Revista Brasileira de Paleontologia, 23(2):138–152, Abril/Junho 2020 A Journal of the Brazilian Society of Paleontology doi:10.4072/rbp.2020.2.05

ISOTOPIC PALEOECOLOGY (δ13C, δ18O) OF A LATE VERTEBRATE COMMUNITY FROM THE BRAZILIAN INTERTROPICAL REGION

MÁRIO ANDRÉ TRINDADE DANTAS  Laboratório de Ecologia e Geociências, Instituto Multidisciplinar em Saúde, Universidade Federal da Bahia – Campus Anísio Teixeira, Vitória da Conquista, BA, . [email protected]

ALEXANDER CHERKINSKY  Center for Applied Isotope Studies, University of Georgia, Athens, GA 30602, USA. [email protected]

CARLOS MICAEL BONFIM LESSA  Laboratório de Ecologia e Geociências, Instituto Multidisciplinar em Saúde, Universidade Federal da Bahia – Campus Anísio Teixeira, Vitória da Conquista, BA, Brazil. [email protected]

LUCIANO VILABOIM SANTOS , MARIO ALBERTO COZZUOL  Programa de Pós-Graduação em Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. [email protected], [email protected]

ÉRICA CAVALCANTE OMENA  Programa de Pós-Graduação em Geociências, Universidade Federal de Pernambuco, Recife, PE, Brazil. [email protected]

JORGE LUIZ LOPES DA SILVA  Departamento de Paleontologia, Museu de História Natural, Universidade Federal de Alagoas, Maceió, AL, Brazil. [email protected]

ALCIDES NÓBREGA SIAL  NEG-LABISE, Departamento de Geologia, Centro de Tecnologia e Geociências, Universidade Federal de Pernambuco, Recife, PE, Brazil. [email protected]

HERVÉ BOCHERENS  Biogeology, Department of Geosciences and Senckenberg Center for Human Evolution and Palaeoenvironment (HEP), Universität Tübingen, Hölderlinstr. 12, 72074 Tübingen, Germany. [email protected]

ABSTRACT – Isotopes are one of the best tools to reconstruct the paleoecology of extinct taxa, allowing us to evaluate their diet (through carbon; C3 and C4 plants), their niche breadth (BA) and the environment in which they lived. In the present work we go deeper in the use of isotopes, and explore a mathematical mixing model with the stable isotopic composition of one (carbon) and two elements (carbon and oxygen) to evaluate (i) the relative contributions of three types of food resources (leaves, fruits and C4 grass) for meso- and megaherbivores (body mass > 100 kg) that lived during the in Sergipe, Brasil, and (ii) which of these (together with some faunivorous taxa) could be potential preys for populator and Caiman latirostris. Finally, we reconstructed the paleoenvironment in which the vertebrate community of Sergipe lived and concluded that the environment of Sergipe was a closer and drier landscape than African savannah nowadays, at least between 27 ka to 11 ka.

Keywords: Quaternary, , paleoecology, , stable isotopes.

138 Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 139

RESUMO – Isotópos são uma das melhores ferramentas para reconstruir a Paleoecologia de táxons extintos, permitindo sugerir dieta (por meio do carbono, plantas C3 e C4), o nicho ecológico (BA) e ambiente em que viveram. No presente artigo nos aprofundamos no uso dos isotópos, e exploramos um modelo matemático misto com um isotópo (carbono) e dois isotópos (carbono e oxigênio) (i) para sugerir três recursos tipos de recursos alimentares (folhas, frutas e gramíneas C4) para meso-megaherbívoros (massa corporal acima de 100 kg) que viveram no Pleistoceno final de Sergipe, Brasil, e (ii) qual desses herbívoros (juntamente com faunívoros) foram presas potenciais deSmilodon populator e Caiman latirostris. Por fim, reconstruímos o paleoambiente na qual a comunidade de vertebrados de Sergipe viveu, concluindo que era mais fechada e seca do que as savanas da Africa atualmente, pelo menos entre 27 mil a 11 mil anos atrás.

Palavras-chave: Quaternário, paleoecologia, América do Sul, isotópos estavéis.

INTRODUCTION MATERIAL AND METHODS

During the last three decades, stable isotopes have Dataset been used in paleoecology to infer the diet of extinct (and Sixteen samples (Table S1) of adult individuals of extant) taxa, based primarily on carbon isotopic data (e.g. Eremotherium laurilardi (Lund, 1842) (one exception is Bocherens et al., 1996; MacFadden, 2005; França et al., LPUFS 5693 assigned to a juvenile), Catonyx cuvieri (Lund, 2014a). Besides, nitrogen isotopic data have been used 1839), Pachyarmatherium brasiliense Porpino, Bergqvist to infer carnivory or omnivory in mammals as well (e.g. & Fernicola, 2009, Holmesina paulacoutoi (Guerra & Bocherens et al., 2016). Isotopic approaches represented a Marecha, 1984), Glyptotherium sp., Panochthus sp., major advance in paleoecological studies, helping to infer platensis Owen, 1837, Palaeolama major (Liais, 1872), two main food resources for herbivores (C3 and C4 plants) () neogeus Lund, 1840 and Smilodon and the paleoenvironmental context in which herbivores populator Lund 1842 from four localities in Sergipe (Fazenda and carnivores could live (forested or open environments; Elefante, Gararu; Fazenda Charco and Fazenda São José, Kingston & Harrison, 2007; Dantas et al., 2017). Poço Redondo; and Sítios Novos, Canhoba; Figure 1) However, stable isotopes can provide more ecological were analyzed to retrieve the carbon and oxygen isotopic information than previously thought, such as an estimate composition from structural carbonate of their bones, dentin of niche width and overlap, helping us to understand better and enamel. the ecology of extinct taxa, the competition for resources The samples were collected in “tanks”, which are natural and identify which were keystone species in extinct depressions on Neo-Mesoproterozoic litotypes, characterized communities (e.g. Dantas et al., 2017). Two isotopic pairs in by numerous fractures resulting from physical and chemical mathematical mixing models could be used to suggest more erosion, that contain sediments transported by seasonal rains than two food resources for herbivores (for example seven including the remains of and plants accumulated resources; Phillips, 2012 and references therein). during the dry season (e.g. Oliveira & Hackspacher, 1989). Most researchers use carbon and nitrogen isotopic The sediments in these depressions are estimated as being of data, extracting these data from collagen. However, in late Pleistocene and ages. tropical regions this protein is poorly preserved, leading to The isotopic composition of hydroxyapatite can be use only carbon and oxygen isotopic data extracted from preserved with minimal or no significant diagenetic alteration. hydroxyapatite. Indeed, hydroxyapatite usually survives Hydroxyapatite carbonate and phosphate in bone and dentin much better than the organic fraction of bone, i.e. collagen are more susceptible to diagenetic overprinting than enamel (Cherkinsky, 2009), and therefore is the best option to recover (Bocherens et al., 1996, 2011; Lee-Thorp & Sponheimer, 2003). diet information from extinct species in tropical regions. However, we noticed that in Sergipe localities diagenesis was The main aim of this paper was to use mathematical no significant, because similar values for bone and dentine mixing models using only carbon, or carbon and oxygen were found for Eremotherium laurillardi (UGAMS 9431 isotopic data in combination (measured on hydroxyapatite) and 9432), and bone, dentine and enamel for Notiomastodon from fossil vertebrates from the late Pleistocene of Sergipe, platensis (UGAMS 9437 and 9439) and Toxodon platensis Brazil, to: (i) infer three types of resources for herbivores (leaf, (UGAMS 9446) (Table S1), which gives us confidence in fruit and C4 grass); (ii) suggest, among the vertebrate taxa, isotopic results found in bone for Catonyx cuvieri, Holmesina which ones contributed to the isotopic diet of predators such as paulacoutoi, Glyptotherium sp., Panochthus sp., Palaeolama Smilodon populator and Caiman latirostris, allowing to infer major, and Smilodon populator (Table S1). a trophic web structure for this community; and, finally, (iii) Substitutions are mainly in the phosphate position and are suggest a reconstruction of the paleoenvironment in which most likely in the hydroxyl position. The absorbed carbonates these taxa could have lived. are more labile, but substituted ones are structural carbonates, Knowing the paleoecology and structure of this community and, thus, contribute to preserving the original isotopic will help us to understand the role of environmental change composition (Cherkinsky, 2009). in the of the in the late Pleistocene/ The stable isotope analyzes were performed at NEG- early Holocene. LABISE in “Centro de Tecnologia e Geociências” of 140 Revista Brasileira de Paleontologia, 23(2), 2020

Figure 1. Brazilian Intertropical Region map (sensu Oliveira et al., 2017) showing Gararu (1), Poço Redondo (2) and Canhoba (3) municipalities in Sergipe State, Brazil.

Universidade Federal de Pernambuco (Recife, Pernambuco, 2014). In addition, França et al. (2014a) reported that isotopic Brazil) and in Center for Applied Isotope Studies from diet (δ13C) of Eremotherium laurillardi and Notiomastodon University of Georgia (Georgia, USA). All samples were platensis did not change between 12–19 ky, suggesting a cleaned by ultrasonic bath with distilled water and then stable environment. left to dry naturally. The samples were then crushed into smaller fragments to be treated with diluted 1N acetic acid to Additional published data remove surface absorbed and secondary carbonates. Periodic In order to complement our results, and refine the evacuation ensured that evolved carbon dioxide was removed determination of the isotopic diet of Sergipe taxa, we included from the interior of the sample fragments, and that fresh acid previously published isotopic data (δ13C and δ18O, of which was allowed to reach even the interior micro-surfaces. most have 14C AMS datings; Table S1) and 14C AMS and The chemically cleaned samples were then reacted ESR datings for Eremotherium laurillardi, Notiomastodon under vacuum with 100 % phosphoric acid to dissolve the platensis, Toxodon platensis and Caiman latirostris (Dantas bone/dentine/enamel mineral and release carbon dioxide et al., 2011; França et al., 2014b; Dantas et al., 2014; 2017, from hydroxyapatite. The resulting carbon dioxide was and references therein). cryogenically purified from other reaction products and Furthermore, we refined and compared our results with catalytically converted to graphite (Cherkinsky, 2009). isotopic diet data of some extant African mesoherbivores

All results are reported using delta notation, δ = [(Rsample/ (body mass between 100 kg and 750 kg) and megaherbivores

Rstandard − 1)*1000] (Coplen, 1994). The reference for carbon (body mass > 800 kg) from Kenya and Tanzania (Bocherens isotope values (R = 13C/12C) is V-PDB, and oxygen isotope et al., 1996; Kingston & Harrison, 2007; Cerling et al., 2008), values (R = 18O/16O) is V-SMOW. since they live in an open environment, corresponding to The studied samples were not dated. However, many 14C the modern environment most similar to the one where the Accelerator Mass Spectrometry (AMS) and Electron Spin extinct meso- and megaherbivores mammals from Brazilian Resonance (ESR) datings for Eremotherium laurillardi and Intertropical Region (BIR) probably lived: Loxodonta Notiomastodon platensis are available (Table S1) for Fazenda africana (Blumenbach, 1797), Equus Boddaert, São José, Poço Redondo, Sergipe, allowing us to suggest 1785 (= E. burchelli), Dicerus bicornis (Linnaeus, 1758), that this fossil accumulation had relatively limited time- Ceratotherium simum (Burchell, 1817), Connochaetes averaging (~32 ky, considering both 14C AMS and ESR datings taurinus (Burchell, 1823), Syncerus caffer Sparrman, techniques; Dantas et al., 2011; 2017), similarly to another 1779, Kobus ellipsiprymnus (Ogilby, 1833), Oryx beisa fossil assemblage in northeastern Brazil (~59 ky, based only Rüppell, 1835, Giraffa camelopardalis( Linnaeus, 1758) and on ESR datings; Baixa Grande, Bahia; e.g. Ribeiro et al., amphibius Linnaeus, 1758 (Table 1). Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 141

Multivariate analyses -13±2 ‰) and CAM plants (intermediate values between the 13 18 13 Carbon (δ C) and oxygen (δ O) isotopic data for meso- δ C of C3 and C4 plants) (e.g. MacFadden, 2005; Dantas et al., megaherbivores from Sergipe, Brazil and Africa was submited 2017). However, some authors (e.g. Diefendorf et al., 2010; cluster analyses (Q-mode) using the weighted pair group Kohn, 2010) showed that the fractionation of carbon isotopes

method with simple arithmetic averages (UPGMA), with the in C3 plants presents great variability in different environments Euclidean Similarity coefficient. A bootstrap test (N = 10000) through the globe, which could lead to an overestimation of was applied to evaluate the consistency of the clusterings. the mean value of at least 2 ‰. 13 A Principal Component Analyses (PCA) was made as well. We tried to estimate the µδ C for C3 plants in the late All analyses were performed in the PAST 2.17 (Hammer et Pleistocene of Sergipe (altitude 186 m, latitude 10º), using al., 2001). the equation proposed by Kohn (2010). One problem that we faced was the absence of data about Mean Annual Body mass estimation Precipitation (MAP) in late Pleistocene of Sergipe. Thus, To estimate carbon enrichment (subtopic 2.5) and to we used present MAP data for Poço Redondo, Sergipe (MAP classify the studied mammals between mesoherbivores (body = 548 mm; Sergipe, 2011), and found a value of -26.80 ‰. mass between 100 kg and 750 kg) and megaherbivores (body As we do not have MAP for late Pleistocene of Sergipe, and mass > 800 kg), we calculated the estimated body mass (1) the value found is similar to the know average for C3 plants, for megafauna species that lived in Sergipe (Tables 1 and we choose to use µδ13C = -27 ‰. For Kenya (altitude 1140 S2) using the following regression (Anderson et al., 1985): m; latitude 20º; MAP 350 mm/; Bocherens et al., 1996) and Tanzania (altitude 1130 m; latitude 2º; MAP 550 mm/ year; Magill, 2012) we found µδ13C = -26.08 ‰ and µδ13C

= -26.48 ‰, respectively. Thus, for localities in Africa we 2.73 � � 13 �𝟏𝟏� �� � 0.078𝐶𝐶 ��� used µδ C = -26 ‰. Where bm is the body mass (g), C is the minimum Tejada-Lara et al. (2018) suggested that body mass

circumference of humerus and femur diaphysis (in mm). We influences physiological carbon enrichment (Ɛ*diet-bioapatite) in calculated an average value of circumferences based on the mammals and provided equations to determine these values information available in articles and gray literature (Cartelle & of enrichment. Carbon isotopic data presented here are from Abuhid, 1989; Porpino & Bergqvist, 2002; Castro & Langer, mammals (extinct and extant) with body mass varying from

2008; Porpino et al., 2009; Molena, 2012; Oliveira et al., 2017) 38 to 6,300 kg (Tables 1 and S2), Ɛ*diet-bioapatite varied between and in some collections that were accessible (Laboratório de 12.47 to 14.84 ‰, we used four values: +12 ‰ for taxa Paleontologia, Universidade Federal de Sergipe; Museu weighting less than 75 kg; +13 ‰ for taxa weighting between de Ciências Naturais, Pontifícia Universidade Católica de 75 kg to 600 kg; +14 ‰ for taxa weighting between 600 kg Minas Gerais). When the circumference information was to 3,500 kg; and finally, +15 ‰ for taxa weighting more than not available, we estimated it using the minimum width of 3,500 kg (Table S3). humerus and femur diaphysis as a diameter (d) measure (Table Considering an enrichment of 12–15 ‰, in Upper S2), through a circumference estimation: C = dπ. Pleistocene of Sergipe, δ13C values lower than -15 ‰ to -12 Xenarthrans have flat femur with a high circumference ‰ are typical of animals with a diet consisting exclusively of 13 of diaphysis values, leading to an overestimation of body C3 plants, while in Africa, δ C values lower than -14 ‰ to -11 mass if using standard method. To avoid this problem, we ‰ are typical of animals with a diet consisting exclusively of 13 multiplied their femur circumference by 0.4, trying to acquire C3 plants. For both areas δ C values higher than -1 ‰ to +2

a more realistic body mass estimation (2). The regression ‰ are consistent with a diet based on C4 plants.

adaptation was calibrated using values for three extant taxa, However, C3 plants show different values of enrichment, 13 one (Priodontes maximus (Kerr, 1792)) and two for example, leaves in C3 plants are depleted in C about -1.0 Tardigrada (Tamandua tetradactyla (Linnaeus, 1758) and ‰ than others non-photosynthetic tissues like fruits (in average Myrmecophaga tridactyla Linnaeus, 1758) (Table S2). 1.5±0.07 ‰) and roots (in average 1.1±0.09 ‰); in contrast, 13 Exceptions were made for (Panochthus and C4 plants tend to show no enrichment of C in tissues (e.g. Glyptotherium), whose body masses were estimated by fruits, roots) compared to leaves (e.g. Yoneyama & Ohtani, original regression proposed by Anderson et al. (1985). For 1983; MacFadden, 2005; Badeck et al., 2005; Cernuzak et al., extant African megamammals we used maximum estimate 2009). Thus, we can estimate different type of food resources body mass from Coe et al. (1976). using carbon isotopic values in a mathematical mixing model. Therefore, in this paper, we suggest a refinement of proportion of food items that medium- to large-bodied 2.73 herbivorous mammals (extant summing +2 ‰ to compare ���0.4𝑓𝑓� to extinct animals due to Suess effect - Keeling, 1979 - in �𝟐𝟐� �� � 0.078𝐶𝐶 Isotopic diet interpretation using δ13C and δ18O values carbon isotopic data) could intake using δ13C values in a The interpretation of carbon isotopic values for meso- and single element mathematical mixing model (Phillips, 2012),

megaherbivorous mammals is generally based on known suggesting as food types: leaves, fruits and C4 grass. Trying 13 13 average for C3 plants (µδ C = -27±3 ‰), C4 plants (µδ C = to distinguish food resources, we suggest carbon (using a 142 Revista Brasileira de Paleontologia, 23(2), 2020

difference of 2.5 ‰ between leaves and fruits in 3C plants) nitrogen isotopic data, thus, the only option available is to (Table S4) to be applied in equations (3) in Excel (Microsoft use oxygen isotopic data instead. Corporation, Redmond, Washington) through Solver Herbivores and carnivores acquire oxygen isotopic supplement (presuming non-negative values): through respiration, drunk water and food (Bocherens & Drucker, 2013), thus, for the carnivores we could use carbon 13 13 13 13 13 13 13 13 δ Cmixδ = δCmixC 1=f1 δ+ δC1fC1 2+f2 δ+ δC2fC2 3+f3 δ C3f3 and oxygen isotopic data to establish the proportion of their (3) (3) potential prey as they contribute with these isotopic values. 1 = f1 +1 f =2 +f1 f +3 f2 + f3 We used the isotopic data of the African lion Panthera leo (µδ13C = -5.40 ‰, δ18O = 31.64 ‰, Cerling et al., 2008) to test the use of carbon and oxygen to suggest the isotopic diet of To compare environmental conditions between Africa carnivores such as Smilodon populator and Caiman latirostris. and Sergipe, we considered δ18O values of proboscideans CO3 In these regressions we used as potential prey all the taxa as a “thermometer”, since these animals are considered present in Sergipe, Brazil (carnivores and herbivores; Tables evaporation-insensitive taxa, as their oxygen isotopes values S1 and 3), summing -1 ‰ due to trophic level (Bocherens & come mostly from drinking water (from lakes, rivers, pools), Drucker, 2013) in carbon data. presenting no correlation between carbon and oxygen (Figure 2; Levin et al., 2006) and water in plant tissues (except leaves) 18 13 13 13 13 13 13 13 13 1313 13 13 carries the same O isotopic signal as source water of δ Cmix = δ C1f1 + δ δC2Cf2mix + δ= δC3fC3 +1f 1δ + Cδ4f4C +2 f...2 ++ δ C311f3f11 + δ C4f4 + ... + δ C11f11 environment (Marshall et al., 2007). 18 18 1818 18 18 18 18 1818 18 18 18 (4) (4) δ Omix = δ O1f1 + δ δO2Of2mix + δ= δO3Of3 1+f 1δ + Oδ 4fO4 +2 ...f2 ++ δ δ OO113ff113 + δ O4f4 + ... + δ O11f11 Thus, we used the mean values of δ OCO3 found in 18 Loxodonta africana (Proboscidea; µδ OCO3 = 30.03±1.05 18 1 = f1 + f2 + f3 + f4 + ... + f111 = f1 + f2 + f3 + f4 + ... + f11 ‰; Figure 2A; Table 1) in comparison with δ OCO3 values of Notiomastodon platensis (Proboscidea; µδ18O = 32.57±1.95 CO3 ‰; Figure 2B; Table 1) as a proxy to establish the enrichment (+2.5 ‰) of 18O Sergipe environment in comparison to Africa Ecological measurements

environment. To estimate ecological measurements, we calculated For carnivores (Smilodon populator and Caiman isotope niche breadth (B) using Levins’ (1968) measure (5),

latirostris) we used a mathematical mixing model with two where pi is the relative proportion of individuals in isotope isotopes ( ). In general, nitrogen is used together with carbon 4 bin i. This measure was then standardized (BA) from 0 to 1 to estimate food resources in a mathematical mixing model following equation (6), where n is total number of isotope bins with two isotopes (e.g. Phillips, 2012, and examples therein), available. Values lower or equal to 0.5 suggests a specialist, however, analyses in hydroxyapatite are unable to generate and above 0.5, a generalist.

1 1 𝐵𝐵�1 𝐵𝐵�1 �𝟓𝟓� 𝐵𝐵� 2 �𝟓𝟓� 𝐵𝐵� 2 �𝟔𝟔� 𝐵𝐵𝐴𝐴 � �𝟔𝟔� 𝐵𝐵𝐴𝐴 � 𝛴𝛴𝛴𝛴𝑖𝑖 𝛴𝛴𝛴𝛴𝑖𝑖 ��1 ��1

Finally, to estimate the mean (ymean) and maximum (ymax) potential prey size for Smilodon populator (x - body mass of S. populator), we used regressions (7–8) proposed for Radloff & Du Toit (2004) by carnivores from Africa:

(7) Log10ymean = 1.39Log10x - 0.74 (8) Log10ymax = 1.46 Log10x - 0.17

(7) Log10ymean = 1.39Log10x - 0.74 (8) Log10ymax = 1.46 Log10x - 0.17

RESULTS

Body mass estimation For the Brazilian Intertropical Region (including Sergipe), there are no body mass estimations for Pleistocene mammals. Thus, following the first attempt proposed by Dantas et al. Figure 2. No correlation between δ13C and δ18O values of (A) Loxodonta (2017), we continued the efforts to infer the body mass of africana and (B) Notiomastodon platensis allowing to suggest that their mammals that lived there, which could help us to better oxygen isotopes values come mostly from drinking water. reconstruct their ecology. Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 143

For localities in Sergipe, we were able to suggest body Finally, in Sergipe, we had a fauna composed by one mass estimates (Tables 1 and S2) only for Eremotherium megacarnivore (Smilodon populator), one omnivore laurillardi (bm = ~3,416 kg) and Toxodon platensis (bm = (Pachyarmatherium brasiliense), six mesoherbivores ~1,770 kg). For other taxa there are no fossils available to (Holmesina paulacoutoi, Catonyx cuvieri, Glyptotherium sp., estimate their body masses. Therefore, we estimated body Panochthus sp., Palaeolama major and Equus (A.) neogeus) masses based on fossils from other geographical regions and three megaherbivores (Eremotherium laurillardi, Toxodon through Brazilian Intertropical Region (Table S2). We platensis and Notiomastodon platensis). estimated and used the following body masses: Catonyx 13 18 cuvieri (bm = ~777 kg), Pachyarmatherium brasiliense (bm Isotopic diet (δ C, δ O) = ~38 kg), Panochthus sp. (bm = ~785 kg), Glyptotherium The use of carbon in an one element isotopic mixing sp. (bm = ~710 kg), Holmesina paulacoutoi (bm = ~120 kg), model to suggest three resources allows us to refine the type of C plants consumed by herbivores in leaves and fruits. Palaeolama major (bm = ~285 kg), Equus (Amerhippus) 3 The proportion of C (summing proportions of leaves and neogeus (bm = ~420 kg) and Smilodon populator (bm = ~315 3 fruits) and C plants in this model presents similar values if kg). The body mass estimations for E. laurillardi, C. cuvieri, 4 we compare the proportions found in one element isotopic T. platensis and S. populator are similar to those proposed mixing model suggesting only C3 and C4 plants (Tables 1 for similar taxa from and (Fariña et al., and S5). 1998; Christiansen & Harris, 2005). For P. brasiliense, H. For Sergipe, we generated new isotopic data for paulacoutoi and P. major there is no body mass estimation Eremotherium laurillardi and Toxodon platensis, completed for comparison. We hypothetize that the lower body mass with unpublished isotopic data for Catonyx cuvieri, Holmesina estimation for Panochthus and Glyptotherium in BIR is due paulacoutoi, Glyptotherium sp., Panochthus sp., Palaeolama the avaibility of few bones (humerus and femur; Table S2) major and Equus (Amerhippus) neogeus, and include for both taxa and the lower circunference of the diaphysis published isotopic data for Eremotherium laurillardi, Toxodon in comparison to specimens found in United States and platensis and Notiomastodon platensis (França et al., 2014a; Argentina. Dantas et al., 2017, and references therein; Table S1; Figures

Figure 3. A, Principal Component Analyses (PCA) using δ13C and δ18O values for meso-megaherbivores from Africa and Sergipe, Brazil; B, Dendogram with clustering of taxa according to their ecological guilds (bootstrap test, N = 10.000). 144 Revista Brasileira de Paleontologia, 23(2), 2020

3A and 4) to refine isotopic diet of all taxa that lived in Sergipe mainly in C4 grass (pi = 67 %), but in fruits (pi = 23 %) and during the late Pleistocene. leaves (pi = 10 %), as well (Tables 1 and S1). For the giant Eremotherium laurillardi we We generated isotopic data for three Cingulata. The present five new carbon and oxygen isotopic data, which pampathere Holmesina paulacoutoi presents a δ13C of -6.0 ‰ shows δ13C values ranging from -6.0 ‰ to -3.9 ‰ (µδ13C and δ18O of 30.3 ‰, its diet was composed of 16 % of leaves, 18 18 = -4.9±0.9) and a δ O of 23.4 to 29.4 (µδ O = 27.4±2.3). 29 % of fruits and 55 % of grasses (Tables 1 and S1). For Including published isotopic data (França et al., 2014a; Dantas Glyptotherium sp. was found a carbon isotopic value of -1.8 et al., 2014; 2017) this interval increases, for carbon to -9.2 ‰ ‰ and oxygen isotopic value of 26.4 ‰, this taxon fed in 77 13 to -2.0 ‰ (µδ C = -5.0±1.8), and for oxygen to 23.4 to 30.3 % of C grasses, and little in fruits (p = 20 %) and leaves (p ‰ (µδ18O = 28.4±1.6) (Tables 1 and S1). Using all available 4 i i = 3 %) (Tables 1 and S1). Panochthus sp. presents δ13C of data for Sergipe in one isotopic mixing model, we suggest a -5.9 ‰ and oxygen isotopic value of 29.7 ‰, showing a diet diet composed of leaves (p = 18 %), fruits (p = 27 %) and, i i based on leaves (p = 22 %), fruits (p = 29 %) and C grass mainly, in C grasses (p = 55 %) (Table 1). i i 4 4 i (p = 49 %) (Tables 1 and S1). It is worth noting that LPUFS 5693 was an unworn i molariform from a juvenile (perhaps from a suckling For the Toxodon platensis four unpublished 13 individual), and we noticed that the carbon isotopic data (δ13C isotopic data were generated, which present a δ C variation 13 = -6.0 ‰) was not different from the adults of the same locality of -9.8 ‰ to -3.3 ‰ (µδ C = -5.0±3.2), and oxygen isotopic 18 (Fazenda São José, Poço Redondo; µδ13C = -5.4±2.3), being values between 27.4 ‰ to 34.2 ‰ (µδ O = 31.0±2.9) (Table equivalent to mother diet, because carbon isotopic values S1). Including the isotopic data presented by Dantas et al. of mother milk and offspring would not have significant (2017), carbon isotopic interval increases for -9.8 ‰ to -2.8 differences e.g.( trophic level; Jenkins et al., 2001). ‰ (µδ13C = -4.5±2.9), the oxygen isotopic range remains the Catonyx cuvieri (δ13C = -3.4 ‰; δ18O = 30.2 ‰) was same, but presents as mean values 31.2±2.5 ‰. This taxon another giant ground sloth analyzed, showing diet based presented a high consumption of C4 grass (pi = 58 %), followed

Figure 4. A, Pleistocene meso- megamammals from Sergipe, Brazil; B, two Smilodon populator stalking a Palaeolama major group, while two Caiman latirostris are scavenging a Notiomastodon platensis corpse (Images: Julio Lacerda, 2020). Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 145

by consumption of fruits (pi = 26 %), and low consumption Downing & White (1995) suggested, based on an of leaves (pi = 16 %) (Table 1). edentulous jaw tentatively assigned to Pachyarmatherium The diet of Palaeolama major (δ13C = -7.3 ‰; δ18O = 31.9 leiseyi, a diet composed mainly of termites and ants. Unfortunately, as we do not have nitrogen isotopic data for ‰) was composed mainly of C4 grass (pi = 45 %) but fed also P. brasiliense, we could not test this hypothesis. However, on fruits (pi = 32 %) and leaves (pi = 23 %) (Tables 1 and S1). For the Equus (Amerhippus) neogeus fossil we following Downing & White (1995), our results in 13 found a carbon isotopic value of -3.0 ‰, and a δ18O of 31.3 mathematical mixing model (δ C = -6.6 ‰; δ18O = 28.7 ‰; ‰, indicating a diet composed mainly of grasses (p = 70 %), Table S1) would not reflect a diet based on plants, but on i Blattodea taxa which lived in close (p = 48 %), as well as in while feeding on fruits (p = 22 %) and leaves (p = 8 %) was i i i open areas (p = 52 %). limited (Tables 1 and S1). i Smilodon populator (δ13C = -6.0 ‰; δ18O = 30.5 ‰; Table The proboscidean Notiomastodon platensis (µδ13C = S1) hunted similarly in closed (p = 52 %) and in open areas -0.1±1.1 ‰; µδ18O = 32.5±1.9 ‰; Table S1) presented a diet i (pi = 48 %), and had as main preys (pi ≥ 10 %; Table 3; Figure based mainly in C4 grass (pi = 83 %), 12 % in fruits, and low 5), Palaeolama major (pi = 14 %), Holmesina paulacoutoi proportions of leaves (pi = 5 %) (Table 1). (pi = 12 %), Toxodon platensis (pi = 12 %), Pachyarmatherium In addition to the isotopic data of meso-megaherbivores brasiliense (p = 11 %), Panochthus sp. (p = 12 %), Catonyx from Poço Redondo, Sergipe, we generated isotopic data of i i cuvieri (pi = 10 %), Equus (Amerhippus) neogeus (pi = 10 %) carbon and oxygen for Pachyarmatherium brasiliense and and Caiman latirostris (pi = 10 %) (Table 3). Smilodon populator, and included published isotopic data Another carnivore found in Sergipe was Caiman latirostris for Caiman latirostris (França et al., 2014b), to suggest a (δ13C = -3.0 ‰, δ18O = 31.4 ‰; França et al., 2014b; Table trophic web in this assemblage (Figure 5). Besides, isotopic S1), our analyses allow us to suggest that it could feed on data were used to estimate the possible habitat in which the a variety of taxa, mainly on taxa that lived in open areas terrestrial predators hunted. (pi = 82 %), as Notiomastodon platensis (pi = 44 %), as well

13 Table 1. Weight (t), mean values of proportional contributions (pi) of food sources (leaf, fruit, C4 grass), carbon isotopes (δ C), standardized isotopic niche 18 (1) breadth (BA), oxygen isotopes (δ O) and niche overlap (O) for extant meso-megamammals from Africa and Pleistocene of Sergipe. References: Coe et al. (1976); (2) Our data. Abreviations: mammals from Sergipe, Brazil. El, Eremotherium laurillardi; Cc, Catonyx cuvieri; Hp, Holmesina paulacoutoi; G, Glyptotherium sp.; P, Panochthus sp.; Tp, Toxodon platensis; Np, Notiomastodon platensis; Pm, Palaeolama major; En, Equus (Amerhippus) neogeus. Mammals from Africa. La, Loxodonta africana; Eq, Equus quagga; Db, Diceros bicornis; Cs, Ceratotherium simum; Ct, Connochaetes taurinus; Sc, Syncerus caffer; Ke, Kobus ellipsiprymnus; Ob, Oryx beisa; Gc, Giraffa camelopardalis; Ha, Hippopotamus amphibius. p 13 i 18 W (t) δ C BA δ O leaves fruits C4 grass Sergipe El 3.42 -5.0±1.8 0.18 0.27 0.55 0.68 28.4±1.6 Cc 0.78 -3.4 0.10 0.23 0.67 0.49 30.2 Hp 0.12 -6.0 0.16 0.29 0.55 0.72 30.3 G 0.71 -1.8 0.03 0.20 0.77 0.28 26.4 P 0.78 -5.9 0.22 0.29 0.49 0.84 29.7 Tp 1.77 -4.7±2.8 0.16 0.26 0.58 0.57 31.2±2.5 Np 6.27 -0.2±1.1 0.05 0.12 0.83 0.22 32.5±1.9 En 0.42 -3.0 0.08 0.22 0.70 0.43 31.3 Pm 0.28 -7.3 0.23 0.32 0.45 0.89 31.9 Africa La 5.00 -8.6±2.0 0.34 0.33 0.33 0,88 30.0±1.0 Eq 0.29 -0.6±1.1 - 0.01 0.99 0.01 31.2±1.8 Db 1.00 -10.1±1.8 0.35 0.36 0.29 0.89 29.5±1.3 Cs 2.00 0.3±0.2 - - 1.00 0.00 35.2 Ct 0.22 -0.1±1.3 - 0.01 0.99 0.01 33.3±0.9 Sc 0.66 0.9±1.3 - - 1.00 0.00 30.6±1.4 Ke 0.20 1.0 - - 1.00 0.00 29.5 Ob 0.16 -0.7 - - 1.00 0.00 33.4 Gc 1.20 -11.3±1.9 0.42 0.39 0.19 0.80 37.0±1.5 Ha 1.40 -4.1±1.5 0.06 0.21 0.73 0.38 26.9±1.5 146 Revista Brasileira de Paleontologia, 23(2), 2020

as Equus (A.) neogeus (pi = 18 %), Toxodon platensis (pi = Table 2), and closer to the HI found for

16 %), Catonyx cuvieri (pi = 12 %) and Glyptotherium sp. americanum (HI = 1.02±0.07; Table 2). This is unexpected,

(pi = 10 %; Table 3). but it could suggest that in Sergipe a population adapted to a diet with a higher consumption of dust and grid ingested

Niche breadth together with their food items (such as C4 grass), which We estimated the niche breadth for all vertebrates found reinforces our interpretation based on the mathematical mixing model of carbon isotopes. in Sergipe, Brazil (Table 1), suggesting as specialists (BA Another evidence came from L. Asevedo (pers.comm.), < 0.50), in crescent order: Notiomastodon platensis (BA which analyzed the feeding ecology of Eremotherium = 0.22±0.13), Glyptotherium sp. (BA = 0.28), Equus (A.) neogeus (B = 0.43) and Catonyx cuvieri (B = 0.49). Toxodon laurillardi from Gararu and Poço Redondo (both in Sergipe, A A Brazil) through stereomicrowear analysis, and noted high platensis (BA = 0.57±0.19), Eremotherium laurillardi (BA = 0.68±0.21), Holmesina paulacoutoi (B = 0.72), Panochthus values of scratch (fine and coarse), as well hypercoarse A scratches, gouges, cross-scratches and pits, which suggests sp. (BA = 0.84) and Palaeolama major (BA = 0.89) were generalists. The faunivorous Pachyarmatherium brasiliense a mixed feeder diet based mainly in grasses, but feeding in fruits and leaves as well, consistent with our interpretation (BA = 0.78) and Smilodon populator (BA = 0.85) were generalists, presenting similar values of niche breadth, and based on stable isotopes. Caiman latirostris was a specialist with the lowest niche The diet of the other Pilosa, Catonyx cuvieri, was partially breadth (B = 0.29) (Table 1). in contrast to the expectation for a Scelidotherinae, as a A selective feeder habit was expected, feeding more in fruits, leaves, buds and roots (Bargo et al., 2006a,b). The analyzed DISCUSSION sample (UGAMS 35324; Table S1) belonged to an adult individual (Dantas & Zucon, 2007), which presented a diet 13 18 Isotopic paleoecology (δ C, δ O): feeding habit lower in fruits and leaves (p = 33 %) and a major consumption Through the one element isotopic mixing model we could i of C4 grass (pi = 67 %) (Table 1). Maybe competition or refine the suggestion of diet for several taxa from Sergipe, in environmental conditions induced a change in its feeding all studied specimens we noted a diet composed mainly of habits, leading to a consumption of the most available abrasive resources, such as C4 grass. resources that were C4 grasses. Eremotherium laurillardi presented a consumption of 45 Some authors (Vizcaíno et al., 1998; 2011) suggested that % of C3 plants (fruits and leaves) and mainly a C4 grass diet Glyptotherium, Panochthus and Holmesina could be mainly (pi = 55 %; Table 1). Bargo et al. (2006a) suggested that E. grazers, based in biomechanics of the masticatory apparatus laurillardi and Megatherium americanum had masticatory and hypsodonty index. However, these observations could apparatus with similar biomechanical functions, presenting be effects of natural selection, based on the environments in robust cranial muscles which allows them to had a strong which these taxa evolved, and did not reflect an exclusive diet bite, and a thick cone-shaped and prehensile upper lip which on grass, thus, our isotopic results (Table 1) from Sergipe are could select part of plants. To support the discussion of our not odd, as presented a good consumption of C4 grasses (pi > isotopic results for E. laurillardi we followed Vizcaíno et al. 49 %), plus fruits and leaves of C3 plants. (2006) and Bargo et al. (2006b), and estimated the occlusal In Sergipe Toxodon platensis presented a diet composed surface area (OSA) and the Hypsodonty index (HI) for a mainly of C4 grass (pi = 57 %; Table 1). Compared to the dentary of E. laurillardi (LPUFS 4755) from Poço Redondo, data presented by Dantas et al. (2017) for all BIR, we noted Sergipe (Table 2). a contrast, as it fed more on C3 plants (pi = 60 %) than on C4 The estimated OSA from LPUFS 4755 was 10,650.83 plants (pi = 40 %), suggesting a drier environment in Sergipe mm2, which is equivalent to the OSA found for Megatherium than in other regions of BIR. For Palaeolama major our americanum (Table 2), suggesting that it could process a large analyses yielded a fair consumption of C4 grass (pi = 46 %). amount of turgid to soft food items, such as C4 grass and fruits. Compared to the data based on the analysis of coprolites The HI of Eremotherium laurillardi LPUFS 4755 was (Marcolino et al., 2013), we found a partial correspondence, higher (HI = 0.96; Table 2) than those found for northeastern as it suggested a diet based exclusively on C3 plants and our

Brazilian species (MCL and MNRJ samples; HI = 0.76±0.02; results suggest the consumption of, at least, 54 % of C3 plant

Table 2. Oclusal Surface Area (OSA) and Hypsodonty index (HI) of Megatherium americanum and Eremotherium laurillardi. Abbreviations: LTR, length of the tooth row; DM, depth of the mandible; HI, Hypsodonty Index. Data from Bargo et al. (2006b) and Vizcaíno et al. (2006). M. americanum E. laurillardi (LPUFS 4755) E. laurillardi (MCL & MNRJ) OSA (mm²) 10,818.36±464.23 10,650.83 - LTR 213.00±17.91 172.94 188.44±7.13 DM 215.64±18.14 166.06 143.56±8.50 HI 1.02±0.07 0.96 0.76±0.02 Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 147

tissues (fruits and leaves). Equus (Amerhippus) neogeus (pi = 29–33 %), fruits (pi = 33–36 %) and leaves (pi = 34–35 %; presented in Sergipe a diet composed mainly on C4 plants Table 1; Figure 3). Hippopotamus amphibius (BA = 0.38±0.23)

(pi = 69 %), which is in accordance with the isotopic results fed more on C4 grass (pi = 73 %), while in its case, values presented for Bahia (pi = 84 %; Dantas et al., 2017). Finally, attributed to fruits and leaves (pi = 27 %) could be C3 aquatic Notiomastodon platensis exhibited a diet composed of 83 % plants (Table 1). of C4 plants, presenting a similar consumption of C4 plants in Based on PCA and Cluster Analyses of the Sergipe extinct comparison with the mean value of the diet in BIR (pi = 70 %; mammals (Figure 3), we noticed that only Notiomastodon Dantas et al., 2017). Silva (2015), through stereomicrowear platensis was included in the grazer guild, feeding on more analysis, noticed that N. platensis individuals from Canhoba than 83 % of C4 grass, as observed in herbivores mammals were mixed feeders, but with a diet composed mainly of from Africa. The remaining studied taxa were included grasses. in the mixed-feeder guild (Figure 3), being subdivided in four subgroups, which presented mainly variations in their 13 18 Isotopic paleoecology (δ C, δ O): guilds consumption of C4 plants. Using carbon and oxygen isotopic data in PCA we noticed The taxa Toxodon platensis, Equus (A.) neogeus and Catonyx cuvieri showed an important consumption of C that the contribution of carbon (pi = 68 %) is higher than that 4 grass (p = 43–57 %) but fed significantly on fruits (p = of oxygen (pi = 32 %) and together with the Cluster analyses i i showed three well defined groups/guilds: browsers, mixed- 22–26 %) and leaves (pi = 8–16 %). In the other subgroup feeders and grazers (Figure 3). we have Palaeolama major, Panochthus sp. and Holmesina To better understand isotopic paleoecology of Sergipe paulacoutoi, these taxa exhibited a moderate consumption

Pleistocene mammalian taxa, we compared their isotopic of C4 grass (pi = 45–55 %), fruits (pi = 29–32 %) and leaves data with those available for 11 extant mammals from (pi = 16–23 %). Africa (Table 1 and Figure 3), and we analyzed the isotopic Finally, Eremotherium laurillardi and Glyptotherium sp. diet patterns found using mathematical mixing model using were grouped with Hippopotamus amphibius, mainly because carbon isotopes. of their lower oxygen isotopic values. For Glyptotherium sp. In Africa savannahs there were, at least, 20 species of we have only one sample, its lower value of oxygen is odd, grazers, 13 of browsers, 10 of mixed-feeders and one of as it had a great consumption of C4 grass (pi = 77 %). Gillette omnivore (Owen-Smith, 1982). The grazer guild was composed & Ray (1981) suggested that Glyptotherium could have had a of the megaherbivore Ceratotherium simum, a specialist semi-aquatic habit, like H. amphibius. However, as we have only one sample, we cannot discard or confirm this hypothesis. grazer (BA = 0.00), and for the specialists mesoherbivores

Equus quagga (BA = 0.01±0.02), Connochaetes taurinus (BA = 13 18 0.01±0.02), Syncerus caffer (BA = 0.00), Kobus ellipsiprymnus Isotopic paleoecology (δ C, δ O): trophic web

(BA = 0.00) and Oryx beisa (BA = 0.00), which have a diet To show the efficiency of the use of carbon and oxygen composed mainly of C4 grass (varying from 99 % to 100 %; (mainly this last one) isotopes values in a mathematical mixing Table 1; Figure 3), consumption of leaves and fruits were model to suggest the proportional contribution of herbivores virtually inexistent. in the diet of carnivores, we estimated the proportional In the browser guild we have data only for Giraffa contribution of African herbivores (Table 1) to the diet of camelopardalis (BA = 0.80±0.18) feeding in 42% of leaves and the lion Panthera leo. 39 % of fruits (Table 1; Figure 3), and, in the mixed-feeder Our results suggest that Panthera leo has a diet based on guild are Loxodonta africana (BA = 0.88±0.07) and Diceros Giraffa camelopardalis (pi = 20 %), Diceros bicornis (pi = 15 bicornis (BA = 0.89±0.16), which fed similarly on C4 grass %), Loxodonta africana (pi = 14 %), Hippopotamus amphibius

Table 3. Prey isotopic (δ13C, δ18O) contribution (%) to isotopic diet of two vertebrate carnivores from the Late Pleistocene of Sergipe, Brazil. Potential preys (weight in kg) Smilodon populator Caiman latirostris Smilodon populator (315) - - Caiman latirostris (60) 0.10 - Eremotherium laurillardi (3,416) 0.06 - Catonyx cuvieri (777) 0.10 0.12 Pachyarmatherium brasiliense (38) 0.11 - Holmesina paulacoutoi (120) 0.12 - Glyptotherium sp. (710) 0.02 0.10 Panochthus sp. (785) 0.12 - Toxodon platensis (1,770) 0.12 0.16 Notiomastodon platensis (6,300) 0.01 0.44 Palaeolama major (285) 0.14 - Equus (Amerhippus) neogeus (420) 0.10 0.18 148 Revista Brasileira de Paleontologia, 23(2), 2020

(pi = 12 %), Equus quagga (pi = 9 %), Connochaetes taurinus prey size. The on Caiman latirostris is suggested (pi

(pi = 8 %), Syncerus caffer (pi = 8 %), Kobus ellipsiprymnus = 10 %) based mainly on observations of predation nowadays

(pi = 8 %) and Oryx beisa (pi = 8 %). These results are in by the extant Felidae Panthera onca on this crocodilian taxon agreement with the literature (e.g. Hayward & Kerley, 2005; (e.g. Azevedo & Verdade, 2011). Isotopic contribution of

Loveridge et al., 2006) which shows a prey preference of P. leo Pachyarmatherium brasiliense (pi = 11 %) and Holmesina on G. camelopardalis, L. africana (calves, probably the same paulacoutoi (pi = 12 %) for S. populator diet could represent for D. bicornis and H. amphibius), E. quagga, C. taurinus, a scavenging habit for this carnivore (Table 3; Figure 5). S. caffer and O. beisa, in other words, 67 % of what was In Sergipe S. populator could not have a specialization on estimated by the mathematical mixing model using oxygen a prey type, which could suggest a pack-hunting behavior, and carbon isotopes. as individuals of this pack could feed on a variety of prey For Sergipe isotopic data are available for three samples proportionally. faunivorous taxa (Smilodon populator, Caiman latirostris In southern , Prevosti & Martin (2013), based and Pachyarmatherium brasiliense), allowing us to suggest on carbon and nitrogen isotopes, suggested as possible a trophic web structure for this late Pleistocene vertebrate prey for Smilodon: , indeterminated community (Figure 5) using the mathematical mixing model and Lama guanicoe (Camelidae). This is similar to the using oxygen and carbon isotopes. results of the present study, where the dominant prey Smilodon populator hunted more or less equally in also belonged to Camelidae taxa. However, the isotopic closed landscapes (pi = 52 %) and open environments (pi = approach depends on the isotopic data available, 48 %). Using regressions proposed by Radloff & Du Toit and Bocherens et al. (2016) suggested as main prey for (2004) we estimated that the mean and maximum prey Smilodon, (), followed by size for S. populator could had ranged between 540–3,000 Megatherium (Megatheriidae) and Lestodon (Mylodontidae), kg, suggesting that only 36 % of its diet was composed of which is different from the results of the present study, mainly taxa belonging to his optimal interval (Table 3). Above this because we do not have isotopic data for Macraucheniidae limit there is a low percentage (pi = 7 %), including the and Mylodontinae taxa in Sergipe. These results could reflect megaherbivores Eremotherium laurillardi and Notiomastodon a regional difference in prey types for S. populator, or, as platensis. However, the majority of its diet (pi = 56 %) was stated previously, it could be a consequence of the absence based on mammals weighting lower than 540 kg (Table 3). of isotopic data for more herbivores in our analyses. It is possible that Smilodon populator hunted actively The crocodylian Caiman latirostris could not actively

Equus (A.) neogeus (pi = 10 %) and Palaeolama major (pi = hunt mammals’ taxa found in Sergipe, as they body mass 14 %), as their body mass is not so distant from their mean were more than 420 kg (Table 3). However, we suggest that

Figure 5. Isotopic (δ13C and δ18O) trophic web from pleistocenic meso-megamammals from Sergipe, Brazil. Labels: bold arrows, food resources that contributed more than 50% in isotopic signature of consumer; gray thin arrow, food resources that contributed more than 10% in isotopic signature of consumer; gray thin cracked arrow, food resources that contributed less than 10% in isotopic signature of consumer. Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 149 it could feed on carcasses, acting as a scavenger, like other Looking at the oxygen isotopic values of the evaporation- crocodiles, since this would facilitate the dismembering of insensitive taxa Loxodonta africana (extant, Africa) and large prey corpses (e.g. Dixon, 1989; Perez-Higareda et al., Notiomastodon platensis (extinct, late Pleistocene of Sergipe 1989; Figures 4B and 5). Brazil) (Figure 2) we noticed that Sergipe presented, in comparison, a drier environment than Africa nowadays, with Paleoenvironmental reconstruction a difference of almost +2.5 ‰. The available isotopic data from extant megamammals França et al. (2014) noticed that, at least between 27 ka and 11 ka, the diet of Eremotherium laurillardi and Notiomastodon from Kenya and Tanzania (Table 1; Figure 3) yield a good platensis did not change, suggesting an environmental illustration of the meso-megaherbivore fauna from Africa, stability in Poço Redondo, Sergipe, including dated carbon with a predominance of grazer species with high consumption isotopic data from Toxodon platensis for Poço Redondo, N. of C plants (p = 99–100 %; Table 1), and where even mixed- 4 i platensis from Canhoba and E. laurillardi from Gararu, we feeder and browser species had a significant consumption of tentatively expand this interpretation to Sergipe. grass (p = 19–33 %). i The oxygen isotopic data of Eremotherium laurillardi In the late Pleistocene of Sergipe, the available data of and Toxodon platensis allowed us to suggest that these taxa meso-megaherbivores fauna showed a assemblage acquired their oxygen content through the drinking water, composed of mixed-feeders and species (Table 1; as well as Notiomastodon platensis (Figure 6A). Oxygen

Figure 3). They fed less on C4 grass (pi = 45–83 %) than extant isotopic data for dated T. platensis are similar to those from fauna from Africa, which could indicate that they lived in a N. platensis, but this is an isolated observation and does 18 more closed environment in comparison, with more C3 plants, not allow us to discuss this point further. The δ O values as herbs and shrubs. of dated N. platensis did not show variations trough time,

Figure 6. A, δ18O values through time: No correlation between δ13C and δ18O values for Eremotherium laurillardi (El; y = 0.12x + 29.03, R² = 0.02), Toxodon platensis (Tp; y = 0.20x + 32.16, R² = 0.05) and Notiomastodon platensis (Np; y = 0.63x + 32.68, R² = 0.13) allowing to suggests that their oxygen isotopes values reflect mostly their drinking water.B , δ13C values through time: Environmental stability through the late Pleistocene of Sergipe, between 27 ka to 11 ka. 150 Revista Brasileira de Paleontologia, 23(2), 2020 while oxygen isotopic values of dated E. laurillardi showed a Bargo, M.S.; Toledo, N. & Vizcaíno, S.F. 2006b. Muzzle of South slight variation, which could indicate an increase of humidity American Pleistocene ground sloths (Xenarthra, Tardigrada). through time, but virtually, it is similar to the oxygen data Journal of Morphology, 267:248–263. doi:10.1002/jmor.10399 from N. platensis (Figure 6B). Bocherens, H.; Cotte, M.; Bonini, R.; Scian, D.; Straccia, P.; Soibelzon, L. & Prevosti, F.J. 2016. Paleobiology of sabretooth cat Smilodon populator in the Pampean Region (Buenos Aires FINAL REMARKS Province, Argentina) around the Last Glacial Maximum: insights from carbon and nitrogen stable isotopes in bone

The herbivore fauna had a high consumption of C4 collagen. Palaeogeography, Palaeoclimatology, Palaeoecology, grass, belonging to two guilds: grazers (piC4 grass > 83%; 449:463–474. doi:10.1016/j.palaeo.2016.02.017 N. platensis) and Mixed Feeders (Glyptotherium sp; Equus Bocherens, H. & Drucker, D.G. 2013. Terrestrial teeth and bones. neogeus; Toxodon platensis; Holmesina paulacoutoi; In: S.A. Elias (ed.) The Encyclopedia of Quaternary Science, Panochthus sp.; Catonyx cuvieri; Eremotherium laurillardi; Elsevierp. 304–314. doi:10.1016/B0-44-452747-8/00353-7 and Palaeolama major). Bocherens, H.; Koch, P.L.; Mariotti, A.; Geraards, D. & Jaeger, J.J. 13 18 Smilodon populator could feed on meso-megaherbivores 1996. Isotopic biogeochemistry ( C, O) of mammalian enamel from African Pleistocene hominid sites. Palaios, :306–318. weighting between 285 kg to 6,300 kg (p = 67 %), eventually 11 i doi:10.2307/3515241 they could have hunted Caiman latirostris (p = 10 %), and i Bocherens, H.; Sandrock, O.; Kullmer, O. & Schrenk, F. 2011. we suggest that S. populator acted as scavengers feeding on Hominin palaeoecology in Late Malawi: Insights from the carcasses of Pachyarmatherium brasiliense (pi = 11 %) isotopes (13C, 18O) in mammal teeth. South African Journal of and Holmesina paulacoutoi (pi = 12 %). Besides this, we Science, 107:95–100. doi:10.4102/sajs.v107i3/4.331 suggest that C. latirostris could have behaved as a scavenger, Cartelle, C. & Abuhid, V.S. 1989. Novos espécimes brasileiros de feeding on carcasses of these meso-megamammals, especially Smilodon populator Lund, 1842 (Carnivora, ):

Notiomastodon platensis (pi = 44 %). morfologia e conclusões taxonômicas. In: CONGRESSO Finally, we suggest that the meso-megamammals from the BRASILEIRO DE PALEONTOLOGIA, 11, 1989. Anais, late Pleistocene of Poço Redondo, Sergipe, lived in a more Curitiba, p. 607–620. Castro, M.C. & Langer, M.C. 2008. New postcranial remains of closed (presence of C3 plants, like herbs and shrubs) and drier environment than that found nowadays in Africa savannah, Smilodon populator Lund, 1842 from south-central Brazil. and that this environment occurred in Sergipe between 27 Revista Brasileira de Paleontologia, 11:199–206. doi:10.4072/ ky to 11 ky at least. rbp.2008.3.06 Cerling, T.E; Harris, J.M.; Hart, J.A.; Kaleme, P.; Klingel, H.; Leakey, M.G.; Levin, N.E.; Lewison, R.L. & Passey, B.H. 2008. ACKNOWLEDGEMENTS Stable isotope ecology of the common hippopotamus. Journal of Zoology, 276:204–212. doi:10.1111/j.1469-7998.2008.00450.x To CNPq by financial support through Universal project Cernusak, L.A. et al. 2009. Why are non-photosynthetic tissues 13 (process 404684/2016-5) and research fellowship to MATD generally C enriched compared with leaves in C3 plants? (PQ/CNPq 311003/2019-2); To A. Liparini (Laboratório de Review and synthesis of current hypotheses. Functional Plant Paleontologia/UFS) and C. Cartelle (PUC/MG) for allow Biology, 36:199–213. doi:10.1071/FP08216 measurements in fossils collection that they are responsible Cherkinsky, A. 2009. Can we get a good radiocarbon age from “bad bone”? Determining the reliability of radiocarbon age for; To biologist V. Gomes and L. Alves for help in Solver from bioapatite. Radiocarbon, 51:647–655. doi:10.1017/ (Excel) analysis; To H. Araujo Jr., L. Asevedo and reviewers S0033822200055995 for critical evaluation of manuscript. Christiansen, P. & Harris, J.M. 2005. Body size of Smilodon (Mammalia: Felidae). Journal of Morphology, 266:369–384. REFERENCES doi:10.1002/jmor.10384 Coe, M.J.; Cumming D.H. & Phillipson, J. 1976. Biomass and Anderson, J.F.; Hall-Martin, A. & Russel, D.A. 1985. Long-bone production of large African herbivores in relation to rainfall circumference and weight in mammals, birds and dinosaurs. and primary production. Oecologia, 22:341–354. doi:10.1007/ Journal of Zoology, 207:53–61. doi:10.1111/j.1469-7998.1985. BF00345312 tb04915.x Coplen, T.B. 1994. Reporting of stable hydrogen, carbon, and oxygen Azevedo, F.C.C. & Verdade, L.M. 2011. Predator–prey interactions: isotopic abundances. Pure and Applied Chemistry, 66:273–276. jaguar predation on caiman in a floodplain forest. Journal of doi:10.1016/0375-6505(95)00024-0 Zoology, 286:200–207. doi:10.1111/j.1469-7998.2011.00867.x Dantas, M.A.T.; Cherkinsky, A.; Bocherens, H.; Drefahl, M.; Badeck, F.W.; Tcherkez, G.; Nogues, S.; Piel, C. & Ghashghaie, Bernardes, C. & França, L.M. 2017. Isotopic paleoecology of J. 2005. Post-photosynthetic fractionation of stable carbon the Pleistocene megamammals from the Brazilian Intertropical isotopes between plant organs - a widespread phenomenon. Region: Feeding ecology (δ13C), niche breadth and overlap. Rapid Communications in Mass Spectrometry, 19:1381–1391. Quaternary Science Reviews, 170:152–163. doi:10.1016/j. doi:10.1002/rcm.1912 quascirev.2017.06.030 Bargo, M.S.; De Iuliis, G. & Vizcaíno, S.F. 2006a. Hypsodonty Dantas, M.A.T.; Porpino, K.O.; Bauermann, S.G.; Prata, A.P.N.; in Pleistocene ground sloths. Acta Palaeontologica Polonica, Cozzuol, M.A.; Kinoshita, A.; Barbosa, J.H.O. & Baffa, O. 51:53–61. 2011. Megafauna do Pleistoceno superior de Sergipe, Brasil: Dantas et al. – Isotopic paleoecology of a late Pleistocene vertebrate community 151

registros taxonômicos e cronológicos. Revista Brasileira de Unites States of America, 107:19691–19695. doi:10.1073/ Paleontologia, 14:311–320. doi:10.4072/rbp.2011.3.10 pnas.1004933107 Dantas, M.A.T.; Santos, D.B.; Liparini, A.; Queiroz, A.N.; Carvalho, Lee-Thorp, J.A. & Sponheimer, M. 2003. Three case studies used to O.A.; Castro, É.S.V. & Cherkinsky, A. 2014. A dated evidence reassess the reliability of fossil bone and enamel isotope signals of the interaction between humans and megafauna in the late for paleodietary studies. Journal Anthropology Archaeology, Pleistocene of Sergipe state, northeastern Brazil. Quaternary 22:208–216. doi:10.1016/S0278-4165(03)00035-7 International, 352:197–199. doi:10.1016/j.quaint.2014.09.040 Levin, N.E.; Cerling, T.E.; Passey, B.H.; Harris, J.M. & Ehleringer, J.R. Dantas, M.A.T. & Zucon, M.H. 2007. Occurrence of Catonyx cuvieri 2006. A stable isotope aridity index for terrestrial environments. (Lund, 1839) (Tardigrada, Scelidotheriinae) in Late Pleistocene- Proceedings of the National Academy of Science of the Unites States Holocene of Brazil. Revista Brasileira de Paleontologia, of America, 103:11201–11205. doi:10.1073/pnas.0604719103 10:129–132. Levins, R. 1968. Evolution in changing environments. New Jersey, Diefendorf, A.F.; Mueller, K.E.; Wing, S.L.; Koch, P.L. & Freeman, Princeton University Press, 120 p. K.H. 2010. Global patterns in leaf 13C discrimination and Loveridge, A.J.; Hunt, J.E.; Murindagomo, F. & MacDonald, D.W. implications for studies of past and future cimate. Proceedings of 2006. Influence of drought on predation of (Loxodonta the National Academy of Science of the Unites States of America, africana) calves by lions (Panthera leo) in an African wooded 107:5738–5743. doi:10.1073/pnas.0910513107 savannah. Journal of Zoology, 270:523–530. doi:10.1111/j.1469- Dixon, D.M. 1989. A note on some scavengers of ancient Egypt. 7998.2006.00181.x World Archaeology, 21:193–197. doi:10.1080/00438243.198 MacFadden, B.J. 2005. Diet and habitat of toxodont megaherbivores 9.9980101 (Mammalia, Notoungulata) from the late Quaternary of South Downing, K.F. & White, R.S. 1995. The cingulates (Xenarthra) of and Central America. Quaternary Research, 64:113–124. the Leisey Shell Pit local fauna (Irvingtonian), Hillsborough doi:10.1016/j.yqres.2005.05.003 County, . Bulletin of the Florida Museum of Natural Marcolino, C.P.; Isaias, R.M.S.; Cozzuol, M.A.; Cartelle, C. & History, 37:375–396. Dantas, M.A.T. 2012. Diet of Palaeolama major (Camelidae) Fariña, R.A.; Vizcaíno, S.F. & Bargo, M.S. 1998. Body mass of Bahia, Brazil, inferred from coprolites. Quaternary estimations in (late Pleistocene-early Holocene International, 278:81–86. doi:10.1016/j.quaint.2012.04.002 Marshall, J.D.; Brooks, J.R. & Lajtha, K. 2007. Sources of variation of South America) mammal megafauna. Mastozoología in the stable isotopic composition of plants. In: K. Michemer Neotropical, 5:87–108. (ed.) Stable isotopes in ecology and environmental ccience, França, L.M.; Dantas, M.A.T.; Bocchiglieri, A.; Cherkinsky, A.; Blackwell Publishing, p. 22–60. Ribeiro, A.S. & Bocherens, H. 2014a. Chronology and ancient Molena, F.P. 2012. Variação individual no esqueleto apendicular de feeding ecology of two upper Pleistocene megamammals from mastodontes (Proboscidea: Gomphotheriidae) provenientes de the Brazilian Intertropical Region. Quaternary Science Reviews, São Bento do Una, Pernambuco, Brasil. Universidade de São 99:78–83. doi:10.1016/j.quascirev.2014.04.028 Paulo, Dissertação de Mestrado, 185 p. doi:10.11606/D.41.2012. França, L.M.; Fortier, D.C.; Bocchiglieri, A.; Dantas, M.A.T.; tde-01052013-093838 Liparini, A.; Cherkinsky, A. & Ribeiro, A.S. 2014b. Radiocarbon Oliveira, A.M.; Becker-Kerber, B.; Cordeiro, L.M.; Borghezan, dating and stable isotopes analyses of Caiman latirostris (Daudin, R.; Avilla, L.S.; Pacheco, M.L.A.F. & Santos, C.M.D. 2017. 1801) (Crocodylia, Alligatoridae) from the late Pleistocene of Quaternary mammals from Central Brazil (Serra da Bodoquena, Northeastern Brazil, with comments on spatial distribution of the Mato Grosso do Sul) and comments on Paleobiogeography species. Quaternary International, 352:159–163. doi:10.1016/j. and Paleoenvironments. Revista Brasileira de Paleontologia, quaint.2014.06.046 20:31–44. doi:10.4072/rbp.2017.1.03 Gillette, D.D. & Ray, C.E. 1981. Glyptodonts of North America. Oliveira, L.D.D. & Hackspacher, P.C. 1989. Gênese e provável idade Smithsonian Contributions to Paleobiology, 40:1–255. dos tanques fossilíferos de São Rafael-RN. In: CONGRESSO Hammer, Ø.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontologial BRASILEIRO DE PALEONTOLOGIA. Anais, Curitiba, UFPR, Statistics Software Package for Education and Data Analysis. p. 30–34. Palaeontology Electronica, 4:1–9. Owen-Smith, N. 1982. Factors influencing the consumption of plant Hayward, M.W. & Kerley, G.I.H. 2005. Prey preferences on the lion products by large herbivores. In: B.J. Huntley & B.H. Walker (Panthera leo). Journal of Zoology, 267:309–322. doi:10.1017/ (eds.) The ecology of tropical savannas, Springer-Verlag, p. S0952836905007508 359–404. Jenkins, S.G.; Partridge, S.T.; Stephenson, T.R.; Farley, S.D. & Pérez-Higareda, G.; Rangel-Rangel, A.; Smith, H.M. & Chiszar, D. Robbins, C.T. 2001. Nitrogen and carbon isotope fractionation 1989. Comments on the food and feeding Hhabits of Morelet’s between mothers, neonates, and nursing offspring. Oecologia, Crocodile. Copeia, 4:1039–1041. doi:10.2307/1445994 129:336–341. doi:10.1007/s004420100755 Phillips, D.L. 2012. Converting isotope values to diet composition: Keeling, C.D. 1979. The Suess effect: 13Carbon-14Carbon the use of mixing models. Journal of Mammalogy, 93:342–352. interrelations. Environment International, 2:229–300. doi:10.1644/11-MAMM-S-158.1 doi:10.1016/0160-4120(79)90005-9 Porpino, K.O. & Bergqvist, L.P. 2002. Novos achados de Panochthus Kigston, J.D. & Harrison, T. 2007. Isotopic dietary reconstructions (Mammalia, Cingulata, Glyptodontidae) no nordeste do Brasil. of Pliocene herbivores at Laetoli: Implications for early Revista Brasileira de Paleontologia, 4:51–62. hominin paleoecology. Palaeogeography, Palaeoclimatology, Porpino, K. O.; Fernicola, J.C. & Bergqvist, L.P. 2009. A new Palaeoecology, 243:272–306. doi:10.1016/j.palaeo.2006.08.002 Cingulate (Mammalia: Xenarthra) Pachyarmatherium Kohn, M.J. 2010. Carbon isotopic compositions of terrestrial brasiliense sp. nov. from the late Pleistocene of northeastern C3 plants as indicator of (paleo)ecology and (paleo)climate. Brazil. Journal of Vertebrate Paleontology, 29:881–893. Proceedings of the National Academy of Science of the doi:10.1671/039.029.0305 152 Revista Brasileira de Paleontologia, 23(2), 2020

Prevosti, F.J. & Martin, F.M. 2013. Paleoecology of the mammalian Society Biological Sciences B, 285:20181020. doi:10.1098/ predator guild of Southern Patagonia during the latest Pleistocene: rspb.2018.1020 ecomorphology, stable isotopes, and taphonomy. Quaternary Vizcaino, S.F.; Bargo, M.S. & Cassini, G.H. 2006. Dental occlusal International, 304:74–84. doi:10.1016/j.quaint.2012.12.039 surface area in relation to body mass, food habits and other Radloff, F.G.T. & Du Toit, J.T. 2004. Large predators and their prey biological features in fossil xenarthrans. Ameghiniana, in a southern African savanna: a predator’s size determines 43:11–26. its prey size range. Journal of Ecology, 73:410–423. Vizcaíno, S.F.; Cassini, G.H.; Fernicola, J.C. & Bargo, M.S. 2011. doi:10.1111/j.0021-8790.2004.00817.x Evaluating habitats and feeding habits through ecomorphological Ribeiro, R.C.; Araújo-Júnior, H.I.; Kinoshita, A.; Figueiredo, features in glyptodonts (Mammalia, Xenarthra). Ameghiniana, A.M.G.; Baffa, O. & Carvalho, I.S. 2014. How much time is 48:305–319. doi:10.5710/AMGH.v48i3(364) represented in the fossil record of tank deposits? In: SIMPÓSIO Vizcaíno, S.F.; De Iullis, G. & Bargo, M.S. 2008. Skull shape, BRASILEIRO DE PALEONTOLOGIA DE VERTEBRADOS, masticatory apparatus, and diet of Vassalia and Holmesina 9, 2014. Boletim de resumos, Vitória, SBP, p. 115. (Mammalia: Xenarthra: ): when anatomy Secretaria de Estado do Planejamento, da Ciência e da Tecnologia. constrains destiny. Journal of Mammalian Evolution, 5:291–322. 2011. Atlas digital sobre recursos hídricos Sergipe. Sergipe, doi:10.1023/A:1020500127041 SEPLANTEC/SRH. CD-ROM. Yoneyama, T. & Ohtani, T. 1983. Variations of natural 13C Silva, L.A. 2015. Paleoecologia alimentar dos gonfotérios abundances in leguminous plants. Plant & Cell Physiology, (proboscidea: mammalia) pleistocênicos da América do Sul. 24:971–977. doi:10.1093/oxfordjournals.pcp.a076627 Universidade Federal do Estado do Rio de Janeiro, Dissertação de Mestrado, 139 p. Tejada-Lara, J.V.; MacFadden, B.J.; Bermudez, L.; Rojas, G.; Salas- Gismondi, R. & Flynn, J.J. 2018. Body mass predicts isotope enrichment in herbivorous mammals. Proceedings of the Royal Received in 24 September, 2019; accepted in 30 March, 2020.