Review of Feeding Ecology Data of Late Pleistocene Mammalian Herbivores from South America and Discussions on Niche Differentiation

Home , Eremotherium, Macraucheniidae, Neosclerocalyptus, Scelidodon, Scelidotherium, Toxodon

Earth-Science Reviews 140 (2015) 158–165

Contents lists available at ScienceDirect

Earth-Science Reviews

journal homepage: www.elsevier.com/locate/earscirev

Review of feeding ecology data of Late Pleistocene mammalian herbivores from South America and discussions on niche differentiation

Lucas de Melo França a,⁎, Lidiane de Asevedo b, Mário André Trindade Dantas c, Adriana Bocchiglieri a, Leonardo dos Santos Avilla b, Renato Pereira Lopes d, Jorge Luíz Lopes da Silva e a Programa de Pós-graduação em Ecologia e Conservação, Universidade Federal de Sergipe, São Cristovão, SE, Brazil b Laboratório de Mastozoologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil c Instituto Multidisciplinar em Saúde, Universidade Federal da Bahia — Campus Anísio Teixeira, Vitória da Conquista, BA, Brazil d Universidade Federal do Rio Grande do Sul (UFRGS) — Programa de Pós-graduação em Geociências, Avenida Bento Gonçalves, 9500, Agronomia, CEP 91540-000, Porto Alegre, RS, Brazil e Setor de Biodiversidade e Ecologia, Instituto de Ciências Biológicas e da Saúde, Setor de Geologia e Paleontologia, Museu de História Natural da Universidade Federal de Alagoas, Maceió, AL, Brazil article info abstract

Article history: The present contribution provides a review of the feeding paleoecology studies based on carbon isotopic data Received 7 September 2013 available for 13 extinct megamammals that existed in South America during the Late Pleistocene. These ancient Accepted 19 October 2014 feed ecology data were grouped into four geographic ecoregions, supplying the basis for an analysis of the inter- Available online 27 October 2014 speciﬁc interactions within a mammal assembly, based on the classiﬁcation of taxa in three trophic guilds — grazers, browsers, and mixed-feeders. Keywords: Megafauna © 2014 Elsevier B.V. All rights reserved. South America Carbon isotopes Feeding ecology Niche differentiation

Contents

1. Introduction...... 158 2. Materialsandmethods...... 159 3. Resultsanddiscussion...... 160 3.1. Ecoregion 1 — EcuadorandPeru...... 161 3.2. Ecoregion 2 — Amazonbasin...... 161 3.3. Ecoregion 3 — BrazilianIntertropicalRegion...... 161 3.4. Ecoregion 4 — southernBrazil,UruguayandnorthernArgentina...... 163 3.5. Paleocommunitiesandnichedifferentiation...... 163 4. Finalremarks...... 164 AppendixA. Supplementarydata...... 164 References...... 164

1. Introduction valuable evidence on speciﬁc paleoenvironmental and paleoclimatic aspects of the habitats occupied by these species (e.g. MacFadden Over the past few decades, several paleoecological studies of the et al., 1994, 1999; Sánchez et al., 2004; Asevedo et al., 2012; Marcolino herbivorous mammals from the South American Pleistocene have pro- et al., 2012; Dantas et al., 2013a). duced important insights about dietary adaptations. In addition to the Traditionally, paleodietary studies have been based primarily on characterization of feeding patterns, the results of these studies provide ecomorphological analyses, which evaluate potential analogies and homologies in the cranial, dental, and mandibulary structural charac- ⁎ Corresponding author. Tel.: +55 (0xx79)2105 6697. teristics of the extinct taxa with those of modern species (MacFadden E-mail address: [email protected] (L.M. França). and Shockey, 1997). However, some innovative techniques have been

http://dx.doi.org/10.1016/j.earscirev.2014.10.006 0012-8252/© 2014 Elsevier B.V. All rights reserved. L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165 159 developed and employed in the interpretation of South American fossil et al., 1999; Sánchez et al., 2003; Sánchez et al., 2004), while δ13C values mammals, including analyses of isotopic composition from mineralized higher than −1‰ are consistent with a diet based on C4 plants. Inter- tissues, microwear patterns of tooth enamel, microfossils from teeth mediate δ13C values (between −10‰ and −1‰) indicate a mixed calculi and coprolites (e.g. MacFadden et al., 1994; Sánchez et al., diet of C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005). 2004; Asevedo et al., 2012; Marcolino et al., 2012). This study has two main objectives: (i) to review the data available In the literature, the great contribution of isotopic studies to feeding on the feeding paleoecology of 13 herbivorous megamammals from pattern reconstructions is remarkable. This geochemical approach the Late Pleistocene of South America, and (ii) to evaluate possible also permits the identification of environmental variables, such as paleodietary patterns related to the geographic distribution of the taxa temperature and humidity, as well as the type of vegetation found in analyzed and identify potential interspecific interactions among the the environment (Kohn and Law, 2006; Tapia and Adriano-Morán, taxa, assigning them to ecological guilds based on three major feeding 2012; Lopes et al., 2013). Thus, some isotopic paleodiet studies in categories (grazers, browsers, and mixed-feeders). South America (e.g. MacFadden et al., 1999; Sánchez et al., 2004; Dantas et al., 2013a; Lopes et al., 2013) have permitted inferences about the dynamics of plant communities in Late Pleistocene, through 2. Materials and methods the diet information of the herbivorous megamammal specimens from a range of different latitudes represented by Quaternary fossilifer- The present review analyzed data obtained from 15 published feed- ous sites. ing paleoecology studies of 13 South American megamammal taxa The plant carbon isotope profiles (δ13C) depends primarily on the that became extinct during the Late Pleistocene (Supplementary photosynthetic pathway (Koch, 2007). Most existing plants, ranging [Tables S1–S3]). Most of the articles reviewed used isotopic carbon from trees and woody shrubs to grasses found on prairies and steppes analysis (δ13C) performed in hydroxyapatite (Table S1) and collagen at high altitudes or latitudes, are dependent on the Calvin–Benson (Table S2) in enamel, dentine or bone. The articles that used other 13 (C3) photosynthetic cycle. These plants present δ CVPDB values of analyses (Table S3) were compiled here for comparison. The taxa −22‰ to −30‰, with a medium value of around −27‰. By contrast, evaluated include: Proboscidea (Gomphotheriidae: Notiomastodon), the few terrestrial plants that use the Hatch–Slack (C4) photosynthetic Perissodactyla (Equidae: Equus and Hippidion), Artiodactyla (Camelidae: route are primarily tropical and subtropical grasses. These species are Palaeolama), Notoungulata (Toxodontidae: Toxodon), Liptoterna typically found in open areas in warm regions subject to hydrological (Macrauchenidae: Macrauchenia), Pilosa (Megatheriidae: Eremotherium; stress, and are able to tolerate low concentrations of CO2. In general, Mylodontidae: Scelidotherium, Scelidodon,andValgipes), and Cingulata 13 C4 plants have δ CVPDB values of −10‰ to −14%, averaging −12‰. (Glyptodontidae: Sclerocalyptus, Glyptodon and Neosclerocalyptus). Plants that photosynthesize using Crassulacean Acid Metabolism We follow the most current taxonomic arrangements proposed (CAM), such as succulents, present intermediate δ13Cvalues(Ehleringer for the Gomphotheriidae taxa of South America. Thus the paleoecologi- et al., 1991; Cerling, 1992; Quade et al., 1992; Ehleringer et al., 1997; cal data presented by Sánchez et al. (2004), Alberdi et al. (2008), and MacFadden and Shockey, 1997; MacFadden et al., 1999; Sánchez et al., Lopes et al. (2013) for Stegomastodon platensis (Ameghino, 1888), 2004; MacFadden, 2005; Domingo et al., 2012). Stegomastodon waringi (Holland, 1920), and Stegomastodon sp., respec- The diet of extinct mammals can be determined through δ13C analy- tively will be attributed to Notiomastodon platensis postulate by Mothé sis from collagen and hydroxyapatite found in enamel, dentine or bone et al. (2012). (Fricke, 2007; Bocherens and Drucker, 2013). A few decades ago the For monospecific taxa in our analysis – e.g. Eremotherium main source of this information was the enamel, because this tissue is (Eremotherium laurillardi, Cartelle and De Iuliis, 1995), Notiomastodon less porous and, consequently, less susceptible to contamination by (N. platensis, Mothé et al., 2012) – only genus-level taxa are considered. secondary carbonate, therefore this has contributed a large number of This position is reinforced by the fact that some of the studies consulted studies that used this component (e.g. MacFadden et al., 1999,and consider only genera, e.g. Equus (MacFadden et al., 1999); Toxodon references there in). However, the use of hydroxyapatite extracted (MacFadden, 2005; Lopes et al., 2013); Stegomastodon (=Notiomastodon from fossil bone and dentine is extremely useful after specifictreat- sensu Mothé et al., 2012)(Lopes et al., 2013). ments to remove the secondary carbonates. In the articles reviewed the used δ13C analysis from hydroxyapatite The interpreted values of δ13C in the different tissues represent and collagen in bone or dentine (e.g. MacFadden et al., 1999; Drefahl, fractionated values of the plant ingested. Studies of modern medium- 2010; Dantas et al., 2013a; França et al., 2014) were chemically to large-bodied herbivorous mammals have recorded fractionation pretreated to eliminate the potential effects of diagenesis (secondary values of δ13C range of 14.1 ± 0.5‰ between diet and tissue (Cerling carbonate contamination), using the protocol described elsewhere. and Harris, 1999). Differences in diet-to-enamel δ13C fractionation These, can be compared and analyzed together with other enamel in mammals of different sizes (voles, rabbits, pigs and cattle) exposed analyses. to the same feed items were observed by Passey et al. (2005). These Although Dantas et al. (2013a) and Drefahl (2010) did not mention 13 animals have differences in digestive physiology, including differences pretreatment of the samples in their texts, all analyses (δ CinCO3 in methane production, which according to the authors, is the major hydroxyapatite and collagen; AMS dating) were done with chemically determinant of enrichment of bioapatite-diet for an individual or spe- pretreated samples (Dantas and Drefahl, personal communication). cies. For this reason, independent of the body mass of animals, our All δ13C data recovered were plotted on maps of vegetation recon- study only focuses on analysis of ruminants and monogastric South structed for South America during the Last Glacial Maximum — LGM American herbivore megamammals, which potentially had the greatest (Pennington et al., 2000; Vivo & Carmignotto, 2004; Anhuf et al., similarities in digestive physiology and methane production. 2006; Mayle, 2006; Fig. 1). We observed that the data are grouped According to Domingo et al. (2012), the δ13Cvaluesexpectedfor into four ecoregions, mainly composed of Dry Forest vegetation, exclusively C3 mammal consumers in different habitats are: −22‰ to Savanna and grasslands (Fig. 1) in: (1) Ecuador and Peru; (2) Amazon −16‰ (closed canopy forests); −16‰ to −11‰ (mesic habitats or basin; (3) northeastern Brazil, the Brazilian Intertropical Region (sensu woodland); and −11‰ to −8‰ (wooded C3 grassland to open arid Cartelle, 1999); and (4) a wide region, including southern Brazil, C3 grassland). These values are valid for regions at high latitudes (35– Uruguay and northern Argentina. 40°) and high altitudes (N3000 m), no C3 grasses are found in the tropics Geographic patterns and paleobotanical information for each area at low altitudes. In this case, δ13C values lower than −10‰ should be were used to corroborate the type of the habitat inferred by the carbon interpreted as the product of an exclusive C3 diet in closed habitats, isotope data for these mammals, aiming to provide a more systematic i.e., trees and shrubs, which is typical of browsers (e.g. MacFadden evaluation of ecological patterns. 160 L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165

Fig. 1. Map of the estimate distribution of vegetation in Late Pleistocene showing the four ecoregions of South America recognized in the present study based on an overview of the available data on the paleodiets of herbivorous Pleistocenic megammals. Legends: CA = Caatinga nucleus; MI = misiones nucleus; CH = Chiquitano dry forest nucleus; PI = piedmont nucleus; BP = Bolivian and Peruvian inter-Andean valleys; PE = Paciﬁc coastal Ecuador. Map composition based on maps provided by Vivo & Carmignotto, 2004; Mayle, 2006; Amhuf et al., 2006.

One problem that may hamper reliable inferences on the feeding 3. Results and discussion paleoecology of extinct taxa is the lack of absolute dating or stratigraphic controls for most of the South American Quaternary fossil deposits. While paleoecological characteristics are commonly attributed This problem is particularly serious in the case of the cave and tank to extinct taxa based on the type of dentition (hypsodont, bunodont, deposits from the Brazilian Intertropical Region, which may contain etc.), and in the tooth and oral morphology, it is important to recognize fossil assemblages with a high degree of time-averaging. More robust the potential for the modification of feeding habits, especially in chronological or stratigraphic controls would be necessary in these opportunistic species faced with major alterations of their habitats cases for a reliable interpretation of the effects of Quaternary climate (e.g. Sánchez et al., 2004; Asevedo et al., 2012). fluctuations on the diet composition and behavior of each taxa. The map shows that some sites were located relatively close to one Although the absence of dated samples is a complicating factor in the another, suggesting that they represent the same ecoregion, leading to reconstruction of paleoenvironments, we will try to do this reconstruc- the definition of groups of samples within the South American conti- tion treating the information without an absolute age for the specimens, nent. When the data were analyzed within each group, similar diets as belonging to Late Pleistocene. could be diagnosed for the different specimens of the same taxon, L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165 161 indicating that they were subject to the same local conditions and (11–14°S, Fig. 1; MacFadden, 2005). The δ13C data from hydroxyapa- habitat types. Meanwhile, those specimens with different diets could tite are available for Notiomastodon (δ13C=− 9.2‰)andToxodon indicate the existence of distinct types of plant resources, reflecting (δ13C=−15.4‰ to −10.7‰; Table S1, Fig. 2). In this region, based the presence of other types of habitats. on the interpretation of the authors, the analyses of both tissues

The present overview of the data available on the feeding paleoecol- indicate that these two taxa fed primarily or exclusively C3 on plant ogy of the herbivorous megamammals from a number of different sites resources (MacFadden et al., 2005; Domingo et al., 2012), which in South America also permitted the analysis of potential competition or would be consistent with the predominance of closed forests with resource partitioning, which would have been reflected in the observed a continuous canopy. variations in the composition of the diet. In some cases, it is even possi- Comparing the meaning of these isotopic values with palynological ble to identify certain modifications in feeding patterns related to vari- data, some works indicate that climatic oscillations during the Late ations in the habitat and the presence of potential competitors. Pleistocene could have modified considerably the composition of local vegetation. Pennington et al. (2000) proposed that dry forests substitut- 3.1. Ecoregion 1 — Ecuador and Peru ed for the typical Amazonian rainforest in some regions during periods of colder and drier climate. However, Mayle (2006) has argued that the Carbon isotope data (Table S1) are available for only two taxa – differentiation of humid and dry forests based solely on the available Equus (MacFadden et al., 1999)andNotiomastodon (Sánchez et al., fossil palynomorphs may be unreliable. Either way, the vast majority 2004) – from the coastal regions of Ecuador and Peru (2–3°S, Figs. 1 of the Amazon region was covered with continuous, closed forest and 2). Data are also available on Cuvieronius (Sánchez et al., 2004), al- during the Last Glacial Maximum, even if the exact type of forest cover though as they are derived from specimens obtained from an altitude of is unclear. 2778 m, they were not considered to be typical of the region. Anhuf et al. (2006) nevertheless concluded that the characteristics of The data indicate that the two taxa occupied distinct niches, with the forest were different from those observed in the present day, having 13 Equus (δ C=−0.80‰ to 2.10‰) grazing exclusively on C4 grasses suffered changes in their composition and distribution during the last (MacFadden et al., 1999) and Notiomastodon (δ13C=−5.97‰ to glaciation. In particular, a corridor of dry forest would have formed dur-

−0.78‰; Table S1) exploiting a mixed diet of C3 plants and C4 grasses, ing the LGM, with the rainforest remaining intact only in the western, with predominance of the latter (Sánchez et al., 2004). These results indi- central, and southwestern sectors of the region. cate that the taxa occupied areas of open habitat characterized by the Based on this scenario, the taxa found in this region probably would presence of both herbaceous and shrubby vegetation, habitats and have been located within the dry corridor, where they would have climate probably similar to those of the present day. The savannas and inhabited areas of dry forest with a closed canopy, as suggested by dry forests that stretch along the coasts of the two countries (Aguirre Dantas et al. (2013b) for Notiomastodon. The diversity of C3 plants in et al., 2006; Marcelo-Peña et al., 2007; Espinosa et al., 2012) can be clas- this type of forest may have underpinned niche differentiation in this siﬁed as Seasonally Dry Tropical Forest, or SDTF (Pennington et al., 2000; environment. In Peru, the diet of Notiomastodon, analyzed by Domingo 13 Mayle, 2006). Thus, the feeding ecology data, based on the isotopic ratios, et al. (2012), may also have included C4 plants (δ C=−9.2‰; indicate that the two taxa occupied distinct niches within the region, with Table S1, Fig. 2), which may have favored niche partitioning in this Equus in the grazing guild, and Notiomastodon classiﬁed as a mixed- region. Overall, then, the taxa in this region were members of the feeder (but with the major part of the diet composed of C4 plants). browser guild.

3.2. Ecoregion 2 — Amazon basin 3.3. Ecoregion 3 — Brazilian Intertropical Region

In our analysis the Amazon basin includes data from Peru (8–12°S, Dantas et al. (2013a) discuss δ13CdataforNotiomastodon, Fig. 1; MacFadden, 2005; Domingo et al., 2012) and northern Bolivia Eremotherium and Toxodon for this region. Based on these data they

Fig. 2. Carbon isotope (δ13C ‰) values for the mammalian taxa analyzed in the present study. 162 L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165 propose a subdivision of this region into three: subregion A (between At 9°S, in subregion B (Table S1), there are data from the BIR only latitudes 9°S and 14°S), B (latitude 9°S), C (latitude 6°S). for the taxa Notiomastodon (δ13C=−1.86‰ to 1.47‰), Toxodon Data are available for three taxa from the northern portion of (δ13C=−4.10‰ to 1.51‰), and Eremotherium (δ13C=−6.65% to the Brazilian Intertropical Region (BIR, sensu Cartelle, 1999;Subregion 0.30‰; Fig. 2). The available data (Viana et al., 2011; Dantas et al., C, latitude 6°S, Fig. 1, Table S1) — Eremotherium (δ13C°=°0.50‰ 2013a) indicate that Notiomastodon was a grazer, while Eremotherium 13 13 and 5.22‰), Notiomastodon (δ C°=°0.44‰), and Toxodon (δ C= and Toxodon had a mixed diet of C3 and C4 plants in this region, accord- −1.32‰; Fig. 2). These values indicate a diet based exclusively on C4 ing to Dantas et al. (2013a). grasses, that is, that all three taxa were grazers (Dantas et al., 2013a). The BIR was a diverse ecoregion, probably characterized by the pres- Pereira et al. (2013) presented δ13C data for another taxon that ence of different types of Caatinga habitats, including more humid areas inhabited the region, the ground sloth Valgipes. These animals fed exclu- with relatively dense vegetation and other, more arid habitats, with 13 sively on C3 plants (δ C=−10.17‰, Table 1), probably consuming leaf more open vegetation composed of smaller plants (Pennington et al., shoots, roots, and fruit, with a diet similar to that of a second 2000; Mayle, 2006). Dantas et al. (2013a) observed a dietary gradient

Scelidotheriine, Scelidotherium (Bargo, 2001 apud Bargo et al., 2006a). within the BIR, shifting from grazing on C4 plants in the northern Based on models of potential distribution, Werneck et al. (2011) extreme (Rio Grande do Norte) to feeding exclusively on C3 plants in suggested that at 21 Ka the vegetation of this region would have been the south, between 9°S and 14°S. This reflects the differences in the similar to that of the present-day Caatinga, a conclusion supported vegetation within different areas, which in turn, influenced the diet of by the feeding ecology data. The palynological data presented by the herbivorous mammals that inhabited them. Behling et al. (2000) indicate the presence in the region of plant families Despite these overall differences in habitats within the BIR, the same typical of semi-arid environments, such as the Poaceae, Cyperaceae, type of dry forest (Caatinga) would have been found between 6°S and Asteraceae, Palmae, Myrtaceae, Melastomataceae, and Combretaceae – 10°S, according to the vegetation maps provided by Pennington et al. similar to those predominant today – between 42 Ka and 8.5 Ka, (2000) and Mayle (2006). Even so, the shift in the isotopic profile indi- interrupted only by relatively short periods of more humid climate. cates that, while 6°S was dominated by relatively arid habitats, the Seasonally dry tropical forests, such as the Caatinga, may encompass vegetation was more mixed between 9°S and 10°S, being more open a wide range of habitat types (Pennington et al., 2000), including tracts in some parts, but denser in others. These differences were not marked of denser vegetation in more humid locations, but also more open areas enough, however, to constitute ecological barriers to migration of local dominated by cacti and small shrubs. Given this, the principal habitat mammals within the region. in this region may have been more open, with a predominance of herba- For the southernmost BIR (9–14°S, subregion A) data are available ceous plants. on the diets of five different taxa – Eremotherium, Notiomastodon,

While most C4 plants are grasses belonging to the family Poaceae, a Toxodon, Paleolama,andEquus (Fig. 2) – derived from three distinct number of genera belong to other families, such as the Cyperaceae, analytical approaches, and indicate that the vegetation in this area Asteraceae, and Amaranthaceae (Sage, 2004), which are also common was a little bit different from that in the north of the BIR discussed in the Caatinga. Based on the isotopic proﬁle obtained for the mamma- above. MacFadden et al. (1999) present data on Equus (δ13C= lian taxa from the BIR, it seems likely that C4 plants were more widely −1.40‰ to 3.7‰; Table S1) and conﬁrmed a diet of C4 grasses for distributed during this period due to the wider areas of open habitat, the taxon in this region. Analyzing new δ13C data together with compared with the actual Caatinga. those from previous studies (Sánchez et al., 2004; MacFadden, 2005;

Table 1 Resume of the weight and variation on δ13C(‰) values through South America.

Taxa Estimate Variation on δ13C(‰) values weight (kg) Region 1 Region 2 Region 3 Region 4

Order Pilosa Family Megatheriidae Eremotherium 4000a –– −6.65 to 5.22 (H)/−18.20 (C) – Family Mylodontidae Scelidotherium 500b –– – −6.00 (H) Scelidodon 500a –– – −8.70 (H) Order Cingulata Family Glyptodontidae Sclerocalyptus 600a –– – −10.50 (H) Neosclerocalyptus 600a –– – −5.30 (H) Glyptodon 2000b –– – −8.80 (H) Order Notoungulata Family Toxodontidae Toxodon 1100b – −15.40 to −11.00 (H) −13.24 to −1.00 (H) −12.20 to −1.50 (H) Order Perissodactyla Family Equidae Equus 300b −0.80 to 3.00 (H) – −0.60 to 1.70 (H) −11.10 to −0.80 (H) Hippidion 460b –– – −12.10 to −8.10 (H) Order Artiodactyla Family Camelidae Paleolama 300a –– – −8.50 (H) Order Proboscidea Family Gomphotheriidae Notiomastodon 4000b −5.97 to −0.78 (H) −9.20 (H)/−28.50 (C) −8.20 to 0.76 (H) −12.11 to −1.00 (H) Order Liptoterna Family Macraucheniidae Macrauchenia 1000b –– – −9.50 to −5.70 (H)

(H) performed in hydroxyapatite, (C) performed in collagen. a Estimation based in proposition made by related taxa. b Data from Fariña et al. (1998). L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165 163

Drefahl, 2010), Dantas et al. (2013a) concluded that in this region, the mixed diet for these glyptodontids, contradicting the traditional view carbon isotopic ratio values in collagen from Eremotherium (δ13C= based exclusively on morpho-functional parameters (e.g. Farina and −18.20‰; Table S2) and in hydroxyapatite for Toxodon (δ13C= Vizcaíno, 2001). −13.24‰ and −12.60‰) indicates that these animals fed exclusively The isotopic data for Macrauchenia (δ13C=−9.5‰ to −5.7‰; on C3 plants, while the range of carbon isotopic ratio values in hydroxy- Table S1) at high latitudes also indicate a mixed diet. The only data apatite of Toxodon (δ13C=−7.70‰ to −5.50‰) and Notiomastodon available for the camelids are those for Paleolama from latitudes above (δ13C=−8.20‰ to −5.00‰; Table S1) indicates a mixed-feeder 38°S (δ13C=−8.5‰; Table S1), which indicate the consumption of habit, feeding on C3 plants, but with small quantities of C4 plants. C3 plants in open habitats. Asevedo et al. (2012) also confirmed a C3–C4 mixed-feeder diet for In this region, then, the grazer guild was formed by Equus and Toxodon, Notiomastodon (19–21°S) based on the analysis of enamel microwear while the mixed-feeders included all the other taxa — Notiomastodon, and plant microfossils extracted from dental calculi (Table S3). Hippidion, Nothrotheriinae, Scelidodon, Scelidotherium, Neosclerocalyptus, These results indicate the presence of mixed habitats, as confirmed Sclerocalyptus, Glyptodon, Macrauchenia,andPaleolama.Noneofthetaxa by the palynological data. Mayle (2006) discusses the composition of analyzed in this region were exclusively browsers. the vegetation of Minas Gerais during the Late Pleistocence based on the palynological study of Ledru et al. (1996), and concluded that 3.5. Paleocommunities and niche differentiation there was an expansion of the areas of seasonally dry tropical forest (SDTF), within a mosaic of semi-deciduous forests, savanna woodland, Sánchez et al. (2004) and MacFadden (2005) present data on and swamps. However, the exact distribution of the SDTFs remains un- Notiomastodon and Toxodon, respectively, from a range of South clear, given the evidence for the existence of open grassland (savanna) American sites. A number of recent studies, in particular in Argentina at one of the sites analyzed by Ledru et al. (1996). In comparison with (Domingo et al., 2012) and Brazil (Asevedo et al., 2012; Dantas et al., the more northern areas, then, where diets were based primarily or ex- 2013a; Lopes et al., 2013; França et al., 2014), have produced new clusively on C4 plants, the occurrence of Equus (11°S) and the probable data on the feeding habits of these taxa, which confirm that they reduction of areas of open habitat probably combined to contribute to exploited a wide resource base, ranging from browsers to mixed- shifts in the diets of Eremotherium and Toxodon. feeders, depending on the predominant type of vegetation, which is While Eremotherium, Notiomastodon,andToxodon fed primarily on consistent with opportunistic feeding strategies (Table 1). Within

C3 plants in mixed dry forest and savanna habitats, niche partitioning South America, there is an increase in the consumption of C3 plants may have been determined by the considerable diversity of C3 plants with increasing latitude. The only exception to this general pattern in this type of forest (SDTF). Similarly, based on the study of coprolites, was found in the animals that inhabited the closed forests of the inter- 13 Paleolama, appears to have had a diet based on shrubs (C3 plants tropical zone, where more negative values of δ C were recorded. (Marcolino et al., 2012); Table S3), and may also have been sharing re- Isotopic studies are still scarce for the terrestrial sloths and sources with these other species, while Equus represented the grazer glyptodontids, mostly due to the absence of dental enamel in these guild in this region, Notiomastodon and Toxodon were mixed-feeders, animals, which has been the source of the carbon used for most of the and Eremotherium and Paleolama were browsers. δ13C analyses up to now. However, new techniques have been developed that permit the extraction of samples from the tooth cementum 3.4. Ecoregion 4 — southern Brazil, Uruguay and northern Argentina or bone, and the first data for these taxa are now becoming available (Domingo et al., 2012; Dantas et al., 2013a). This region, located between 26°S and 39°S, encompasses southern While Eremotherium was widely distributed in South America, the Brazil, Uruguay and northern-central Argentina (Tables S1–S2, Fig. 1), only δ13C data available for this taxon are from the Brazilian Intertropi- presents the largest set of δ13C data for the taxa Toxodon (MacFadden, cal Region (Viana et al., 2011; Dantas et al., 2013a; França et al., 2014; 2005; Lopes et al., 2013), Equus (MacFadden et al., 1999; Domingo Table 1). These data indicate that Eremotherium was also a mixed- et al., 2012), Hippidion (Prado et al., 2011; Domingo et al., 2012), and feeder on a variety of resources, ranging from C4 grasses to C3 plants Notiomastodon (Sánchez et al., 2004; Alberdi et al., 2008; Domingo (leaves, fruit). This could be visualized in Dantas et al. (2013a),that et al., 2012; Lopes et al., 2013; Fig. 2). Other data are also available for found significant differences in the dietary patterns of the taxa found Glyptodon, Sclerocalyptus, Neosclerocalyptus, Scelidotherium, Scelidodon, in the different subregions (A, B, and C; see Fig. 1 in Dantas et al., Macrauchenia,andPaleolama (Domingo et al., 2012). 2013a) inside the Brazilian Intertropical Region. In future papers, it In this region, the grazer guild is represented by Equus (δ13C= may be possible to extrapolate these findings to other regions of South −11.1‰ to −0.80‰, Table S1) and Toxodon (δ13C=−12.20‰ to America, for the predicted composition of the diet of Eremotherium,as −1.50‰; Table S1). However, between 26°S and 39°S, the diet of well as that of its sister taxon, Megatherium, providing further insights

Equus shifts gradually from a diet based exclusively on C4 plants to a into the ecological adaptations and niche differentiation of these mixture of C3 and C4 grasses (MacFadden et al., 1999; MacFadden, taxa. Data for other terrestrial sloths are scarce, and mostly restricted 2005; Domingo et al., 2012; Table 1). Notiomastodon (δ13C=−14.8‰ to ecoregion 4, i.e., Uruguay and Argentina (Table S1). Bargo et al. to −1.00‰) presented mixed diets including C3 shrubs and C4 grasses, (2006a,b) concluded that Scelidotherium would have been a mixed- while Hippidion (δ13C = -12.20‰ to −8.10‰; Table S1) had an exclu- feeder, for example, as confirmed by its isotopic profile, which also sively C3 diet, which probably also included grasses (Sánchez et al., indicates the same type of diet as that of Scelidodon (Domingo et al., 2004; Alberdi et al., 2008; Domingo et al., 2012). 2012). The diets of the ground sloth Scelidodon (δ13C=−8.7‰)and The glyptodontids are considered to have been grazers occupying 13 Scelidotherium (δ C=−6.0‰; Table S1) at 32°S included both C3 open habitats, although Vizcaíno et al. (2011) proposed that these plants and C4 grasses. In the case of the glyptodontids, Neosclerocalyptus mammals adopted a mixed diet in denser habitats, which has been 13 (δ C=−5.3‰; Table S1) had a mixed diet of C3 plants and C4 grasses confirmed by Domingo et al. (2012) in the case of Sclerocalyptus, at 37°S, whereas the diet of Sclerocalyptus was based exclusively on C3 Neosclerocalyptus,andGlyptodon. plants (δ13C=−10.5‰;TableS1). In previous studies, both MacFadden et al. (1999) and Prado et al The isotopic data available for Glyptodon indicate variations in (2011) identified a predominantly grazing feeding strategy for Equus the diet related to latitude, with its composition shifting from a mixture and a mixed-feeder strategy for Hippidion. In the case of Paleolama, 13 of C3 plants (predominantly) and C4 grasses at 32°S (δ C=−8.8‰), the sum of the evidence also indicates that this taxon was a specialist, 13 to a diet based exclusively on C3 grasses (δ C=−10.0‰; Table S1) feeding primarily on C3 plants, in both South and North America. A in open habitats at 37°S. Domingo et al. (2012) also identified a similar diet has been recorded for Macrauchenia. 164 L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165

Some taxa, in particular Toxodon and Notiomastodon, presented rela- rainforest during the LGM. Palaeogeogr. Palaeoclimatol. Palaeoecol. 239, 510–527. fl http://dx.doi.org/10.1016/j.palaeo.2006.01.017. tively exible feeding strategies, as might be expected according to their Asevedo, L., Winck, G.R., Mothé, D., Avilla, L.S., 2012. Ancient diet of the Pleistocene wide geographic distribution. Other taxa had less diverse feeding habits, gomphothere Notiomastodon platensis (Mammalia, Proboscidea, Gomphotheriidae) which may have contributed to a reduced geographic range. These from lowland mid-latitudes of South America: stereomicrowear and tooth calculus analyses combined. Quat. Int. 255, 42–52. http://dx.doi.org/10.1016/j.quaint.2011.08.037. mammals include Scelidotherium, Neosclerocalyptus,andDoedicurus, Bargo, M.S., 2001. The ground sloth Megatherium americanum: Skull shape, bite forces, which have only been found up to now in deposits in southern Brazil, and diet, Acta Palaeontol. Pol. 46 (2), 173–192. Uruguay, and Argentina. Bargo, M.S., De Iuliis, G., Vizcaíno, S.F., 2006a. Hypsodonty in Pleistocene ground sloths. – Palynological data indicate a northwards migration of up to 750 km Acta Palaeontol. Pol. 51 (1), 53 61. Bargo, M.S., Toledo, N., Vizcaíno, S.F., 2006b. Muzzle of South American Pleistocene of the cold-adapted vegetation which is currently found only in south- ground sloths (Xenarthra, Tardigrada). J. Morphol. 267, 248–263. http://dx.doi.org/ ernmost Brazil (e.g. Ledru et al., 1996; Behling and Lichte, 1997). This 10.1002/jmor.10399. probably had a major effect on the distribution of many mammalian Behling, H., Arz, H.W., Tzold, J.R.P., Wefer, G., 2000. Late Quaternary vegetational and climate dynamics in northeastern Brazil, inferences from marine core GeoB 3104-1. taxa. Oscillations in the composition of the vegetation over a time Quat. Sci. Rev. 19, 981–994. scale of a few hundred to a few thousand years may have imposed Behling, H., Lichte, M., 1997. Evidence of dry and cold climatic conditions at glacial times nutritional stress on the more selective taxa, and even mixed-feeders in tropical southeastern Brazil. Quat. Res. 48, 348–358. Bocherens, H., Drucker, D.G., 2013. Terrestrial teeth and bones. In: Elias, S.A. (Ed.), The may have been unable to cope with the drastic changes occurring over Encyclopedia of Quaternary Science. 1, pp. 304–314. short periods of time. Cartelle, C., 1999. Pleistocene mammals of the Cerrado and Caatinga of Brazil. In: Eisenberg, J.F., Redford, K.H. (Eds.), Mammals of the Neotropics. The University of Chicago Press, pp. 27–46. 4. Final remarks Cartelle, C., De Iuliis, G., 1995. Eremotherium laurillardi: the Panamerican Late Pleistocene Megatherid sloth. J. Vertebr. Paleontol. 15 (4), 830–841. Further analyses of feeding patterns calibrated with reliable absolute Cerling, T.E., 1992. Development of grasslands and savannas in East Africa during the Neogene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 97, 241–247. datings would permit a more systematic interpretation of diets in the Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation between diet and bioapatite context of the paleoclimatic conditions derived from geological and pal- in ungulate mammals and implications for ecological and paleoecological studies. ynological data, and provide important new insights into the dynamics Oecologia 120, 347–363. Dantas, M.A.T., Dutra, R.P., Cherkinsky, A., Fortier, D.C., Kamino, L.H.Y., Cozzuol, M.A., of the plant and animal communities of the late Quaternary of South Ribeiro, A.S., Silva, F.V., 2013a. Paleoecology and radiocarbon dating of the Pleistocene America. megafauna of the Brazilian Intertropical Region. Quat. Res. 79 (2013), 61–65. http:// The analyses of carbon isotopes, coprolites, tooth enamel microwear, dx.doi.org/10.1016/j.yqres.2012.09.006. Dantas, M.A.T., Xavier, M.C.T., França, L.M., Cozzuol, M.A., Ribeiro, A.S., Figueiredo, and dental calculi provide important evidence on the feeding paleoecolo- A.M.G., Kinoshita, A., Baffa, O., 2013b. A review of the time scale and potential gy of extinct mammals. Together with anatomical studies, this evidences geographic distribution of Notiomastodon platensis (Ameghino, 1888) in the a more complete picture of the ecological niches of these animals. late Pleistocene of South America. Quat. Int. 317, 73–79. http://dx.doi.org/10. Of the taxa analyzed, only Notiomastodon, Toxodon,andEremotherium 1016/j.quaint.2013.06.031. Domingo, L., Prado, J.L., Alberdi, M.T., 2012. The effect of paleoecology and paleobiogeography presented a truly opportunistic feeding strategy, varying according to the on stable isotopes of Quaternary mammals from South America. Quat. Sci. Rev. 55 availability of different resources and the degree of competition from (2012), 103–113. http://dx.doi.org/10.1016/j.quascirev.2012.08.017. δ specialist taxa. Drefahl, M., 2010. Implicações paleoambientais preliminares da análise de 13C em osso de paleomastofauna procedente de Quijingue, Bahia. Boletim de Resumos, Simpósio Based on these preliminary conclusions, there is a clear need for Brasileiro de Paleobotânica e Palinologia, Salvador, ALPP, Bahia, p. 239. the collection of a more ample database on the paleodiet of the taxa Ehleringer, J.R., Sage, R.F., Flanagan, L.B., Pearcy, R.W., 1991. Climate change and the evo- analyzed in the present study, in particular the analyses of coprolite, lution of C4 photosynthesis. Tree 6 (3), 95–99. Ehleringer, J.R., Cerling, T.E., Helliker, B.R., 1997. C4 photosynthesis, atmospheric CO2, and microwear, and dental calculus. This should include the analysis of a climate. Oecologia 112, 285–299. much larger number of taxa, with specimens dated reliably, as well as Espinosa, C.I., Cruz, M., Luzuriaga, A.L., Escudero, A., 2012. Bosques tropicales secos de la the sampling of a wider range of sites. región Pacífico Ecuatorial: diversidad, estructura, funcionamiento e implicaciones para la conservación. Ecosistemas 21 (1–2), 167–179. In any paleoecological study of this type, comparisons with the paleo- Farina, R.A., Vizcaíno, S.F., 2001. Carved teeth and strange jaws: how glyptodonts masti- climatic and paleobotanical data available for the region inhabited by the cated. Acta Palaeontol. Pol. 46 (2), 219–234. taxon should also be a priority. This will ensure a more reliable interpre- Fariña, R.A., Vizcaíno, S.F., Bargo, M.S., 1998. Body mass estimations in Lujanian (Late fi Pleistocene-Early Holocene of South America) mammal megafauna. Mastozoología tation not only of the interspeci c interactions within the communities of Neotropical 5, 87–108. South American megamammals, but also the dynamics of these commu- França, L.M., Dantas, M.A.T., Bocchiglieri, A., Cherkinsky, A., Ribeiro, A.S., Bocherens, nities during the Late Pleistocene, and possibly provide new insights into H., 2014. Chronology and ancient feeding ecology of two upper Pleistocene the extinction of these animals during the transition to the Holocene. megamammals from the Brazilian Intertropical Region. Quat. Sci. Rev. 99 (2014), 78–83. Fricke, H., 2007. Stable isotope geochemistry of bonebed fossils: reconstructing Appendix A. Supplementary data paleoenvironments, paleoecology, and paleobiology. In: Rogers, R.R., Eberth, D.A., Fiorillo, A.R. (Eds.), Bonebeds: Genesis, Analysis, and Paleobiological Significance. University of Chicago Press, Chicago and London, pp. 437–490. Supplementary data to this article can be found online at http://dx. Koch, P.L., 2007. Isotopic study of the biology of modern and fossil vertebrates. Stable doi.org/10.1016/j.earscirev.2014.10.006. Isotopes in Ecology and Environmental Science. 2, pp. 99–154. Kohn, M.J., Law, J.M., 2006. Stable isotope chemistry of fossil bone as a new paleoclimate indicator. Geochim. Cosmochim. Acta 70, 931–946. References Ledru, M.-P., Braga, P.I.S., Soubiès, F., Fournier, M., Martin, L., Suguio, K., Turcq, B., 1996. The last 50,000 years in the Neotropics (Southern Brazil): evolution of vegetation Aguirre, Z., Kvist, L.P., Sanchez, O., 2006. Bosques secos en Ecuador y su diversidad. In: and climate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 123, 239–257. Morales, M.R., Øllgaard, B., Kvist, L.P., Borchsenius, F., Balslev, H. (Eds.), Botánica Lopes, R.P., Ribeiro, A.M., Dillenburg, S.R., Schultz, C.L., 2013. Late middle to late Pleisto- Económica de los Andes Centrales. Universidad Mayor de San Andrés, La Paz, cene paleoecology and paleoenvironments in the coastal plain of Rio Grande do Sul Bolivia, pp. 162–187. state, Southern Brazil, from stable isotopes in fossils of Toxodon and Stegomastodon. Alberdi, M.T., Cerdeño, E., Prado, J.L., 2008. Stegomastodon platensis (Proboscidea, Palaeogeogr. Palaeoclimatol. Palaeoecol. 369 (2013), 385–394. http://dx.doi.org/ Gomphotheriidae) en el Pleistoceno de Santiago del Estero, Argentina. Ameghiniana 10.1016/j.palaeo.2012.10.042. 45 (2), 257–271. MacFadden, B.J., 2005. Diet and habitat of toxodont megaherbivores (Mammalia, Amhuf, D., Ledru, M.P., Behling, H., Da Cruz, F.W., Cordeiro, R.C., Van der Hammen, T., Notoungulata) from the late Quaternary of South and Central America. Quat. Res. Karmann, I., Marengo, J.A., De Oliveira, P.E., Pessenda, L., Siffedine, A., Albuquerque, 64 (1), 113–124. http://dx.doi.org/10.1016/j.yqres.2005.05.003. A.L., Dias, P.L.D., 2006. Paleo-environmental change in Amazonian and African MacFadden, B.J., Shockey, B.J., 1997. Ancient feeding ecology and niche differentiation of rainforest during the LGM. Palaeogeography, Palaeoclimatology, Palaeoecology 239, Pleistocene mammalian herbivores from Tarija, Bolivia: morphological and isotopic 510–527. evidence. Paleobiology 23 (1), 77–100. Anhuf, D., Ledru, M.P., Behling, H., Da Cruz, F.W., Cordeiro, R.C., Van der Hammen, T., MacFadden, B.J., Wang, Y., Cerling, T.E., Anaya, F., 1994. South American fossil mammals Karmann, I., Marengo, J.A., De Oliveira, P.E., Pessenda, L., Siffedine, A., Albuquerque, and carbon isotopes: a 25 million-year sequence from the Bolivian Andes. A.L., Dias, P.L.D., 2006. Paleo-environmental change in Amazonian and African Palaeogeogr. Palaeoclimatol. Palaeoecol. 107, 257–268. L.M. França et al. / Earth-Science Reviews 140 (2015) 158–165 165

MacFadden, B.J., Cerling, T.E., Harris, J.M., Prado, J.L., 1999. Ancient latitudinal gradients of Prado, J.L., Sánchez, B., Alberdi, M.T., 2011. Ancient feeding ecology inferred from stable C3/C4 grasses interpreted from stable isotopes of New World Pleistocene horse isotopic evidence from fossil horses in South America over the past 3 Ma. BMC (Equus) teeth. Glob. Ecol. Biogeogr. 8, 137–149. Ecol. 11, 15. http://dx.doi.org/10.1186/1472-6785-11-15. Mayle, F.E., 2006. The Late Quaternary biogeographical history of South American season- Quade, J., Cerling, T.E., Barry, J.C., Morgan, M.E., Pilbeam, D.R., Chivas, A.R., Lee-Thorp, J.A., ally dry tropical forests: insights from palaeo-ecological data. In: Pennington, R.T., van der Merwe, N.J., 1992. A 16-Ma record of paleodiet using carbon and oxygen iso- Lewis, G.P., Ratter, J.A. (Eds.), Neotropical Savannas and Dry Forests: Plant Diversity, topes in fossil teeth from Pakistan. Chem. Geol. 94, 183–192. Biogeography and ConservationSystematics Association Special vol. 69. CRV Press, Sage, R.F., 2004. The evolution of C4 photosynthesis. New Phytol. 161, 341–370. Taylo & Francis, London, pp. 395–416. Sánchez, B., Prado, J.L., Alberdi, M.T., 2004. Feeding ecology, dispersal, and extinction Marcelo-Peña, J.L., Reynel-Rodríguez, C., Zevallos-Pollito, P., Bulnes-Soriano, F., Pérez- of South American Pleistocene gomphotheres (Gomphotheriidae, Proboscidea). Ojeda, A., 2007. Diversidad, composición ﬂorística y endemismos en los bosques Paleobiology 30, 146–161. estacionalmente secos alterados del distrito de Jaén, Perú. Ecología Aplicada 6 Sánchez, B., Prado, J.L., Alberdi, M.T., 2003. Paleodiet, ecology, and extinction of Pleisto- (1–2), 9–22. cene gomphotheres (Proboscidea) from Pampean Region (Argentina). Coloquios de Marcolino, C.P., Isaias, R.M.S., Cozzuol, M.A., Cartelle, C., Dantas, M.A.T., 2012. Diet of Paleontología 1, 617–625. Palaeolama major (Camelidae) of Bahia, Brazil, inferred from coprolites. Quat. Int. Tapia, E.M., Adriano-Morán, C.C., 2012. Stable carbon isotopes applied to vegetation 278, 81–86. http://dx.doi.org/10.1016/j.quaint.2012.04.002. reconstruction in the Teotihuacan Valley, Mexico. Boletin de la Sociedad Geológica Mothé, D., Avilla, L.S., Cozzuol, M., Winck, G.R., 2012. Taxonomic revision of the Quaterna- Mexicana 64 (2), 161–169. ry gomphotheres (Mammalia: Proboscidea: Gomphotheriidae) from the South Viana, M.S.S., Silva, J.L.L., Oliveira, P.V., Julião, M.S.S., 2011. Hábitos alimentares em American lowlands. Quat. Int. 276–277 (2012), 2–7. http://dx.doi.org/10.1016/j. herbívoros da megafauna pleistocênica no nordeste do Brasil. Estud. Geol. 21 (2), quaint.2011.05.018. 89–95. Passey, B.H., Robinson, T.F., Ayliffe, L.K., Cerling, T.E., Sponheimer, M., Dearing, M.D., Vivo, M.D., Carmignotto, A.P., 2004. Holocene vegetation change and the mammal faunas Roeder, B.L., Ehleringer, J.R., 2005. Carbon isotope fractionation between diet, breath of South American and Africa, J. Biogeogr. 31 (6), 943–957. CO2, and bioapatite in different mammals. J. Archaeol. Sci. 32 (10), 1459–1470. Vizcaíno, S.F., Cassini, G.H., Fernícola, J.C., Bargo, S., 2011. Evaluating habitats and feeding Pennington, T.R., Prado, D.E., Pendry, C.A., 2000. Neotropical seasonally dry forests and habits through ecomorphological features in glyptodonts (Mammalia, Xenarthra). Quaternary vegetation changes. J. Biogeogr. 27, 261–273. Ameghiniana 48, 305–319. Pereira, I.C.S., Dantas, M.A.T., Ferreira, R.L., 2013. Record of the giant sloth Valgipes Werneck, F.P., Costa, G.C., Colli, G.R., Prado, D.E., Sites Jr., J.W., 2011. Revisiting the historical bucklandi (Lund, 1839) (Tardigrada, Scelidotheriinae) in Rio Grande do Norte state, distribution of seasonally dry tropical forests: new insights based on palaeodistribution Brazil, with notes on taphonomy and paleoecology. J. S. Am. Earth Sci. 43 (2013), modelling and palynological evidence. Glob. Ecol. Biogeogr. 20, 272–288. http://dx.doi. 42–45. http://dx.doi.org/10.1016/j.jsames.2012.11.004. org/10.1111/j.1466-8238.2010.00596.x.