AMQ32(1) 43-56 Alberdi Prado.pub REVISITING THE EVOLUTIONARY HISTORY AND PALEOBIOGEOGRAPHY OF FOSSIL HORSES FROM SOUTH AMERICA María Teresa Alberdi 1, José Luis Prado 2 1 Departamento de Paleobiología, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain. 2 INCUAPA, CONICET-UNICEN. Universidad Nacional del Centro de la Provincia de Buenos Aires, Olavarria, Argentina. Corresponding author: M.T. Alberdi ABSTRACT: Horses are a conspicuous group of immigrant mammals from North America that arrived in South America during the late Pliocene and no survived the megafaunal extinction, approximately ten thousand years ago. Two main equids lineages are found in South America. The first lineage is the species assigned to Equus, which appears during the middle Pleistocene and shows horse-like anatomical features. The second lineage is the genus Hippidion, which were horses with very distinctive anatom- ical features are recorded for the first time during the late Pliocene. The predominance of the dispersal events over vicariant ones is consistent with the migratory habits of horses. The global biogeographic distributions of horses explain the mode of dispersal and their migration from North America to another continent. The dispersal and the diversification process in small to middle size species (Equus andium, Equus insulatus, Hippidion devillei, and Hippidion saldiasi) occurred through the Andes corridor; whereas the large species (Equus neogeus and Hippidion principale) mainly traveled using the eastern plain route. The pathway of disper- sion in each species reflects its adaptive change and habitat preference. The present study aims to provide a synthesis of already published data on the phylogeny, systematics, palaeobiogeography and palaeoecology of both the lineages recorded in South America, updating some taxonomic data. Keywords: Equidae, macroevolution, South America, Quaternary. Available online http://amq.aiqua.it ISSN (print): 2279-7327, ISSN (online): 2279-7335 Alpine and Mediterranean Quaternary, 32 (1), 2019, 43 - 56 1. INTRODUCTION The fossil record of horses is one of the best known and provides an exceptional example of large- scale morphological change (Simpson, 1951). The radi- ation of equids during the Neogene in North America has been cited as a textbook example of adaptive radia- tion for more than a century (Marsh, 1874), as it is cru- cial in the development of evolutionary theory, linking trait evolution and adaptive success (Simpson, 1953; MacFadden, 1992; Cantalapiedra et al., 2017). In this study, we present an update on the information of fossil horses in South America, providing a synthesis of al- ready published data on the evolutionary history, phy- logeny, systematics, palaeobiogeography, and palaeoe- cology of two key equid lineages (Hippidion and Equus) recorded in South America. In his first voyage to South America (1832), Darwin made a series of observations on the extinct fauna that were key in many of his later conclusions. During Octo- ber 1833, Darwin found a horse tooth in the red argilla- ceous earth in the Pampas, at “Bajada de Santa Fé”, in the province of Entre Rios, Argentina. Later, the paleon- tologist Richard Owen (1840: 109) confirmed the tooth was from an extinct species and remarked "This evi- dence of the former existence of a genus, which, as regards South America, had become extinct, and has a second time been introduced into that Continent". Since this publication, notes and articles proliferated which in most cases do not reflect the general diversity of this group. Recent papers on the Equidae from South Ameri- ca recognize two genera: Equus and Hippidion (Prado & Alberdi, 2008, 2012, 2016, 2017). The dental morpholo- gy of Hippidion (oval protocone, rounded protoconid, and hypoconid, reduced metaconid-metastylid double knot) is more primitive than Equus, and its body struc- ture is more robust (Prado, 1984; Alberdi, 1987; Alberdi et al., 1986, 1987; Cerdeño et al., 2008; Prado & Alber- di, 1994, 2014, 2016; among others). The genus Equus originated in North America dur- ing the Pliocene and subsequent dispersal to Eurasia, Africa and South America (MacFadden, 1992). In 1950, the French paleontologist Robert Hoffstetter created the subgenus Amerhippus to include all species of genus Equus from South America. The author justifies this subgenus by a single character: the absence of infundib- ulum along the surface of the lower incisors and, there- fore, the loss of enamel on the chewing surface. In a https://doi.org/10.26382/AMQ.2019.04 44 Alberdi M.T. & Prado J.L. 45 Fossil horses from South America later work on the revision of mammals of Ecuador Hoff- stetter (1952) indicated that the ulna is stronger in the South American horses than other Equus. In the litera- ture, the recognition of the subgenus Amerhippus is controversial. Recently Prado & Alberdi (2017) ques- tioned the use of subgenus Amerhippus. Orlando et al. (2008) conducted DNA-based phylogenetic analyses revealing that all Pleistocene South American species of Equus were members of the caballine horse lineage, not a distinct subgenus as first suggested by Hoffstetter (1950). Therefore, the validity of the subgenus Amerhip- pus is questionable, and is not employed herein. The dispersal of the horse Equus into South America repre- sents an important event (MacFadden, 2013). There is some controversy about the timing of this dispersion. Several studies have asserted that the age of this dis- persal event is late Pleistocene, 0.125 Ma (Lujanian South American Land Mammals Age, SALMA), during a late phase of the Great American Biotic Interchange, GABI 4 (Cione & Tonni, 1999; Coltorti et al., 2010; Woodburne, 2010). However, Tonni et al. (2009) point out that in comparison with the Pampean standard, the Tarija fauna is not exclusively Ensenadan or Lujanian SALMA, given that, although the bulk of the fauna is comparable to that of the Pampean Lujanian, there are some exclusive taxa of the Pampean Ensenadan. New biostratigraphic evidence documents that Equus occurs from 15 superposed faunal horizons or zones through- out the Tolomosa Formation at Tarija, Bolivia. This bio- stratigraphic sequence is independently calibrated to occur between 1.07 to <0.76 Ma (Ensenadan SALMA) and coincident with GABI 3 (MacFadden, 2013). Many articles have been published of the Equus species in South America (Fig. 1). Prado & Alberdi (2017) reviewed this group and recognized three valid species: Equus andium Branco 1883, ex Wagner (1860), Equus insulatus Ameghino, 1904, and Equus neogeus Lund, 1840 (Fig.s 2 and 3). Recently, Machado et al. (2017) proposed reducing the number of Equus species in South America to one, Equus neogeus. We do not share this proposal. This proposal may be due, in our opinion, to the fact that species from North and South America are mixed in the analysis, possibly by the alleged affinity of Equus occidentalis with South American forms. The infundibulum in its lower incisors is shared by South American species, for which Hoffstetter (1950, 1952) proposes the new subgenus Amerhippus, in which he also included the Rancho La Brea equid, Equus occidentalis. The latter species, however, diverg- es from the other South American species in various characteristics. Beside the cornets in the lower incisors, South American equids, according to Hofstetter, are characterized by a ventral rotation of the occiput, with a strong deflection of the braincase relative to the face, a broad supraoccipital crest, the vomer joining the palatal processes of the maxillaries well in front of the palatines, and a massive jaw and short limbs. It is true that not all elements of the appendicular skeleton of South Ameri- can horses are equally diagnostic. For example, when the first phalanges of the third finger are mixed (anterior and posterior), the limits overlap. In the case of meta- podes, the metacarpal is more diagnostic than the meta- tarsals. This is partly because the former limbs are where the weight of the body and the head are most affected (Eisenmann, 1984). Limb morphometric studies have been useful for discriminating Hipparion and mono- dactyl horse species (Eisenmann, 1979). This approach offers a comprehensive view of the material studied. However, in some cases, there are some overlaps, as in the case of the morphometric data between the meta- podes of horses, hemiones, asses and Equus hydrunti- nus (Eisenmann & Beckouche, 1986). The latter do not alter the correlation between all the variables analyzed. In our opinion, it is a mistake to interpret these partial overlaps as continuity. The distal limb of horses is close- ly related to the adaptation to different environments, type of substrates, body weight, and locomotion. The adaptive nature of metapodials and phalanges variation can be explained by the differential success of lineages in macroevolution. Lineages with more advantageous patterns of regulated variation are likely to produce more species (Sharov, 2014). This is in relation to the epige- netic mechanisms that provide organisms with opportu- nities for rapid adaptive change (Gokhman et al., 2016). The epigenome is viewed today as a collection of regu- latory layers that control when, where, and how genes <<<<< - - - - - - - - - - - - - - - - - - - - Fig. 1 - Geographic distribution of different taxa of Hippidion and Equus from South America. In Argentina: 1-35, Arrecife; 2-34, Mercedes (Luján); 3-25, Arenero Spósito y Venta Obligado (San Pedro); 4, Ayacucho; 5, Necochea; 6, Arroyo Seco; 7-39, Montehermoso; 8, Río Quequén Salado; 9, Paso Otero 5; 10-33, Arroyo Ramallo; 11, Arroyo Tapalqué; 12, Calera Avellaneda; 13, Anchorena; 14-38, Barrancas de San Lorenzo y Alvear (Santa Fé province); 15, Los Toldos; 16, Las Buitreras; 17, Cerro Bombero; 18, Piedra Museo; 19, Voruheé; 20, Mar del Sur; 21, Lobería; 22, Olivos; 23, Canal de Conjución en puerto La Plata; 24, Mar del Plata; 26, margen izquierda del Río Quequén Grande (Buenos Aires); 27, Barranco Negro (Jujuy); 28, Esquina Blanca in Uquía; 29, Río Salado; 30, San Luis; 31, Carcaraña; 32, Uspallata; 36, Anchorena; 37, Quequén Salado; in Bolivia: 40-42, Tarija; 41-43, Ulloma; in Brazil: 44, Santana (Estado de Bahia); 45-68, Toca dos Ossos (Estado de Bahia); 46-63, grutas de la región de Lagoa Santa; 47, Confins (Lapa do Galinheiro); 48, Lapa Come Nâo bebe; 49, Lapa de Bahu and Lapa de Escribanía (Estado de Minas Gerais); 50, Rio Paraguai in Corumba (Estado de Mato Grosso do Sul); 52, Curaçaba (Estado de Bahia); 53, Santa Vitoria do Palmar (Rio Grande do Sul); 54, Tanque 2 de Itapipoca (Estado Ceará); 55, Curimatãs (Estado de Paraíba); 56, Lage Grande (Alagoinha); 57, Pesqueira (Estado de Pernambuco); 58, Lapa do Cavalo; 59, Lapa de Escribanía 5 and 11; 60, Lapa da Lagoa do Sumidouro; 61, Lagoa Santa Flere Hule Lapa dos Coses; 62, Lapa do Galinheiro; 64, Sao Raimundo Nonato; 65, Piaui; 66, Aguas do Araxa; 67, Chique-Chique; in Chile: 69, Cueva del Milodón (Ultima Esperanza); 70, Cueva Lago Sofia 1; 71, Cueva Lago Sofia 4; 72, Cueva de la Ventana; 73, Cueva del Medio; 74, Cueva de los Chinges; 75, Cueva Fell; 76, Cerro Sota; 77, Alero Tres Arroyos 1; 78, Betecsa 1; 79, Kamac Mayu (Atacana Desert); 80, Chacabuco; 81, Santa Rosa de Chena; 82, Tierras Blancas; 83-93, Taguatagua; 84, Cueva Pali Aike; 85-86, Calera, Lo Aguirre; 87, Valle de Elqui; 88, Los Vilos; 89, Conchalí; 90, Colina; 91, Punta Rieles; 92, Huimpil; in Colombia: 94, Cerrogordo; 95, Tibitó; in Ecuador: 96, Quebrada Otón; 97, Riobamba; 98, Punín (Quebrada Chalán, Quebrada Colorada, Quebrada Grande, Quebrada El Colegio, etc); 99, Alangasí; 100, La Carolina; 101, Salinas Oil Fields (Santa Elena Peninsula); 102, Río Chiche (Andes Ecuadorian); in Perú: 103, Tirapata; in Uruguay: 104, Formación Sopas, Artigas Department; 105, Arapey Grande creek; 106, Sopas Creek in the Sopas Formation; in Venezuela: 107, Breal de Orocual; 108, Inciarte (Estado de Zulia). Modified from Prado & Alberdi (2017). are turned on and off. The promising new high-coverage genome of horses (Schubert et al., 2014; Gaunitz et al., 2018; Librado et al., 2017) will enable paleoepigenetic reconstruction in the near future. The other group of horses in South America is the hippidiforms. Owen (1869) created the genus Hippidion based on only one molar from Brazil. In 1891, Moreno described one complete skull and some postcranial remains from the Pleistocene of Lobería (Argentina), and assigned it to Onohippidium munizi. The uncertainty began after the nomination and description of both gen- era in North America by MacFadden & Skinner (1979). Alberdi & Prado (1993, 2004) recognized just one ge- nus, Hippidion, which is endemic to South America, and that the materials from North America assigned to both genera were not hippidiforms, but closer to Dinohippus (Prado & Alberdi, 1996; Alberdi & Prado, 1998). Avilla et al. (2015) proposed a new genus (Boreohippidion) for the remains described as Onohippidium in North Ameri- ca. Hippidion is recorded from the Pliocene to the late Pleistocene mainly in Argentina, Bolivia, Brazil, Chile, Peru, and Uruguay (Figure 1). Prado & Alberdi (2017) recognized three species: Hippidion principale (Lund), Hippidion devillei (Gervais), and Hippidion saldiasi (Roth) (Figures 3 and 4). These species differ mainly by their body size. Hippidion principale is much larger than others, and the differences between Hippidion saldiasi and Hippidion devillei are based on the shortening meta- podial (Fig. 5). Hippidion is characterized by a retracted nasal notch, which has been interpreted as an adapta- tion to the presence of a proboscis and limbs with robust metapodials (Figures 4 and 5). The upper teeth present an oval protocone, more or less rounded, with simple enamel plication, and the lower teeth have a deep ec- toflexid, penetrating the isthmus, and a rounded para- conid and hypoconid. 2. PHYLOGENY The South America species of Equus, genus shows horse-like anatomical features and genetic affini- ties (Orlando et al., 2009). Biochronological data sug- 46 Fig. 2 - Skull of different Equus species. 1: Equus neogeus from Luján, Buenos Aires province, Argentina; 2: Equus insulatus from La Carolina, Santa Elena Peninsula, Ecuador; 3: Equus andium from Chalan Punín, Ecuador. Fig. 3 - Upper and lower cheek teeth length of different Equus and Hippidion species. 1: P2-M3 left of Hippidion saldiasi from Betecsa 1, Calama (II Región, Chile); 2: P2-M3 left of Equus neogeus from Arroyo Tapalqué at level of Avellaneda street, Olavarría (Buenos Aires province, Argentina); 3: p2-m3 right of Hippidion principale from Monte Hermoso (Buenos Aires prov- ince, Argentina); 4: p2-m3 right of Equus neogeus from Monte Hermoso (Buenos Aires province, Argentina). Alberdi M.T. & Prado J.L. gests most of these occurrences are late Pleistocene; with one significant exception from the Tarija basin in Bolivia were Equus insulatus is recorded between 0.99 to 0.76 Ma (sensu MacFadden, 2013). The Hippidion genus was first recorded at around 2.5 Ma, and includes two genetically similar generalists (Hippidion principale, Hippidion saldiasi) and one genet- ically distinct high-altitude specialist, Hippidion devillei (Prado & Alberdi, 1996; Orlando et al., 2009). Currently, the diversification of Hippidion species remains contro- versial. Prado & Alberdi (1996) proposed, on the basis of a cladistic analysis using morphological data, the affinity of Hippidion with Pliohippus. The latter is record- ed between 6 and 14 Ma in North America. Also, Hip- pidion would have diverged from the lineage that leads to modern Equidae before 10 Ma. This implies a disper- sion prior to the time when Hippidion is recorded for the first time in South America. On the contrary, a much later divergence date, with Hippidion nesting within modern equids, was indicated by the study of partial ancient mitochondrial DNA sequences (Weinstock et al., 2005). This analysis proposed that Hippidion was phylo- genetically close to the caballine horses, with origins considerably more recent than the accepted date of around 10 Ma. Furthermore, based on analysis of an- cient DNA, Orlando et al. (2009) proposed Hippidion devillei clusters outside a paraphyletic assemblage con- 47 sisting of Hippidion principale and Hippidion saldiasi. Recently, Der Sarkissian et al. (2015) obtained new mitochondrial data and suggested that the two morphos- pecies sequences (Hippidion saldiasi and Hippidion principale) formed a monophyletic clade, basal to extant and extinct Equus lineages. This contrasts with previous genetic analyses, and supports Hippidion as a distinct genus. This new data allowed us to estimate the diver- gence between Hippidion and Equus at approximately 5.6 to 6.5 Ma before Hippidion entered South America, following the formation of the Panamanian Isthmus 3.0 to 3.7 Ma. 3. PALAEOBIOGEOGRAPHY The contemporary South American mammalian communities were determined by the emergence of the Isthmus of Panama, and by the profound climatic oscil- Fig. 4 - Skull of different Hippidion species. 1: Hippidion principale from Mar del Plata, Argentina; 2: Hippidion devillei, incomplete, from Tarija, Bolivia; 3: Hippidion saldiasi from Calama, Chile. Fig. 5 - Metapodials of different Hippidion and Equus species: 1: MCIII of Hippidion principale from Tarija, Bolivia; 2: MCIII of Hippidion devillei from Tarija, Bolivia; 3: MCIII of Hippidion salsiasi from Última Esperanza, Punta Arenas, Chile; 4: MTIII of Equus neogeus from Quequén Salado-Indio Rico, Buenos Aires province, Argentina; 5: MTIII of Equus insulatus from Santa Elena Peninsula, Ecuador; 6: MTIII of Equus andium from Riobamba, Ecuador. Fossil horses from South America lations during the late Pliocene and Pleistocene. The emergence of the Isthmus closed communication be- tween the Atlantic and Pacific oceans and changed both water circulations, facilitating the installation of the Arctic polar ice cap. The cool Circum-Antarctic Current was finally established (Pascual et al., 1996). The Pliocene in South America is characterized by the apogee of the Age of the Southern Plains (Ortiz-Jaureguizar & Cladera, 2006). In northern South America, the Pliocene vegetation changed sequentially from tropical lowland to high-elevation vegetation as a result of the developing Andes. On the contrary, in southern South America, grasslands and steppes were dominant. The most evi- dent changes between Tertiary and Quaternary climatic conditions are correlated to the amplitude and frequency of the environment. Throughout the Pleistocene, the repeated advance and retreat of glaciers produced an evident and coincident expansion and retraction of arid and humid environments. A savannah corridor devel- oped along the eastern border of the Andes, offering a corridor that linked the grasslands of Argentina and Colombia, continuing northward across the Panamanian land bridge to North America. Conversely, when open areas withdrawal during interglacial periods of warm-wet climates, rainforests enlarge and favored a second corri- dor to expand across eastern South America (Sánchez et al., 2004). The GABI is a complex history of multiple dispersal events between the Americas during the Pliocene and Pleistocene. Horses were a conspicuous group of immi- grant mammals from North America. Their demographic history was punctuated by major cycles of expansions and collapses, probably related to the major glacial and interglacial cycles. These dispersions event coincided with the devel- opment of two dispersal pathways (Webb, 1991), that ultimately contributed to the distribution of horses (Prado & Alberdi, 2014). Recent biogeography studies based both on phyto- and zoogeographic data, show that South America is composed of two regions with different evolutionary histories and showing closest links with other Austral areas. This pattern is evident in the recent distributions, and in the fossil record dispersion. Compiling numerous sources of information, Morrone (2014), confirmed the Neotropical and Andean regions, separated by the Andean Cordillera, which in turn di- vides the continent into two different areas: western and eastern. The dispersal and the diversification process in small to middle size species, Equus andium, Equus insulatus, Hippidion devillei, and Hippidion saldiasi, oc- curred through the Andes corridor, whereas the large species, Equus neogeus, and Hippidion principale used the eastern plain route, firstly (Fig. 6). The pathway of dispersion in each species reflects its adaptive change and habitat preference (Alberdi & Prado, 1992) and may have occurred during two or three immigration events. Woodburne (2010) described the principal phases of interchange between the Americas as GABI 1 (2.6 to 2.4 Ma), GABI 2 (1.8 Ma), GABI 3 (1.0 to 0.8 Ma) and GABI 4 (0.125 Ma). In this context, MacFadden (2013) suggest that Equus neogeus may have originated inde- pendently from a North American sister species within the caballine clade, thus suggesting a second dispersal of Equus during GABI 4 at 0.125 Ma. The first arrival corresponded to Equus insulatus recorded in Tarija (Bolivia) and dispersal through the Andes corridor during GABI 3 (MacFadden & Azzaroli, 1987; MacFadden, 2013). Equus neogeus is the largest and most slender morphotype of the South American horses, and occurs in eastern South America, but does not occur outside of lowland Argentina, Uruguay, and Brazil. This species preferred savannas and consequently would have been better adapted to open and arid landscapes (Prado & Alberdi, 1994). The first record of Hippidion came from Esquina Blanca (Jujuy, Argentina) were Hippidion dev- illei appears in a sedimentary layer dated around 2.5 Ma (Prado et al., 1998, 2000; Reguero et al., 2007) and corresponds to GABI 1. 4. BIOCHRONOLOGY The SALMA are stratigraphic units not formally recognized by any code of nomenclature, but as an or- ganizing device. They have proven to be very useful in developing concepts about mammalian stratigraphy and evolution (Savage, 1962; Simpson, 1971). Pascual et al. (1996) suggest that SALMA has proved to be useful for intra and intercontinental correlations and subdividing 48 Fig. 6 - The geographic distribution of the Equini tribe from South America and possible migratory routes. Small to middle size species through the Andes corridor (Equus andium, Equus insulatus, Hippidion devillei, Hippidion saldiasi) in orange and the large forms (Equus neogeus, Hippidion principale) used the eastern plain route in violet. Modified from Prado & Alberdi (2017). Alberdi M.T. & Prado J.L. stages in the Pampean Region. In this paper, we follow both of these criterions to establish the chronological position of the horses (Figure 7). According to Alberdi & Prado (2004), Hippidion devillei was the first species of the Equini recorded in South America. It is found in land-mammal bearing sedi- ments of the Uquian SALMA in northern Argentina (Prado et al., 1998). Hippidion principale was recorded for the first time in sediments of the Ensenadan SALMA in Bolivia. Hippidion saldiasi was recorded in sediments of the Lujanian SALMA in Patagonia, Argentina (Alberdi Cenozoic time. The Land Mammals Ages were first pro- posed by Wood et al. (1941) and characterized by unique mammalian assemblages. Pascual et al. (1965, 1966), Marshall et al. (1983, 1984) and Pascual et al. (1996) among others, used SALMA for South America. Recently, Cione & Tonni (2005) proposed a new bio- stratigraphic framework involving the continental sedi- ments and faunas of the Pampean region, from the Late Miocene to the present. These authors recognized 13 biozones for this interval, which represent the biostrati- graphic basis for the recognition of stages and sub- 49 Fig. 7 - The chronological framework of mammalian biochronology of South America modified from Cione & Tonni (1999). Fossil horses from South America & Prado, 2004). So far as the biochronology is known, most of these occurrences of Equus are late Pleisto- cene; with one significant exception of Equus insulatus from the Tarija basin of Bolivia. In Argentina, Uruguay and Brazil, Equus occurred during the latest Pleisto- cene, and it defines the base of the Lujanian SALMA (sensu Pascual et al., 1996). In the Pampean Region, Cione et al. (2009) proposed the Equus neogeus bi- ozone based on the “Piso Lujanense” from Ameghino. Nevertheless, if Equus is restricted to the Pampean species Equus neogeus, then the use of this latter taxon still can be used as an index fossil for the Lujanian Stage within the Pampean region. It is clear that the Lujanian Stage or Biozone of Equus neogeus defined by Cione & Tonni (1999, 2005) does not correspond to the Lujanian SALMA of Pascual et al. (1965, 1996). Recent- ly, we recorded remains assigned to Equus neogeus from the Campo Spósito site (province of Buenos Aires). This site was referred to the Bonarian Stage, with a base at ~130 ka and top at 10 Ka. The level containing the remains of Equus was dated by OSL, ESR and U-Th series between 40 to 200 ky BP (Prado et al., 2012; Toledo et al., 2014, 2015). These findings implied that the status of Equus neogeus as an index fossil of the Lujanian Stage, or its lower limit, should be revised as this taxon clearly expanded in the Pampean region be- fore ~130 ka BP. Also, these results reinforce the fact that Equus dispersed into South America during GABI 3. Argentina has allowed discussions on the correlation of type sections in the Pampean area with other regions (e.g. Reguero & Candela, 2011; Tauber, 2005). It is necessary to carry out new studies in areas outside the Pampean region to contrast this scheme. 5. PALAEOECOLOGY The skeleton of the fossils mammals has been the main source of information for interpreting its ecology. Several studies in horses from South America document changes in body size, skull magnitudes, dentition mor- phology and limb structure (Alberdi & Prado, 1993; Al- berdi et al., 1995; Bernardes et al., 2013; Prado & Alber- di, 1994, 2014). Additionally, the use of stable isotopes in fossil horses has been successfully increased (Domingo et al., 2012; Dantas et al., 2013; Prado et al., 2015; among others), and have contributed to under- standing the feeding paleoecology of extinct species (MacFadden et al., 2004). Carbon is fixed through plant photosynthesis, which has three different pathways: C3 (Calvin-Benson), C4 (Hatch-Slack), and CAM (crassulacean acid metabolism). The C3 pathway is found mainly in dicotyledonean trees and shrub, and in some temperate grasses. The C4 pathway is typical of monocotyledonean grasses, as well as some trees and shrubs from warm regions (Cerling et al., 1997) and the CAM pathway is found in succulent plants such as cacti and bromeliads. Several factors, such as saline soils, low light intensity, and a lack of nutrients, affect the abundance of C3 and C4 plants in ecosystems. The tem- perature plays an important role, as localities with tem- peratures below 25 °C show an increase in C3 plants while C4 plants decrease (Ehleringer & Cerling, 2002). 50 In mammals, digested carbon becomes incorporated into the tissue of the consumer; this is the case for den- tal enamel apatite (Koch, 2007). Herbivores have carbon isotopic values enriched by 14‰ in comparison with plant δ13C values (Cerling & Harris, 1999). Based on classifications proposed by Hofmann & Stewart (1972) and MacFadden & Cerling (1996), C4 plant eaters show values from -2‰ to 2‰, C3 plant eaters have values from −19 ‰ to −9‰, and C3/C4 mixed-diet herbivores show values between −9‰ and −2‰. The δ13C values of herbivore teeth record a dramatic increase in con- sumption of C4 grasses during the late Miocene and provide the first evidence for appearances of C4 grass in the past (Strömberg, 2004). Based on mesowear and microwear analyses, Fig. 8 - Average and standard error of isotopic values from differ- ent localities in Argentina, Bolivia, Colombia and Ecuador of Equus (a) and Hippidion (b). A: Alangasi, AT: Arroyo Talpaqué, B: Buenos Aires, CV: Cantera Vial. Buenos Aires province, CM: Centinela Mar, E: Última Esperanza, LB: La Banda, LC: La Carolina, LV: La Venta, L: Luján, M: Magdalena, N1: Napua-1, N3: Napua-3, O: Ourolandia, PH: Punta Hermengo, PO: Paso Otero, P: Punín, Q: Quebrada Colorada, RC: Río Chiche, RQ: Río Quequén, S: Salinas Oil, T: Tarija, Z: Zajón Seco, MA: Mina Aguilar, O: Olivos, P: Paraná, B: Buenos Aires, L: Luján, S: Río Salado, A: Arroyo Talpaqué, Q: Rio Quequén, E: Última Esperanza. Modified from Prado & Alberdi (2017). Alberdi M.T. & Prado J.L. Mihlbachler et al. (2011) showed that Pleistocene hors- es from North America are able to mainly eat not only grass but also leaves off trees or shrubs. MacFadden et al. (1996) suggested the existence of a latitudinal gradi- ent, meaning that above 35° latitude, C3 plants start to increase while C4 plants decrease. The South American horses in general were C3/C4 mixed feeders and lived in grasslands or prairies. Although there were some popu- lations that exclusively fed on C3 and occupied forest habitat and other that fed on C4 plants and living in grassland zones (Pérez-Crespo et al., 2018). The horse populations from Argentina show that they mainly ate C3 plants, which indicated the presence of C3 grassland areas (Domingo et al., 2012). On the other hand, horses from Colombia, Brazil, and Perú, located above parallel 35°, were specialized C4 plants feeders. Domingo et al. (2012) also indicated the presence of a vegetation ele- vation gradient, where C4 plants were abundant in lower zones, and C3 plants were abundant in higher zones, explaining the diet of Bolivian and Ecuadorian popula- tions. The flexibility in their diet and by extension in their occupied biome agrees with the habitat theory (Vrba, 1992) according to which generalists and open biome specialists from North America accomplished successful radiation throughout South America (Moreno Bofarull et al., 2008). Hippidion only fed on C3 plants, although some individuals were C3/C4 mixed feeders, but with important ingest of C3 plants (Prado et al., 2011; Pérez-Crespo et al., 2016). This could be explained by the fact that some individuals inhabited higher elevations, where C3 plants are abundant, or lower latitude than 35°S on C3 were predominate grasslands with nearby forests (Domingo et al., 2012). Samples from early Pleistocene show that Hippidion principale and Hippidion devillei have δ13C values typical of wooded C3 grassland (Figure 8a). Hip- pidion devillei and Hippidion saldiasi have lower δ18OCO3 values than Hippidion principale (Figure 8b). This is due to high elevation effects in the case of Hippidion devillei, and high latitude effects in the case of Hippidion saldiasi (52° S). Another important indicator of horses’ ecology is the body size. In all continents, the evolutionary history of the horse was strongly influenced by body size, relat- ed with environmental conditions and type of substrates (Shoemaker & Clauser, 2014; Saarinen et al., 2016). 51 Fig. 9 - Last-appearance dates for megafauna from the Argentine Pampas region, using only robust dates from previous papers and the new dates. The horizontal dashed line indicates a consistent archeological signal. The dotted horizontal line indicates the earliest occupa- tion evidence or minimal human activity. The gray boxes indicate the dates obtained from the literature, the red boxes indicate radiocarbon data of South American horses, and the yellow line is the average of these. Black boxes indicate the new dates and the green line is the average of these. The gray band denotes the timing of Younger Dryas cooling in the Argentine Pampas region (Hajdas et al., 2003; Krohling & Iriondo, 1999) (Modified from Prado & Alberdi, 2017). Fossil horses from South America Alberdi et al. (1995) present the body mass predictions for South American fossil horse species. Both genera present different patterns. Within the Hippidion group, the middle sized Hippidion devillei produced two body mass species: (1) Hippidion saldiasi, which has a similar body mass, and (2) Hippidion principale, which reaches a greater size. In the Equus group, the large-sized Equus insulatus gave rise to two different sized groups: (1) Equus neogeus, which retain or increase their body mass; and (2) the small Equus andium. 6. HORSE EXTINCTION Late Quaternary megafauna extinctions impover- ished mammalian diversity worldwide (Koch & Bar- nosky, 2006). About 70% of South American large mammal species (animals with an average body size ≥ 44 kg) went extinct at the end of the Pleistocene epoch (Prado et al., 2015). The causes of this extinction - the role of humans versus climate - have been the focus of much controversy (Barnosky & Lindsey, 2010; Prado & Alberdi, 2016, 2017; Villavicencio et al., 2016). Horses have figured centrally in this discussion because it’s a species that dominated late Pleistocene faunas in terms of abundance and geographical distribution, but none survived into the Holocene. On a global scale, several species of horses were widespread and com- mon during the middle and late Pleistocene, with a dis- tribution that covered most of Eurasia and northern Afri- ca, as well as North and South America. The late Pleis- tocene was a period of extraordinarily intense environ- mental change. By the end of this period, the last glacial maximum (LGM) marked one of Earths most extreme moments of climatic variability (Clark et al., 2009). The decreased grassland in Eurasia due to of the LGM caused a massive crash in the horse population. How- ever, one formerly wild subspecies (Equus ferus prze- walskii) had survived, and abundant genetic diversity has been preserved in domesticated forms (Orlando et al., 2009; Weinstock et al., 2005). The new world stilt- legged horses disappeared around 30 ka BP in North America, before the earliest arrival of humans (Weinstock et al., 2005; Vilstrup et al., 2013; Prado & Alberdi, 2017). In South America, Hippidion and Equus survived no later than 10 ka BP (Prado & Alberdi, 2016, 2017). The timing of the horse extinctions in each region of South America is poorly known. There are many ar- cheological sites with recorded horses, but the coexist- ence with humans is difficult to verify. The taxon dates evidence is very rare and are strictly concentrated in two regions, Pampas and Patagonia (Borrero, 1997; Alberdi & Prado, 2004). The extinction window in Pampas rang- es from c. 13.9 and 10.1 ka BP for Equus neogeus and c. 11.3 to 15 ka BP for Hippidion principale (Prado et al., 2015; Figure 9). The archaeological record from south- ern Patagonia indicates that the timing of horse extinc- tion was restrained by a complex interaction between climate changes that precipitated vegetation change, associated with growing human impacts (Villavicencio et al., 2016). The data from Pampas and Patagonia are robust enough to consider synergy interaction among last appearance records of horses, first appearance records of humans, and the Holocene climatic transi- tions. However, the evidence is still scarce in other re- gions in South America. ACKNOWLEDGEMENTS This paper is dedicated to the memory of Antonello Bonadonna, for his dedication to the geology and the paleontology, its important contributions to geology and paleontology will always be remembered. The authors wish to express many thanks to Giovanni Zanchetta for your invitation to participate in this volume. The authors show gratitude to Dan Rafues, whose mother tongue is English, by revised the text. This work has been made possible thanks to Research Project ANPCYT PICT 2015-1512 to JLP; DGICYT CGL2016-79334-P from Spain to MTA; and Grant of the National University of Central Argentina (UNICEN) to JLP. REFERENCES Alberdi M.T. (1987) - La Familia Equidae, Gray, 1821 (Perissodactyla, Mammalia) en el Pleistoceno de Sudamérica. In: IV Congreso Latinoamericano de Paleontología, Santa Cruz de la Sierra, Bolivia, 1, 484-499. Alberdi M.T., Prado J.L. (1992) - El Registro de Hippidion Owen, 1869 y Equus (Amerhippus) Hoffstetter, 1950 (Mammalia, Perissodactyla) en América del Sur. Ameghiniana, 29, 265-284. Alberdi M.T., Prado J.L. (1993) - Review of the genus Hippidion Owen, 1869 (Mammalia; Perissodactyla) from the Pleistocene of South America. Zoological Journal of the Linnean Society, 108, 1-22. Alberdi M.T., Prado J.L. (1998) - Comments on: Pleisto- cene horses from Tarija, Bolivia, and validity of the genus Onohippidium (Mammalia: Equidae) by B.J. MacFadden. Journal of Vertebrate Paleontology, 18(3), 669-672. Alberdi M.T., Prado J.L. (2004) - Caballos fósiles de América del Sur. Una historia de tres millones de años. Universidad del Centro de la Provincia de Buenos Aires, INCUAPA serie monográfica 3, Olavarria pp. 269. Alberdi M.T., Fernández J., Menegaz A.N., Prado J.L. (1986) - Hippidion Owen 1869 (Mammalia, Perissodactyla) en sedimentos del Pleistoceno tardío de la localidad Barro Negro (Jujuy, Argentina). Estudios Geológicos, 42, 487-493. Alberdi M.T., Menegaz A.N., Prado J.L. (1987) - Formas terminales de Hippidion (Mammal ia, Perissodactyla) de los yacimientos del Pleistoceno Tardío - Holoceno de la Patagonia (Argentina y Chile). Estudios Geológicos, 43, 107-115. Alberdi M.T., Prado J.L., Ortiz Jaureguizar E. (1995) - Patterns of Body Size changes in fossil and living Equini (Perissodactyla). Biological Journal of the Linnean Society, 54, 349-370. Ameghino F. (1904) - Recherches de Morphologie Phy- lognetique sur les molaires supérieures des Ongulés. Anales del Museo Nacional, 3, 1-541. Avilla L.S., Bernardes C., Mothé D. (2015) - A New ge- 52 Alberdi M.T. & Prado J.L. nus for Onohippidium galushai MacFadden BJ, Skinner MF, 1979 (Mammalia, Equidae), from the Late Hemphillian of North America. Journal of Vertebrate Paleontology, 35(3) Doi: 10.1080/02724634.2014.925909 Barnosky A.D., Lindsey E.L. (2010) - Timing of Quater- nary megafaunal extinction in South America in relation to human arrival and climate change. Qua- ternary International, 217, 10-29. Bernardes C., Sicuro F.L., Avilla L.S., Pinheiro A.E.P. (2013) - Rostral reconstruction of South American hippidiforms (Mammalia, Perissodactyla, Equi- dae): new anatomical and ecomorphological infer- ences. Acta Palaeontologica Polonica, 58, 669- 678. Borrero L.A. (1997) - The Extinction of the Megafauna: A Supra-Regional Approach. Anthropozoology, 25 -26, 209-216. Branco W. (1883) - Ueber eine Fossile Säugethier- Fauna von Punin bei Riobamba in Ecuador. II: Beschreibung der Fauna. Palaeontologische Ab- handlunge, 1, 57-204. Cantalapiedra J.L., Prado J.L., Hernádez Fernández M., Alberdi M.T. (2017) - Decoupled ecomorphological evolution and diversification in Neogene- Quaternary horses. Science, 355, 627-630. Cerdeño E., Moreiras S., Alberdi M.T. (2008) - Primeros hallazgos del équido Hippidion (Perissodactyla) en el Pleistoceno de la provincia de Mendoza. Re- vista del Museo Argentino de Ciencias Naturales, 10(2), 211-220. Cerling T.E., Harris M.J. (1999) - Carbon isotope frac- tionation between diet and bioapatite in ungulate mammals and implications for ecological and pale- oecological studies. Oecologia, 120, 347-363. Cerling T.E., Harris M.J., MacFadden B.J., Leakey M.G., Quade J., Eisenmann V., Ehleringer J.R. (1997) - Global Vegetation Change through the Miocene/Pliocene Boundary. Nature, 389, 153- 158. Cione L.A., Tonni E.P. (1999) - Biostratigraphy and chronological scale of uppermost Cenozoic in the Pampean area, Argentina. In: Tonni E.P. & Cione A.L. (Eds.): Quaternary vertebrate palaeontology in South America. Quaternary of South America and Antarctic Peninsula, 12, 23-52. Cione L.A., Tonni E.P. (2005) - Biostratigrafía basada en mamíferos del Cenozoico superior de la Región Pampeana. In: Barrio R., Etcheverry R.O., Caballé M.F. & Llambías E. (Eds.): Geología y Recursos Minerales de la provincia de Buenos Aires (Relatorio del XV Congreso geológico Argentino, La Plata, 11, 183-200. Cione A.L., Tonni E.P., Soibelzon L. (2009) - Did hu- mans cause the late Pleistocene-early Holocene mammalian extinctions in South America in a con- text of shrinking open areas? In: Haynes G. (Ed.): American Megafaunal Extinctions at the End of the Pleistocene, Springer, New York, 125-144. Clark P.U., Dyke A.S., Shakun J.D., Carlson A.E., Clark J., Wohlfarth B., Mitrovica J.X., Hostetler S.W., McCabe A.M. (2009) - The last glacial maximum. Science, 325, 710-714. Coltorti M., Pieruccini P., Paredes Rios F. (2010) - Late Pleistocene stratigraphy, sedimentology and pale- oenvironmental evolution of the Tarija-Padcaya basin (Bolivian Andes). Proceedings of the Geolo- gist’s Association, 121, 162-179. Dantas M.A.T., Dutra R.P., Cherkinsky A., Fortier D.C., Kamino L.H.Y., Cozzuol M.A., Ribeiro A.S., Silva F.V. (2013) - Paleoecology and radiocarbon dating of the Pleistocene megafauna of the brazilian inter- tropical region. Quaternary Research, 79, 61-65. Der Sarkissian C., Vilstrup J.T., Schubert M., Seguin-Orlando A., Eme D., Weinstock J., Alberdi M.T., Martin F., Lopez P.M., Prado J.L., Prieto A., Douady C.J., Stafford T.W., Willerslev E., Orlando L. (2015) - Mitochondrial genomes reveal the ex- tinct Hippidion as an outgroup to all living equids. Biology Letters, 11(3), 20141058. Domingo L., Prado J.L., Alberdi M.T. (2012) - The effect of paleoecology and paleobiogeography on stable isotopes of Quaternary mammals from South America. Quaternary Science Reviews, 55, 103- 113. Ehleringer J.R., Cerling T.H. (2002) - Stables isotopes. In: Mooney, H.A., Canadell, J.G. (Eds.): The Earth System: Biological and Ecological Dimensions of Global Environmental Change, Encyclopedia of Global Environmental Change, vol. 2. John Wiley and Sons, Ltd, Chichester, pp. 544-550. Eisenmann V. (1979) - Les Métapodes d’Equus sensu lato" (Mammalia, Périssodactyla). Geobios, 12(6), 863-886. Eisenmann V. (1984) - Sur quelques caractères adap- tatifs du squelette d'Equus" (Mammalia, Perisso- dactyla) et leurs implications paléoécologiques. Bulletin du Muséum National d'Histoire Naturelle de Paris, 4(6), 185-195. Eisenmann V., Beckouche S. (1986) - Identification and Discrimination of Metapodials from Pleistocene and Modern Equus, Wild and Domestic. In: Mead- ow R.H., Uerpmann H-P. (eds): Equids in the An- cient World, Beihfte zum Tübingen Atlas des Vor- deren Orients, Reihe A, Naturwissenschaften, 19 (1), 117-163. Gaunitz C., Fages A., Hanghøj K., Albrechtsen A., Khan N., Schubert M., Seguin-Orlando A., Owens I.J., Felkel S., Bignon-Lau O., de Barros Damgaard P., Mittnik A., Mohaseb A.F., Davoudi H., Alquraishi S., Alfarhan A.H., Al-Rasheid K.A.S., Crubézy E., Benecke N., Olsen S., Brown D., Anthony D., Massy K., Pitulko V., Kasparov A., Brem G., Hofreiter M., Mukhtarova G., Baimukhanov N., Lõugas L., Onar V., Stockhammer P.W., Krause J., Boldgiv B., Undrakhbold S., Erdenebaatar D., Lepetz S., Mashkour M., Ludwig A., Wallner B., Merz V., Merz I., Zaibert V., Willerslev E., Librado P., Outram A.K., Orlando L. (2018) - Ancient ge- nomes revisit the ancestry of domestic and Prze- walski’s horses. Science, 360, 111-114. Doi: 10.1126/science.aao3297 Gokhman D., Meshorer E., Carmel L. (2016) - Epigenet- ics: It’s Getting Old. Past Meets Future in Paleoep- 53 Fossil horses from South America igenetics. Trends in Ecology & Evolution, 31, 290- 300. Hajdas I., Bonani G., Moreno P.I., Ariztegui D. (2003) - Precise radiocarbon dating of Late-Glacial cooling in mid-latitude South America. Quaternary Research, 59(1), 70-78. Hoffstetter R. (1950) - Algunas observaciones sobre los caballos fósiles de América del Sur. Amerhippus gen. nov. Boletín Informativo de Ciencias Nacionales, 3, 426-454. Hoffstetter R. (1952) - Les Mammifères Pléistocènes de la République de l'Équateur. Mémoires de la Societé Géologique de France, NS 31(1-4), 1-391. Koch P.L. (2007) - Isotopic study of the biology of mod- ern and fossil vertebrates. In: Michener R., Lajtha K. (Eds): Stable Isotopes in Ecology and Environ- mental Science, 2nd Edition. Boston: Blackwell Publishing. 99-154. Koch P.L., Barnosky A.D. (2006) - Late Quaternary ex- tinctions: state of the debate. Annual Review of Ecology, Evolution and Systematics, 37, 215-250. Krohling D.M., Iriondo, M. (1999) - Upper Quaternary palaeoclimates of the Mar Chiquita area, North Pampa, Argentina. Quaternary International, 57/58, 149-163. Librado P., Gamba C., Gaunitz C., Der Sarkissian C., Pruvost M., Albrechtsen A., Fages A., Khan N., Schubert M., Jagannathan V., Serres-Armero A., Kuderna L.F.K, Povolotskaya I.S., Seguin-Orlando A., Lepetz S., Neuditschko M., Thèves C., Alquraishi S., Alfarhan A.H., Al-Rasheid K., Rieder S., Samashev Z., Francfort H-P., Benecke N., Hofreiter M., Ludwig A., Keyser C., Marques-Bonet C., Ludes B., Crubézy E., Leeb T., Willerslev E., Orlando L. (2017) - Ancient genomic changes associated with domestication of the horse. Science, 356, 442-445. Lund P.W. (1840) - Nouvelles Recherches sur la Faune Fossile du Brésil. Annales de Sciences Naturais, 13, 310-319. MacFadden B.J. (1992) - Fossil Horses. Systematics, Paleobiology, and Evolution of the Family Equi- dae. Cambridge University Press, New York, pp. 369. MacFadden B.J. (2013) - Dispersal of Pleistocene Equus (Family Equidae) into South America and Calibration of GABI 3 Based on Evidence from Tarija, Bolivia. PlosOne, 8(3), e59277. MacFadden B.J., Azzaroli A. (1987) - Cranium of Equus insulatus (Mammalia, Equidae) from the Middle Pleistocene of Tarija, Bolivia. Journal of Vertebrate Paleontology, 7(3), 325-334. MacFadden B., Cerling T.E. (1996) - Mammalian herbi- vore communities, ancient feeding ecology, and carbon isotopes: a 10 millioneyear sequence from the Neogene of Florida. Journal of Vertebrate Pal- aeontology, 16, 103-115. MacFadden B.J., Skinner M.F. (1979) - Diversification and Biogeography of the one-toed horses Onohip- pidium and Hippidion. Postilla, 175, 1-10. MacFadden B.J., Anaya F., Argollo J. (1993) - Magnetic Polarity Stratigraphy of Inchasi a Pliocene Mam- mal-Bearing locality from the Bolivian Andes de- posited just before the Great American Inter- change. Earth Planetary Sciences Letters, 114, 229-241. MacFadden B.J., Higgins P., Clementz M.T., Jones D.S. (2004) - Diets, habitat preferences, and niche dif- ferentiation of Cenozoic sirenians from Florida: evidence from stable isotopes. Paleobiology, 30 (2), 297-324. Machado H., Grillo O., Scott E., Avilla L. (2017) - Follow- ing the Footsteps of the South American Equus: Are Autopodia Taxonomically Informative? Journal of Mammal Evolution, 25(3), 397-405. Doi: 10.1007/s10914-017-9389-6 Marsh O.C. (1874) - Notice of new equine mammals from the Tertiary formation. Journal of Natural History, 13(77), 397-400. Marshall L.G., Hoffstetter R., Pascual R. (1983) - Mam- mals and stratigraphy: geochronology of the Conti- nental Mammal-Bearing Tertiary of South America. Palaeovertebrata, ME, 1-93. Marshall L.G., Berta A., Hoffstetter R., Pascual R., Reig O.A., Bombin M., Mones A. (1984) - Mammals and Stratigraphy: Geochronology of the Continental Mammal-Bearing Quaternary of South America. Palaeovertebrata, ME, 1-76. Mihlbachler M.C., Rivals F., Solounias N., Semperbon G.M. (2011) - Dietary change and evolution of horses in North America. Science, 331, 1178- 1181. Moreno F.P. (1891) - Onohippidium Munizi. Breve Historia sobre los restos fósiles de un género nuevo de la familia de los Equidae conservados en el Museo de La Plata. Revista del Museo de la Plata, 2, 65-71. Moreno Bofarull A., Arias Royo A., Hernández Fernández M., Ortiz-Jaureguizar E., Morales J. (2008) - Influence of continental history on the ecological specialization and macroevolutionary processes in the mammalian assemblage of South America: differences between small and large mammals. BMC Evolutionary Biology, 8 DOI:10.1186/1471-2148-8-97 Morrone J.J. (2014) – Biogeographical regionalisation of the Neotropical region. Zootaxa, 3782(1), 1-110. Orlando L., Male D., Alberdi M.T., Prado J.L., Prieto A., Cooper A., Hänni C. (2008) - Ancient DNA clarifies the Evolutionary History of American Late Pleisto- cene Equids. Journal Molecular Evolution, 66, 533- 538. Orlando L., Metcal J.L., Alberdi M.T., Telles-Antunes M., Bonjean D., Otte M., Martin F., Eisenmann V., Mashkour M., Morello F., Prado J.L., Salas-Gismondi R., Shockeym B.J., Wrinn P.J., Vasil’ev S.K., Ovodov N.D., Cherry M.I., Hopwood B., Male D., Austin J.J., Hänni C., Cooper A. (2009) - Revising the recent evolutionary history of equids using ancient DNA. Proceeding of the Na- tional Academy of Sciences USA, 106, 21754- 21759. Ortiz Jaureguizar E., Cladera G. (2006) - Paleoenviron­ mental evolution of southern South America during 54 Alberdi M.T. & Prado J.L. the Cenozoic. Journal of Arid Environment, 66, 489-532. Owen R. (1840) - The Zoology of the voyage of H.M.S. Beagle under the Command of Captain Fitzroy R.N. during the years 1832 to 1836. Part I.- Fossil Mammalia, Ed Superv C. Darwin, pp. 81-111. Owen R. (1869) - On Fossil Teeth of Equines from Cen- tral and South America, Referable to Equus con- versidens, Equus tau, and Equus arcidens. Proceeding of the Royal Society of London, 17, 267-268. Pascual R., Ortega Hinojosa E.J., Gondar D., Tonni E.P. (1965) - Las Edades del Cenozoico mamalífero de la Argentina, con especial atención a aquellas del territorio bonaerense. Anuario Comisión de Investigación Científica, Provincia de Buenos Aires, 6, 165-193. Pascual R., Ortega Hinojosa E.J., Gondar D., Tonni E.P. (1966) - Las edades del Cenozoico mamalífero de la provincia de Buenos Aires. In: Borrello A.V. (Ed.): Paleontología Bonaerense, Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, 3-12. Pascual R., Ortiz Jaureguizar E., Prado J.L. (1996) - Land Mammals: Paradigm of Cenozoic South American Geobiotic Evolution. Münchner Geowis- senschaftlich Abhandlungen, Geologie Paläontolo- gie, A30, 265-319. Prado J.L. (1984) - Fenética de los metatarsianos de taxa fósiles Hippidion Owen, Onohippidium More- no, Parahipparion C. Ameghino y Equus (Amerhippus) Linne (Mammalia, Perissodactyla). CIPFE Orione Contribución Biología, Montevideo, 11, 11-15. Prado J.L., Alberdi M.T. (1994) - A Quantitative Review of the horse Equus from South America. Paleon- tology, 37, 459-481. Prado J.L., Alberdi M.T. (1996) - A Cladistic Analysis of the Horses of the Tribe Equini. Palaeontology, 39, 663-680. Prado J.L., Alberdi M.T. (2008) - Restos de Hippidion y Equus (Amerhippus) procedentes de las Barrancas de San Lorenzo, Pleistoceno tardío (Provincia de Santa Fé, Argentina). Revista Española de Paleontología, 23(2), 225-236. Prado J.L., Alberdi M.T. (2012) - Equidos y gonfoterios del Pleistoceno tardío de San Pedro, provincia de Buenos Aires, Argentina. Estudios Geológicos, 68 (2), 261-276. Prado J.L., Alberdi M.T. (2014) - Global evolution of Equidae and Gomphotheriidae from South Ameri- ca. Integrative Zoology, 9, 434-443. Prado J.L., Alberdi M.T. (2016) - Fossil Horses from Argentina. In: Agnolin F.L., Lio G.L., Brissón Egli F., Chimento N., Novas F.E. (Eds.): Historia Evolutiva y Paleobiogeográfica de los Vertebrados de América del Sur, Contribuciones Científicas del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, 6, 303-309. Prado J.L., Alberdi M.T. (2017) - Fossil Horses of South America. Phylogeny, Systematics and Ecology. The Latin American Studies Book Series, Spring- er, pp. 150. Prado J.L., Alberdi M.T., Reguero M.A. (1998) - El Registro más antiguo de Hippidion Owen, 1869 (Mammalia, Perissodactyla) en América del Sur. Estudios Geológicos, 54, 85-91. Prado J.L., Alberdi M.T., Reguero M.A. (2000) - Comentarios sobre la Geocronología, Estratigrafía y Paleontología de Vertebrados de la Fm. Uquía en el perfil de Esquina Blanca, Jujuy. Respuesta a E.P. Tonni y A.L. Cione. Estudios Geológicos, 56, 133-137. Prado J.L., Sánchez B., Alberdi M.T. (2011) - Ancient Feeding Ecology Inferred From Stable Isotopic Evi ­dence From Fossil Horses In South America Over The Past 3 Ma. BMC Ecology, 11, 1-15. Prado J.L., Alberdi M.T., Di Martino V.J. (2012) - Équidos y Gonfoterios del Pleistoceno tardío del Sudeste de la Provincia de Buenos Aires. Ameghiniana, 49(4), 623-641. Prado J.L., Martínez-Maza C., Alberdi M.T. (2015) - Megafauna extinction in South America: A new chronology for the Argentine Pampas. Palaeoge- ography, Palaeoclimatology, Palaeoecology, 425, 41-49. Pérez-Crespo A.V., Prado J.L., Alberdi M.T., Arroyo- Cabrales J., Johnson E. (2016) - Diet and habitat for six American Pleistocene proboscidean species using carbon and oxygen stable isotopes. Ameghiniana, 71, 39-51. Pérez-Crespo A.V., Prado J.L., Alberdi M.T., Arroyo- Cabrales J. (2018) - Stable isotopes and diets of Pleistocene horses from southern North America and South America: similarities and differences. Palaeobiodiversity and Palaeoenvironments, in press. Reguero M.A., Candela A.M. (2011) - Late Cenozoic mammals from the northwest of Argentina. In: Salfity R., Marquillas M.R. (Eds.): Cenozoic geolo- gy of the Central Andes of Argentina, SCS Pub- lishers, Salta, pp. 411-426. Reguero M.A., Candela A.M., Alonso R.N. (2007) - Bio- chronology and biostratigraphy of the Uquía For- mation (Pliocene-early Pleistocene, NW Argentina) and its significance in the Great American Biotic Interchange. Journal of South American Earth Science, 23, 1-16. Saarinen J., Eronen J., Fortelius M., Seppä H., Lister A.M. (2016) - Patterns of diet and body mass of large ungulates from the Pleistocene of Western Europe, and their relation to vegetation. Palaeon- tologia Electronica, 19(3), 1-58. Sánchez B., Prado J.L., Alberdi M.T. (2004) - Feeding Ecology, Dispersal, and Extinction of South Ameri- can Pleistocene Gomphotheres (Gomphotheriidae, Proboscidea). Paleobiology, 30(1), 146-161. Savage D.E. (1962) - Cenozoic Geochronology of the Fossil Mammals of the Western Hemisphere. Re- vista Museo Argentino Ciencias Naturales "Bernardino Rivadavia", Ciencias Zoológicas, 8, 53‑67. Schubert M., Jónsson H., Chang D., Der Sarkissian C., Ermini L., Ginolhac A., Albrechtsen A., Dupanloup 55 Fossil horses from South America I., Foucal A., Petersen B., Fumagalli M., Raghavan M., Seguin-Orlando A., Korneliussen T.S., Velazquez A.M.V., Stenderup J., Hoover C.A., Rubin C.J., Alfarhan A.H., Alquraishi S.A., Al-Rasheid K.A.S., MacHugh D.E., Kalbfleisch T., MacLeod J.N., Rubin E.M., Sicheritz-Ponten T., Andersson L., Hofreiter, Marques-Bonet T., Gilbert M.T.P., Nielsen R., Excoffier L., Willerslev E., Shapiro B., Orlando L. (2014) - Prehistoric ge- nomes reveal the genetic foundation and cost of horse domestication. Proceedings of the National Academy of Science USA, 111, E5661-E5669. Sharov A.A. (2014) - Evolutionary constraints or oppor- tunities? Biosystems, 123, 9-18. Shoemaker L., Clauset A. (2014) - Body mass evolution and diversification within horses (family Equidae). Ecological letters, 17(2), 211-220. Simpson G.G. (1951) - History of the Fauna of Latin America. American Science, 38 261-389. Simpson G.G. (1953) - Horses. The Story of the Horse Family in the Modern World and through sixty million years of History. New York. Oxford Univer- sity Press, pp. 247. Simpson G.G. (1971) - The evolution of marsupials in South America. Annales Academia Brasileira de Ciências, 43, 103-118. Strömberg C.A.E. (2004) - Using phytolith assemblages to reconstruct the origin and spread of grass- dominated habitats in the Great Plains during the late Eocene to early Miocene. Palaeogeography, Palaeoclimatology Palaeoecology, 207(3-4), 239- 275. Tauber A.A. (2005) - Mamíferos fósiles y edad de la Formación Salicas (Mioceno Tardío) de la sierra de Velasco, La Rioja, Argentina. Ameghiniana, 42 (2), 443-460. Toledo M.J., Schewnninger J-L., Kinoshita A., Baffa O., Mangini A. (2014) - Dataciones OSL, ESR y U-Th del sitio Paleontológico Spósito (San Pedro, Prov. de Buenos Aires, Argentina). Registro de los OIS6/7 y OIS5. XIX Congreso Geológico Argentino, Junio 2014, Córdoba, S13-6. Toledo M.J., Schewenninger J., Kinoshita A., Baffa O., Mangiri A. (2015) - Is Equus (A.) neogeus a valid index and exclusive taxon of the Lujanian Stage? Sequence Stratigraphy and New OSL, ESR and U -Th dates of OIS 7 to OIS 2, San Pedro, Buenos Aires Province, Argentina. XXIX Jornadas Argentinas de Paleontología de Vertebrados, 1-2. Tonni E.P., Carlini A.A., Scillato-Yané G.J., Figini A.J. (2003) - Cronología radiocarbónica y condiciones climáticas en la “Cueva del Milodón” (sur de Chile) durante el Pleistoceno tardío. Ameghiniana, 40(4), 609-615. Tonni E.P., Soibelzon E., Cione A.L., Carlini A.A., Scillato-Yané G.J., Zurita A.E., Paredes Ríos F. (2009) - Preliminar correlation of the Pleistocene sequences of the Tarija valley (Bolivia) with the Pampean chronological standard. Quaternary In- ternational, 210, 57-65. Vilstrup J.T., Seguin-Orlando A., Stiller M., Ginolhac A., Raghavan M., Nielsen S.C.A.,Weinstock J., Froese D., Vasiliev S.K., Ovodov N.D., Clary J., Helgen K.M., Fleischer R.C., Cooper A., Shapiro B., Orlando L. (2013) - Mitochondrial Phylo- genomics of Modern and Ancient Equids. PLoSONE, 8(2), e55950. Doi: 10.1371/journal.pone.0055950 Villavicencio N.A., Lindsey E.L., Martin F.M., Borrero L.A., Moreno P.I., Marshall C.R,, Barnosky A.D. (2016) - Combination of humans, climate, and vegetation change triggered Late Quaternary meg- afauna extinction in the Última Esperanza region, southern Patagonia, Chile. Ecography, 39(2), 125- 140. Vrba E.S. (1992) - Mammals as key to evolutionary the- ory. Journal of Mammalogy, 73, 1-28. Wagner A. (1860) - Ueber fossile Säugetierknochen am Chimborasso. Sitzugsbenchte der Konigl bayenschen. Akademie der Wissenschapten z München, 330-338. Webb S.D. (1991) - Ecogeography and the Great Ameri- can Interchange. Paleobiology, 17, 266-280. Weinstock J., Willersley E., Sher A., Tong W., Ho S.Y.W., Simon Y.W. Ho1, Rubenstein D., Storer J., Burns J., Martin L., Bravi C., Prieto A., Froese D., Scott E., Xulong L., Cooper A. (2005) - New World Pleistocene Horses: Pruning the Equid Tree. PLoSBiol, 3(8), 1332-1333. Wood H.E., Chaney R.W., Clark J., Colbert E.H., Jepsen G.L., Reeside J.B., Stock C. (1941) - Nomencla- ture and correlation of the North American conti- nental Tertiary. Geological Society of American Bulletin, 52(1), 1-48. Woodburne M.O. (2010) - The Great American Biotic Interchange: Dispersals, Tectonics, Climate, Sea Level and Holding Pens. Journal of Mammalia Evolution, 17, 245-264. Ms. received: June 13, 2018 Final text received: February 14, 2019 56 Alberdi M.T. & Prado J.L.