ, mandibular symphysis, and specialized dentition, which Quinta da Boa Vista, 20940-040, Rio de Janeiro, RJ, Brazil consists of a pair of upper tusks (second incisors) and six e-mail: [email protected] pairs of upper and lower molars (Simpson and Paula-Couto 1957; Paula-Couto 1979; Prado et al. 2001; Ferretti 2008a). L. S. Avilla Departamento de Zoologia, Instituto de Biociências, Laboratório de Mastozoologia, Universidade Federal do Estado do Rio de Janeiro, Taxonomy and Diversity of South American Avenida Pasteur, 458, Urca, 22290-240, Gomphotheres Rio de Janeiro, RJ, Brazil e-mail: [email protected] The taxonomic history of the South American gompho- M. A. Cozzuol theres is long and complex. Most authors consider that they Departamento de Zoologia, Instituto de Ciências Biológicas, were represented by three genera: Cuvieronius Osborn, Universidade Federal de Minas Gerais, 1923, Haplomastodon Hoffstetter, 1950,andStegomastodon Avenida Antônio Carlos, 6627, Pampulha, 31270-910, Belo Horizonte, Minas Gerais, Brazil Pohlig, 1912 (Simpson and Paula-Couto 1957;Ficcarellietal. e-mail: [email protected] 1995;Ferretti2008a, 2010). Later, some authors (Alberdi and J Mammal Evol

Prado 1995; Alberdi et al. 2002, 2004, 2007; Prado et al. proposed a new genus and species, Notiomastodon ornatus, 2005; Prado and Alberdi 2008) synonymized Haplomastodon based on a short, massive tusk and a dentary from Playa del with Stegomastodon, reducing the diversity of genera, but Barco, Argentina. Hoffstetter (1950) proposed Haplomasto- keeping three species: Cuvieronius hyodon (Fischer, 1814), don as a subgenus of Stegomastodon and, in 1952, elevated Stegomastodon platensis (Ameghino, 1888), and S. waringi Haplomastodon to full generic status, based on the absence (Holland, 1920). Very recently, Mothé et al. (in press) of transverse foramina in the atlas (1st cervical vertebra). He proposed to include the last two species in a single species, also included all Brazilian gomphotheres in a new species under the name Notiomastodon platensis, as first suggested by Stegomastodon brasiliensis Hoffstetter, 1952.Thetrans- Madden (1984). verse foramen of the axis was recognized as a variable The first report of gomphothere remains from South character by Simpson and Paula-Couto (1957), and they America was made by Cuvier (1806),whoanalyzedan placed all Brazilian gomphotheres in Haplomastodon war- isolated left M2 from Imbabura, northern Ecuador, and ingi (Holland, 1920). Ficcarelli et al. (1995), based on nameditasthe“Mastodonte des Cordilliéres.” In 1824, diagnostic gomphothere remains from northern Ecuador, Cuvier established the formal names Mastodon andium for synonymized all Haplomastodon species with H. chimbor- the Imbabura (Ecuador) gomphotheres and M. humboldtii azi (Proaño, 1922). Alberdi and Prado (1995) included the for a molar from Concepción (Chile). Before this study, species S. superbus (Ameghino, 1888), and N. ornatus in S. Fischer (1814) analyzed the same specimen from Imbabura, platensis. The genus Haplomastodon was later synony- and named it as Mastotherium hyodon, which has priority mized with the genus Stegomastodon, generating the new over Mastodon andium (see Cabrera 1929). The genus combination S. waringi (Alberdi et al. 2002). Lucas and Cuvieronius was erected by Osborn (1923)andlater, Alvarado (2010) used the combinations Notiomastodon pla- Cabrera (1929), in a revision of the Argentine gompho- tensis, in replacement of S. platensis, which was previously theres, synonymized Mastodon argentinus Ameghino, 1888, suggested by Madden (1984) and Ferretti (2008a). Ferretti under the name Cuvieronius hyodon (Fischer, 1814). (2010) used the combination Haplomastodon chimborazi Ficcarelli et al. (1995), in a taxonomic revision of Cuvier- and employed quote marks for “Stegomastodon” platensis, onius, validated C. tarijensis (Ameghino, 1902), and pro- arguing that the South and North American species attribut- posed the material referred to C. tarijensis from Tarija, ed to this genus are not congeneric with S. mirificus (Leidy, Bolivia, as the topotype for the species. Recently, Lambert 1859), the type species of the genus, from North America. and Shoshani (1998) considered C. hyodon as the type Mothé et al. (in press) reviewed the Pleistocene South species of Cuvieronius, but Lucas (2009) argued that the American lowland gomphotheres and concluded that they genus is monospecific, considering C. tropicus Cope, 1884, belong to a single species for which the valid name is Notio- from Mexico, as a junior synonym of C. hyodon. Lucas mastodon platensis. Consequently, only two gomphothere (2009), in order to solve the taxonomic problem of the name species were present in the Quaternary of South America: Mastotherium hyodon, suggested to keep the name Cuvier- the Andean Cuvieronius hyodon, and the lowland Notiomas- onius and consider M. hyodon as its type species, by desig- todon platensis (Fig. 1). nating a neotype to M. hyodon (the skull and lower jaw from The holotype of Notiomastodon ornatus (Museo Argen- Tarija, Bolivia originally described and illustrated by Boule tino de Ciencias Naturales “Bernardino Rivadavia,” collec- and Thevenin (1920)). tion number MACN 2157) is described by Cabrera (1929), The diagnostic material of C. hyodon comes from Tarija, and it is a mandible with a short symphysis, without lower Bolivia, where several skulls and postcranial remains were incisors, bunolophodont molars with several accessory con- found (Marshall and Sempere 1991; Coltorti et al. 2007). ules (double trefoil wear pattern), and short, massive and Cuvieronius hyodon is a short-jawed gomphothere charac- upper curved tusk with lateral enamel band (Cabrera 1929: terized by having a depressed and elongated cranium, a pair Figs. 2-4). Furthermore, Stegomastodon platensis is de- of twisted upper tusks, which have a spiraled enamel band scribed as having a variable wear pattern on the molars, along their entire length, and lower deciduous incisors in more complex than Haplomastodon chimborazi,and some juveniles (Prado et al. 2005; Ferretti 2008a, b). straight to slightly upper curved tusks, without enamel band The first one to review the taxonomy of South American (Prado et al. 2005). Both genera show a similar tusk mor- lowland gomphotheres was Florentino Ameghino (1888, photype and should represent the same taxon, in which 1889, 1891), who defined four species that he placed in Notiomastodon has priority and Stegomastodon is not ap- the genus Mastodon. After that, the Argentinean fossils were plicable to the South American species (Mothé et al. in again reviewed by Cabrera (1929), who synonymized some press). A brachycephalic skull with a high parieto-occipital species described by Ameghino (1889) and transferred them region, a pair of straight or curved upper tusks with absence to the North American genus Stegomastodon, recognizing of spiraled torsion, complex molar teeth with double-trefoil only two species: S. platensis and S. superbus. He also and simple-trefoil wear patterns (Mothé et al. in press) J Mammal Evol

presence of pre-Quaternary gomphotheres in South America remains 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 South America is that they became extinct by the end of the Pleistocene (Ficcarelli et al. 1997; Prado et al. 2001; Alberdi et 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 South America during the Great American Biotic Interchange (GABI), after the establishment of the Panamanian Isthmus – Fig. 1 Main differences between the South American Quaternary at 3.1 2.8 MyBP (Coates and Obando 1996), a land-bridge gomphotheres. a anterior view of a Notiomastodon platensis high that connects North and South America through Central Amer- cranium (reconstructed, based on Cabrera 1929) with straight upper ica (Cione and Tonni 2001;Coltortietal.2007; Woodburne tusks from Arrecifes, Buenos Aires province, Argentina (MLP 8-1, 2010). However, the record of the Amahuacatherium peruvium Museo de La Plata paleontological collection). b anterior view of a Cuvieronius hyodon low cranium with twisted upper tusks from Tarija, from the late Miocene Amazonian lowlands of Peru (Campbell Bolivia (MACN Pv 1291, Museo Argentino de Ciencias Naturales et al. 2000, 2006, 2009) would indicate, if its morphological “Bernardino Rivadavia” paleontological collection). c lateral view of features are accurately interpreted and its age is correct, that the same specimen described in a. d lateral view of the same specimen proboscideans were present in South America prior to the main described in b stream of the GABI. Besides Amahuacatherium, other species also have an early “arrival” into South America, such as characterize the species N. platensis. Cabrera (1929) indi- procyonid carnivorans and sigmodontine rodents (Woodburne cates that Cuvieronius hyodon have a low and long skull, 2010). Furthermore, ground sloths and terror birds reached large upper tusks with twisted enamel band, lack of lower North America at the same time (Woodburne 2010 and tusks in adults, and short dentary symphysis. Otherwise, the references cited there). Consequently, the beginning of genus Stegomastodon is represented in North America by the GABI could have started approximately ten million three species: S. primitivus, S. mirificus,andS. aftoniae years ago, with a brief period of global sea level drop that (Lucas et al. 2011). The genus is characterized by a skull allowed the emergence of a small land connection between with a tall frontal and parietal region, long and relatively Central and South America. Between 10.71 and 9.36 MybP, straight tusks that lack enamel, no lower tusks, the mandib- calcareous nannofossils indicate a separation between the ular symphysis is relatively short and tall, and the m3 has Caribbean and the east Pacific during this time, compared five lophids and double trefoils. It differs from Notiomasto- with the early and middle Miocene. This was followed by don in some structures of the scapula, humerus, pelvis, and a reinstatement of a deeper connection between 8.35 and femur, and it seems to have a greater degree of graviportality 3.65 MybP between the Caribbean Sea and the eastern equa- than South America gomphotheres (Lucas et al. 2011). torial Pacific, and a final closure of the Isthmus of Panama The discovery and description of Amahuacatherium peru- by 2.76 MybP (Kameo and Sato 2000). About the same vium (Romero-Pittman, 1996), a gomphothere with vestigial geological variations are observed in the sedimentological lower incisors from the late Miocene (approximately 9.5–9.0 record by Coates et al. (2004). MyBP) of the Peruvian Amazonia, has inspired a great con- In North and Central America, the genus Cuvieronius has a troversy (Campbell et al. 2000, 2006, 2009, 2010;Alberdiet continuous distribution while the genus Stegomastodon has a al. 2004; Woodburne 2010). Some authors have stated that the discontinuous distribution in Central America (Arroyo-Cabrales holotype of A. peruvium is, actually, a specimen of Stegomas- et al. 2007). This observation has led some authors to suggest todon (Alberdi et al. 2004), its proposed age is mistaken, and that a taxonomic review of the South American species referred its primitive features (lower incisors and simpler molars with to Stegomastodon is needed (Arroyo-Cabrales et al. 2007; complexity similar to Haplomastodon) were misinterpreta- Ferretti 2008a, 2010; Lucas et al. 2011). tions caused by its fragmentary nature and taphonomomic During the Pleistocene, each of the South American processes (Alberdi et al. 2004; Woodburne 2010). Recently, gomphotheres spread throughout the continent in two dif- Campbell et al. (2009, 2010) have refuted the critics on the ferent “corridors.” In the Andean or highland “corridor,” morphological features and age of Amahuacatherium.The Cuvieronius hyodon was dominant, spreading in the present J Mammal Evol

Fig. 2 Map of the geographical distribution of South American gomphotheres during the Pleistocene. The circles represent Notiomastodon platensis and the triangles represent Cuvieronius hyodon. Modified from Simpson and Paula-Couto (1957), Alberdi et al. (2002), Cione et al. (2005), Ferretti (2008a), and Lucas (2008)

countries of Colombia, Ecuador, Bolivia, Peru, and Chile, and related to their unsolved taxonomic problems. Previous the lowland “corridor,” where Notiomastodon platensis phylogenies by Shoshani et al. (2006) include 125 char- prevailed in Brazil, Ecuador, Venezuela, Colombia, acters and 40 terminals at the generic level; however, Argentina, Uruguay, Paraguay, and the western coastal they published only a simplified cladogram at the fam- areas of Peru and Chile (Simpson and Paula-Couto ily level; Prado and Alberdi (2008) conducted a cladis- 1957; Alberdi and Prado 1995; Prado et al. 2001; tic analysis of the trilophodont gomphotheres, with Alberdi et al. 2002;Ferretti2008a, 2010; Mothé et al. in press; emphasis on the South American species. This phylog- Fig. 2). Cuvieronius hyodon seems to be adapted to live in the eny is problematic in many points, which invalidate highlands, which is supported not only by its geographic both the phylogeny itself and the biogeographic analysis distribution, but also by stable isotope analysis (Sánchez- based on it, as shown by Cozzuol et al. (in press). Chillón et al. 2004). On the other hand, the lowland gompho- Furthermore, several recent studies of the group (Arroyo- there, Notiomastodon platensis, seems to avoid drier environ- Cabrales et al. 2007; Ferretti 2008a, 2010;Lucasand ments (Winck et al. 2010). Alvarado 2010; Cozzuol et al. in press;Mothéetal.in press) show the necessity of a systematic revision of the South American gomphotheres. Phylogeny of South American Quaternary This study proposes a new systematic and biogeographic Gomphotheres view for the South American Pleistocene gomphotheres and presents inferences about the relation of these taxa within The phylogenetic relationships of South American gompho- the family Gomphotheriidae that follows the taxonomic theres are another controversial issue and it is directly review conducted in Mothé et al. (in press). J Mammal Evol

Fig. 3 Resulting consensus tree based on the matrix modified from Shoshani et al. (2006) and Cozzuol et al. (in press), including the new taxon Notiomastodon platensis. The clade 1 represents Elephantida and clade 4 represents the South America Quaternary gomphotheres

Materials and Methods Results and Discussion

A phylogenetic analysis was performed in order to elu- The phylogenetic analysis conducted here resulted in two cidate the relationships of the South American gompho- most parsimonious trees with 7.31205 fit as the best score theres. We modified the original matrix from Cozzuol and the consensus of these two trees is represented in Fig. 3. et al. (in press, modified from Shoshani et al. 2006), Accordingly, the family Gomphotheriidae (sensu Shoshani by reviewing some features and merging “Stegomastodon” et al. 2006) is paraphyletic. This is not a new argument; platensis and Haplomastodon waringi into Notiomastodon Maglio (1972), Tassy (1996), and Arroyo-Cabrales et al. platensis. We also recognized Stegomastodon only by (2007) also rejected the monophyly of the family Gompho- North American species and we recoded the character theriidae. Moreover, Shoshani and Tassy (1996) also argued states for this genus based only on these species (Arroyo- that it requires too many changes to group all taxa tradition- Cabrales et al. 2007; Ferretti 2008a, 2010; Lucas et al. ally incorporated in “gomphotheres.” To consider this taxon 2011). We are in agreement with Ferretti (2008a, 2010), a natural group, it must include the monophyletic Elephan- Lucas et al. (2011), and Mothé et al. (in press), who tidae and Stegodontidae (Fig. 3, Clade 1). This clade, named consider that Stegomastodon is not present in South Elephantida, was also recognized by Shoshani et al. (2006). America. In our results, the Elephantida includes several lineages We ran the taxon-character matrix with TNT software (Fig. 3): a basal great polytomy compromising most of the (Goloboff et al. 2008) using the “Implied weighting” set- traditional gomphotheres, the monophyletic (Notiomastodon ting, with K06, and conducted the search using defaults of platensis and Cuvieronius hyodon), and the four consecutive “xmult” command to finding optimal score 20 times inde- sister-taxa of Elephantoidea (Elephantidae plus Stegodontidae pendently, plus ten cycles of tree-drifting strategies (Goloboff by Shoshani et al. 2006), which are (Stegomastodon mirificus et al. 2008). Group supports are calculated by TBR-swapping (Tetralophodon (Anacus (Paratetralophodon)))). The Ele- the trees found, keeping note of the number of steps needed to phantida is diagnosed here by the presence of a postcingulum collapse each group. on the lower third permanent molars (character 124, state 1). J Mammal Evol

Fig. 4 Five possible systematic combinations involving Amahuacathe- biogeographic histories of gomphotheres in Americas: 1) Short rium peruvium and the gomphotheres recorded in South America, Cuvier- land connection between Central and South Americas at 10.71 onius hyodon and Notiomastodon platensis. a the suggested clade is (C. to 9.36 MyBP. 2) A. peruvium record in Peruvian Amazon at hyodon and N. platensis), with South American arrival at the Great approximately 9.5–9.0 MyBP. 3) Oldest record of Cuvieronius in America Biotic Interchange. b the suggested clade is (C. hyodon and N. North America, at 4.9 MyBP. 4) Isthmus of Panama formation at platensis)withA. peruvium synonymized with N. platensis. c the sug- 3.1 to 2.8 MyBP. 5) Total Andes uplift at 2.7 MyBP. 6) Great gested clade is (Cuvieronius hyodon (Amahuacatherium peruvium and American Biotic Interchange at approximately 2.8 MyBP. 7) Early Notiomastodon platensis). d the suggested clade is (Amahuacatherium Pleistocene gomphothere record in Argentina, at 2.5 MyBP. 8) peruvium (Notiomastodon platensis and Cuvieronius hyodon). e the sug- Oldest record of C. hyodon in South America, middle/late Pleis- gested clade is (Notiomastodon platensis (Amahuacatherium peruvium tocene from Tarija. 9) Pebas system formation, from 10 to 7 and Cuvieronius hyodon). Important moments in the evolutionary and MyBP

The development of the postcingulum in “gomphotheres” can some specimens bear vestigial (or reduced) and deciduous man- be associated with the increase in number of loph(id)s in dibular tusks (Ferretti 2008b), all members of clade 2 lack Elephantida, which are tetra, penta, or have more than five mandibular tusks and are brevirostrine. This brevirostrine condi- lophids on the third lower molars. Tassy (1996)recognizedan tion, an extreme mandible shortening, was possible probably evolutionary trend for the Proboscidea toward the augmenta- because of the horizontal teeth displacement condition evolved tion on cusps due to the subdivision of the main mammalian in the Elephatimorpha (Shoshani et al. 2006). Therefore, in the cusps and by the increase in number of loph(id)s. The incre- members of clade 2, the brevirostrine condition probably allowed ment in crown morphology in Elephantida, compared to other the reduction in the number of erupted molars, where only one Proboscidea, was probably positively selected in response to a molar or one molar plus part of the successive adjacent tooth are more abrasive and complex herbivorous diet in most of the in use at the same time on each half jaw. continents after the spread of grasslands from the early Mio- The monophyletic clade 3 is diagnosed by m2 with four cene on. distinct lophids (character 33, state 3, tetralophodont) and The monophyletic clade 2 comprises clade 3, (Stegomastodon M2 with four or more distinct lophs (character 40, state 2). primitivus (Tetralophodon (Anancus (Paratetralophodon (Ele- Thus, the tendency for increase in the number of loph(id)s is phantoidea))))), and the natural group Notiomastodon platensis also observed in clade 3, but it occurs on the second upper plus Cuvieronius hyodon (clade 4) (Fig. 3). Clade 2 is diagnosed and lower molars, which have more loph(id)s when com- by M3 with postentoconule, pentaloph or with more than five pared to the other taxa in Elephantida. The most basal taxon lophs on the molars (character 34, state 5), and a short and spout- of this clade, Stegomastodon mirificus, is represented here like mandibular symphysis (character 94, state 2). With the by the genus Stegomastodon, which is endemic to North exception of Cuvieronius hyodon and Tetralophodon,inwhich America (Ferretti 2010; Lucas et al. 2011; Mothé et al. in J Mammal Evol press). This genus was previously misinterpreted to occur systematic analysis because we did not analyze these also in South America, and two species were considered, S. remains personally, and it was not included in the matrices waringi and S. platensis (Alberdi and Prado 1995; Alberdi we revised here (see Materials and Methods section). The et al. 2002). However, Mothé et al. (in press) considered question about the validity of A. peruvium is still open and these taxa as the same species and synonymyzed both under needs a systematic character review (presence of lower tusk a new taxonomic combination, Notiomastodon platensis. and characters related to molar morphology), but we agree Furthermore, Stegomastodon has four loph(id)s on m2/M2 with Campbell et al. (2000, 2009, 2010) in respect to the age and five to six loph(id)s on m3/M3, while N. platensis has of this record, considered as the oldest gomphothere in only three loph(id)s on m2/M2 and four to five on m3/M3 South America. (never six complete loph(id)s). The first premise is the “classical” hypothesis for the The South American Notiomastodon platensis and the biogeographical history of the South American gompho- Panamerican Cuvieronius hyodon form the monophyletic theres (Fig. 4a), widespread in the literature (Alberdi and clade 4, which is diagnosed by upper tusks dorsally curved Prado 1995; Alberdi et al. 2002, 2004, 2007; Prado et al. in lateral view (character 7, state 2). Notiomastodon platensis 2005; Prado and Alberdi 2008). In this case, both C. hyodon has tusks in a variety of forms (Mothé et al. in press), but it and N. platensis arrived in South America during the Great could be dorsally curved at a first stage, as does C. hyodon.In American Biotic Interchange, after the formation of the this way, clade 4 is supported by only one synapomorphy, and Isthmus of Panama (3.1 to 2.8 MyBP), and spread through we believe that Cuvieronius also needs taxonomic review, in the Andean and lowlands “corridors” in the Pleistocene. agreement with Montellano-Ballesteros (2002). However, there are several issues that this does not explain: The divergence of these clades probably occurred prior to (1) the presence of A. peruvium in the late Miocene of Peru, the early-middle Miocene (late Hemingfordian to early Bar- (2) when and where the common ancestor of C. hyodon and stovian) when the proboscideans arrived in North American N. platensis diverged (which must have occurred in Central from Asia (Vaughan et al. 2000). Therefore, the clade includ- or North America before 4.9MyBP, the oldest record of ing Notiomastodon (the only Pleistocene genus endemic to Cuvieronius in North America), (3) how N. platensis South America) and Cuvieronius (North, Central, and South reached the lowlands from both sides of the Andes after American) should have originated in Central America. Here their uplift (2.7 MyBP), and (4) why there is no record of N. we agree with Madden (1984), Ferretti (2008a, 2010), and platensis in Central and/or North America. Lucas and Alvarado (2010), who supported the monophyly of In the second hypothesis (Fig. 4b), we considered the South American gomphotheres. The resulting topology sug- taxonomic revision made by Alberdi et al. (2004) for Peru gests that the South American gomphotheres had a common gomphotheres, in which A. peruvium was synonymized with biogeographical history. Stegomastodon and, later, it was synonymized with Notio- In South America, the earliest well dated record of mastodon platensis by Mothé et al. (in press). Thus, this Gomphotheriidae, except for the A. peruvium record, is hypothesis suggests the existence of a Panamerican ancestor a fragmentary vertebra from the early Pleistocene of to the clade (Cuvieronius hyodon and Notiomastodon pla- Argentina (Uquian; López et al. 2001; Reguero et al. tensis) at 10.71 to 9.36 MyBP, when South and Central 2007), while all other records are middle to late Pleis- Americas could be connected through a cluster of islands tocene (Prado et al. 2005). The oldest record of C. (Kameo and Sato 2000). After this period, when Central and hyodon in South America is from the early Pleistocene South America became isolated, this ancestor could have of Tarija (Ensenadan; Prado et al. 2005). However, the evolved into N. platensis in South America and C. hyodon age of the Tarija deposits is controversial (middle to late in Central/North America. Between 9.36 and 3.1–2.8 MyBP, Pleistocene; MacFadden et al. 1983;Coltortietal. South America could be isolated (Kameo and Sato 2000), 2007), and it might not represent the oldest C. hyodon and N. platensis could reach the eastern lowlands before the record in South America (Ferretti 2008a). In Central Colombian Andes became a biogeographical barrier (less America, the genus Notiomastodon is not recorded and than 2,000 m at 4 MyBP, Gregory-Wodzicki 2000) and to Cuvieronius is known from the early Irvingtonian (El reach the South American western lowlands, at least at the Salvador), although its arrival in the late Blancan is suggested early Pleistocene (the second oldest gomphothere record in (Montellano-Ballesteros 2002; Lucas and Alvarado 2010). In South America, 2.5 MyBP, from Argentina). In turn, C. North America, Cuvieronius is recorded for the late Blancan in hyodon was not present in South America until after the United States and Mexico (Lucas et al. 1999). connection with Central America and the uplift of the In this way, five hypotheses are proposed to explain the Colombian Andes (2.8 and 2.7 MyBP, respectively; Coates origin and biogeographical history of South American gom- and Obando 1996; Gregory-Wodzicki 2000), spreading photheres. Three of them include Amahuacatherium peru- through an Andean or highland “corridor” at the middle/late vium as a valid taxon; however, it was not included on our Pleistocene (Fig. 4b). J Mammal Evol

The third, fourth, and fifth hypotheses consider Amahua- previous 10.71 to 9.36 MyBP land connection between catherium peruvium as a valid South American taxon and South and Central America, (2) fast dispersal of gompho- those are based on all possible phylogenetic relationships theres throughout the Americas, and (3) two sympatric between A. peruvium, C. hyodon, and N. platensis. species of gomphotheres living in South America (least- The third hypothesis suggests the clade (Cuvieronius ways in Colombia and western Amazonian regions of hyodon (Amahuacatherium peruvium and Notiomastodon Brazil) in the middle Miocene (when the speciation platensis)), which had a common pan-American ancestor process could have happened) and the record of N. at 10.71 to 9.36 MyBP (Fig. 4c). When Central and South platensis since the middle Miocene (Fig. 4e). The lack America became isolated, this ancestor could originate C. of a land connection between Central and South America hyodon in Central/North America and the South American from 15.83 to 10.71 MyBP (Kameo and Sato 2000) and the ancestor to the clade (Amahuacatherium peruvium and fact that the oldest record of gomphotheres in North America Notiomastodon platensis). This divergence event should is from 13.6 MyBP (Lambert 1996) argues against this idea. occur approximately at 9.5 MyBP (considering the age We suggest the second and third hypothesis as the of A. peruvium between 9.5 and 9.0 MyBP, Campbell et most parsimonious of all hypotheses presented here. al. 2010) and this divergence might be related to the Both depend on the validity of A. peruvium. No matter formation of the Pebas system and the Andes uplift what, it suggests the need for a taxonomic revision of (Hoorn et al. 2010). The Miocene gomphothere A. the South American gomphotheres, mainly by the inclu- peruvium could be isolated in the southern region of sion of A. peruvium. However, all these hypotheses fail the Pebas system, while N. platensis might perhaps be to explain the long temporal gap between the late Mio- isolated in its northern and western regions, spreading cene and late Pliocene gomphothere records in South to western lowlands before the Andes uplift was at its America. In Amazonia itself, this temporal gap extends highest (until 2.7 MyBP) and to eastern lowlands after through the late Pleistocene (Cozzuol 2006). Thus, a the establishment of the Amazon River (approximately long part of the proboscidean history in South America 7 MyBP; Hoorn et al. 2010). However, this hypothesis that should had occurred in the northern part of the does not explain when A. peruvium went extinct and if continent (nearby Colombian, Venezuelan, and Brazilian it dispersed through the South American eastern low- areas) is virtually unknown. lands. If this was possible, the gomphothere vertebra remains from the early Pleistocene of Argentina could be not identified at the generic level, because it could be a specimen of A. peruvium or N. platensis. Conclusions The fourth possibility suggests the clade (Amahuacatherium peruvium (Notiomastodon platensis and Cuvieronius hyodon)), In agreement with several previous studies, our phylogeny which had a common pan-American ancestor at 10.71 to 9.36 results in a paraphyletic Gomphotheriidae as a whole. Con- MyBP (Fig. 4d). When Central and South America became versely, the gomphotheres present in South American isolated, this ancestor could evolve into A. peruvium in South during the Quaternary are grouped in the monophyletic America and the Central/North American ancestor to the clade clade (Notiomastodon platensis and Cuvieronius hyo- (Notiomastodon platensis and Cuvieronius hyodon). Another don). This clade is characterized by the presence of speciation event in Central or North America could explain the dorsally curved upper tusks in lateral view, in agreement occurrence of N. platensis and C. hyodon,before4.9MyBP with Madden (1984), Ferretti (2008a, 2010), and Lucas and, later (after 2.8 MyBP), these taxa reached South America and Alvarado (2010). The genus Stegomastodon appears during the GABI. This hypothesis does not explain how N. as the basal member of a clade characterized by the platensis crossed the Andes to reach the South American presence of m2 with four lophids and M2 with four eastern lowlands in the Pleistocene and the absence of the N. lophs or more. Biogeographically, several alternative platensis record in Central and/or North America. Also, it does hypotheses were suggested to explain the presence of not explain when A. peruvium went extinct and its dispersal gomphotheres in South America. However, the most through the South American eastern lowlands, raising the same parsimonious hypotheses depends on a diversification genus identification problem for the gomphothere vertebra of a South or pan-American ancestor in the Amazonian remains found in the lower Pleistocene of Argentina. region during the late Miocene. In this way, a thorough The fifth possibility (Fig. 4e) suggests the clade (Notio- taxonomic analysis of Amahuacatherium peruvium and mastodon platensis (Amahuacatherium peruvium and also the quest for new proboscidean remains from late Mio- Cuvieronius hyodon)). However, to explain this systematic cene/Pliocene deposits in South America are crucial to fill the arrangement, it is necessary to assume several ad hoc hy- temporal gap in the biogeography history of the Gomphother- potheses that are not supported: (1) the existence of a iidae in the Americas. J Mammal Evol

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