University of Florida Thesis Or Dissertation

Home , Astrapotherium, Mylodontidae, Pebas Formation

FEEDING ECOLOGY OF ANCIENT AND MODERN MAMMALS FROM AMAZONIA: AN ISOTOPIC APPROACH

JULIA VICTORIA TEJADA-LARA

A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE

UNIVERSITY OF FLORIDA

2015

To all those people that risk their lives to protect Amazonian forests

ACKNOWLEDGMENTS

First and foremost, to my advisor, Bruce MacFadden, thanks to whom I had the opportunity to pursue graduate studies in the United States. The confidence he granted at accepting me as a graduate student has been a crucial step of my career and of my life. Realizing how difficult the adaptation to a new country (in my case for the first time) can be, he helped me in different ways and made me feel I was not alone. The reading of his works while I was an undergrad in Peru inspired me and nurtured my interest in paleontology. I can sincerely say that Bruce MacFadden has served as an inspiration both as a scientist and as a person and would like to express how honored I feel to be one of his students.

To my committee members Jonathan Bloch and Karen Bjorndal for their support and advices during the duration of my project. To Jon, I would also like to thank his excitement in some aspects of my project which were highly encouraging. To Douglas

Jones for finding time in his extremely busy agenda to stop by my office and ask about my progress and my project, for his sense of humor, and for helping me in my quest for dead sloths. To Pierre-Olivier Antoine for the countless times he has helped me and advised me, for his integrity, and for being one of the nicest people I was fortunate to meet. To Carlos Jaramillo for kindly help me numerous times in personal and scientific matters even before I ask for them. Fossils included in this study were collected on numerous and hard field expeditions, this work would not be possible without all the people that participated on them. I would like to especially thank John Flynn and Patrice

Baby. Ana Balcarcel was the best field mate I could ever imagine.

Numerous people and institutions were essential for the development of this thesis. I am grateful to the Florida Museum of Natural History (FLMNH) for granting me

the Lucy Dickinson Student Award. I would like to thank Victor Pacheco (Department of

Mammalogy, Museo de Historia Natural-UNMSM) for allowing me to take samples of the specimens under his care, and Melissa Del Alcazar for assisting at sampling collection. Lizette Bermudez (Zoológico de Huachipa, Lima-Perú) kindly donated dead specimens from the zoo under her direction and helped providing information on modern sloths. Craig Pugh, Larry Killmar, Ray Ball, and Heather Henry from the Lowry

Park Zoo in Tampa, Florida, for providing one of the Choloepus specimens used in this study. To Jason Curtis and George Kamenov (Department of Geological Sciences,

University of Florida) for help and advices during the isotopic and rare elemental analyses. To Jorge Moreno and the PCP-PIRE interns for making the effort at trying to collect buried modern sloths. To Jaime Turpo for help processing food samples for the isotopic analyses and Manuel Burga for assisting me at MUSM. The fossils used in this thesis were collected with funds provided by the ECLIPSE Program of the CNRS

(France), the American Museum of Natural History (New York, USA), and with the kindly help of Badis Kouidrat of Devanlay Peru SAC. The different analyses were carried out with funds from the Florida Museum of Natural History and the PCP-PIRE project (NSF PIRE 0966884).

Many people made my life happier and more enjoyable in Gainesville, among them Luz Helena Oviedo, Leonor Suarez, Fabianny Herrera, Benjamin Himschoot,

Chanika Symister, Sean Moran, Carly Manz, Jason Bourque, Sarah Allen, Diego

Ramirez, Paul Morse, Ivelisse Ruiz, Thomas Knight, Gerardo Nunez, Tania Chavarria,

Elena Ortiz, Jenna Moore, Angélica García, Angelo Soto, Ummat Somjee, and many others.

My parents have always been a source of inspiration and taught by example the importance of exceeding one-self in every endeavor, the meaning of hard-work, and to always be driven by honesty and correctness in every action. I thank my brothers for their support and for make me feel that time and distance are meaningless variables between us.

Finally, I would like to thank Rodolfo Salas, for being who he is, for introducing me to the world of paleontology with his endless passion, for his love, for making me laugh, and for making me feel the most important person in the world. Thanks to him, and also to some luck and natural stubbornness from my part, I was able to make passion the driving force of my life and to accomplish the few accomplishments I had.

Paleontology and happiness are linked to me and Rodolfo is the one who knots them tightly.

TABLE OF CONTENTS

page

ACKNOWLEDGMENTS ...... 4

LIST OF TABLES ...... 9

LIST OF FIGURES ...... 10

LIST OF ABBREVIATIONS ...... 11

ABSTRACT ...... 12

CHAPTER

1 INTRODUCTION ...... 14

Background ...... 14 Goals of this Contribution ...... 17 Middle Miocene in Tropical South America and Study Sites ...... 17 Isotopic Analyses: Interest, Previous Studies, and Challenges ...... 20 Diagenesis, Rare Earth Elements Analysis, and Carbon Isotope Enrichment ...... 21 REE Analysis ...... 23 Carbon Isotope Enrichment ...... 24

2 MATERIALS AND METHODS ...... 27

Taxa and Teeth Analyzed for Isotope and REE Analyses ...... 27 Rare Earth Elemental (REE) Analysis...... 29 Isotopic Analysis ...... 30 13 Dental Tissue-to-Diet C Enrichment of Modern Sloths (Ɛ*bioapatite-diet) ...... 31

3 RESULTS ...... 33

REE ...... 33 Isotope Enrichment ...... 34 Isotopic Structure (δ13C) of Mammals from Modern Amazonia ...... 36 Isotopic Signatures of Fossil Mammals from Proto-Amazonia: δ13C ...... 39

4 DISCUSSION ...... 54

Madre de Dios (Peru, Amazonia) and Ituri (Congo, Africa): Two Different Closed-Canopy Forests ...... 54 Feeding Ecology of Fossil Mammals from Proto-Amazonia ...... 55 Amazonia vs Proto-Amazonia Canopy Structure ...... 57

5 SUMMARY AND CONCLUSIONS ...... 62

APPENDIX: RARE EARTH ELEMENTS (REE) ANALYSIS ...... 65

LITERATURE CITED ...... 71

BIOGRAPHICAL SKETCH ...... 79

LIST OF TABLES

Table page

3-1 Isotopic signatures (δ13C and δ18O) of dental bioapatite of modern mammals from Peruvian Amazonia...... 47

3-2 Isotopic signatures of the sloths and their food analyzed to calculate the ε*diet-enamel...... 49

3-3 δ13C and δ18O of tooth enamel and outer dentine of fossil mammals from Miocene proto-Amazonia...... 51

3-4 Descriptive statistics for δ13C of fossil mammals...... 52

A-1 REE data (normalized to PAAS) for specimens analyzed during this study...... 65

A-2 REE Indices ...... 69

LIST OF FIGURES

Figure page

1-1 Map of Peru with the location of the two sites where the fossil vertebrates used in this study were found, Iquitos (A) and Fitzcarrald (B)...... 26

3-1 Rare earth element (REEN) signatures for the four localities containing fossil sloths analyzed in this study...... 43

3-2 Plots of median REEN concentrations for enamel, outer dentine, and bone for each locality...... 44

3-3 Plots of median REEN concentrations for enamel, outer dentine, and bone for all four localities...... 45

3-4 Histogram showing distribution of REE Index values for the 38 enamel/bone. ... 46

3-5 Carbon isotope data from modern mammals of Amazonia (Madre de Dios, Peru)...... 50

3-6 Isotopic signatures (δ13C) of the fossil mammals...... 53

4-1 Comparison of mammal community structure between an Amazonian forest (Madre de Dios, Peru) and the Ituri forest (Congo, Africa)...... 60

4-2 Comparison of δ13C values of modern and fossil mammals from western Amazonia...... 61

LIST OF ABBREVIATIONS

Ɛ* Isotope enrichment

MAT Mean Annual Temperature

MUSM Museo de Historia Natural – Universidad Nacional Mayor de San Marcos

PAAS Post-Archean Australian Shale

REE Rare Earth Elements

SALMA South American Land Mammal Age

Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science

FEEDING ECOLOGY OF ANCIENT AND MODERN MAMMALS FROM AMAZONIA: AN ISOTOPIC APPROACH

Julia Victoria Tejada-Lara

May 2015

Chair: Bruce MacFadden Major: Zoology

Carbon isotope analyses (δ13C) were performed on three major clades of South

American Tertiary mammals (Astrapotheria, Toxodontia, and Folivora) in order to infer resource partitioning in Miocene proto-Amazonia. The inclusion of fossil sloths, mammals with teeth lacking enamel, required (1) the evaluation of potential diagenetic alteration through the Rare Earth Elements Index, and (2) the estimation of the previously unknown isotope enrichment between diet and bioapatite (ε*).

Isotopic results of the fossil mammals showed that the only group with δ13C values non-significantly different from modern Amazonian mammals was that composed by big mylodontines (e.g. Urumacotherium). These animals were most likely feeding deep inside the closed canopy forest. Some of the δ13C values of toxodonts overlap the most positive δ13C values observed in modern Amazonian mammals. These animals could have been inhabiting marginal areas of the forest and/or feeding in the forest gaps. The groups including astrapotheres, Pseudoprepotherium, and

Hapalopsinae/Megalonychidae have δ13C signatures inconsistent with that of modern closed canopy mammals. However, corresponding δ13C values have been observed in

aquatic plants. Considering the prevailing environmental conditions in proto-Amazonia, this work proposes that these taxa could have inhabited the marginal aquatic settings.

Based on the mammals analyzed, the mean δ13C of the fossil mammal assemblage is significantly different than that obtained for those of modern Amazonia.

These differences might reveal a broader range of habitats within the proto-Amazonian biome in the Miocene, including closed-canopy forests fragmented by open non- forested areas probably representing the set of aquatic ecosystems that characterized the Pebas megawetland.

CHAPTER 1 INTRODUCTION

Background

In paleontology, understanding the feeding ecology of fossil mammals allows us to reconstruct ancient environments and ecosystems and to recognize, among many things, niche partitioning, predator-prey interactions, habitat use, and the evolution of trophic specializations over time (e.g., MacFadden and Shockey 1997; MacFadden

2005; Cassini et al. 2012). Paleontologists have historically relied on tooth and craniodental morphology to infer the feeding ecology of extinct mammals. Regardless of the methodology used it has usually been tailored after documented correlations between diet and habitats in modern ecosystems. Ancient ecosystems with similar taxonomic composition to those of modern ones likely follow similar rules and correlations and allow for convincing reconstructions of diet and habitat by analogy.

However, modern analogies can greatly limit our interpretations of faunas when applied to ancient ecosystems composed of completely extinct lineages in potentially non- analogous ecosystems, like those of most of the South American Tertiary mammal fossil record. Indeed, because of the insular nature of South America for much of the

Cenozoic (for ~60 Ma prior the formation of the Panamanian Isthmus, MacFadden

2006) mammals were endemic. Although some converged in morphologies comparable to modern mammals, others have no modern morphological or ecological parallel (Croft

1999). Exemplifying this case are two major clades of South American herbivorous mammals: the xenarthrans, also represented in modern faunas, and the native ungulates (the group Meridiungulata of McKenna (1975)) that became completely extinct by the end of the Pleistocene. Both groups have received special attention in

part because of their relatively high diversity (together they represent around 60% of the non-primate terrestrial mammal faunas in the Tertiary of South America; Croft 2007) and because of the acquisition of hypsodonty (high-crowned dentition), particularly in notoungulates, within the endemic ungulates.

Hypsodonty has been a leading morphological trait to infer feeding ecologies of fossil mammals. This is justified by the fact that in modern ecosystems, guilds of grazing mammals are generally highly hypsodont (as defined by Janis 1988), whereas browsers have usually the opposite type of dentition in terms of crown height (brachydonty or low- crowned teeth; Damuth and Janis 2011). Thus, the relatively high-crowned teeth of notoungulates and most fossil sloths has led to the interpretation that they were grazers and to subsequently depict the environment where they lived as grasslands or open habitats (e.g., Patterson and Pascual 1968; Kay and Madden 1997). Moreover, hypsodont mammals have been documented earlier in South America than in North

America (phenomenon known as “precocious hypsodonty”), leading to the hypothesis that grass-dominated ecosystems appeared earlier in South America than in North

America (e.g., Stebbins 1981; Pascual and Ortiz-Jaureguizar 1990; MacFadden et al.

1994; Flynn and Wyss 1998; Kay et al. 1999; MacFadden 2006). However, while hypsodonty is certainly associated with diet in modern ecosystems (i.e., grasses) and that seems to be advantageously suited for processing grass rather than browse or a more generalized diet (Damuth and Janis 2011), it may also be a response to face other dental wear factors like ingesting soil and grit while feeding at ground level in open habitats, processing large amounts of food per day, or having high dental occlusal stresses (Strömberg 2006, Strömberg et al. 2010, Damuth and Janis 2011, Madden

2015). Therefore, interpreting herbivorous mammals as grazers or inhabitants of open environments just on the basis of their hypsodont nature, which has been the practice for a long time in the literature (e.g., Stebbins 1981; MacFadden 2000; Flynn and Wyss

1998), now seems to be open to other interpretations as well.

More recent studies reinforce a non-intrinsic link between hypsodonty and grazing habits in South American herbivorous mammals. For instance, isotopic signatures of highly hypsodont Pleistocene toxodonts show a latitudinal shift in their diets that ranged from C4 grazers at high-latitudes to C3 forest browsers in Amazonia

(MacFadden 2005). Additionally, microwear profiles of three hypsodont notoungulates

(previously depicted as grazers; e.g., Scott 1932) from the Middle Miocene of the Santa

Cruz Formation (Argentina) are those of typical browsers (Townsend and Croft 2008).

Finally, although microwear signatures of hypsodont notoungulates from Salla (Late

Oligocene of Bolivia) correspond to those of extant grazing ungulates, they could only be unambiguously interpreted in terms of jaw movements (Billet et al. 2009).

Most paleoecological studies of South American mammals have been focused on high/mid-latitude localities, with very little known from equatorial areas. This is mainly a result of a poorly sampled fossil record from this region. Until recently, the highly fossiliferous La Venta locality in Colombia (Kay and Madden 1997) was the only one of a few known in tropical South America. Fortunately, recent decades have brought studies of new paleontological localities from equatorial South America (e.g., Cozzuol

2006, Sanchez-Villagra and Aguilera 2006 ; Antoine et al. 2012, 2013; Tejada-Lara et al. 2015a; Salas-Gismondi et al. 2015). In Peru, paleontological expeditions to the

Amazonian region have been exhaustively carried out since 2004 by a joint effort of

Peruvian, American, and French teams, providing important data that are helping to piece together the phylogenetic and biogeographic history of South American faunas and allowing the application of new paleoecological approaches to address paleoecological questions.

Goals of this Contribution

 To infer the feeding ecology and resource partitioning among fossil mammals (sloths and native ungulates) inhabiting proto-Amazonia during the Middle Miocene using stable isotopes data (δ13C). Variation in the δ13C composition of fossil mammals teeth documented here should reflect similarities and differences in diet and/or habitat preference of these extinct species.

 To calculate the isotope enrichment between bioapapatite and diet (Ɛ*bioapatite-diet) in the two genera of living sloths (Bradypus and Choloepus). The Ɛ*bioapatite-diet is fundamental to interpreting the isotope data archived in the tissues of the fossil sloths in this study (see section 3.3).

 To describe the isotopic composition of modern mammals from the Amazon rainforest. This is justified because of the poor knowledge of the isotope ecology in modern Amazonia and because the most logical mammal community to compare proto-Amazonian mammals would be modern Amazonian mammals. The isotopic characterization of the mammal assemblage from Amazonia could have implications for characterizing closed canopy rainforests and feeding behaviors in the fossil record. To date, this only has been done using the isotope signal of mammal communities in Africa (Cerling and Harris 1999), despite differences in the structure of mammal communities on other continents.

Middle Miocene in Tropical South America and Study Sites

The Miocene in the area now occupied by Amazonia is characterized by two paleogeographic, ecologic, and faunistic regimes: the Pebas and the Acre systems

(e.g., Wesselingh and Salo 2006; Hoorn et al. 2010). The Pebas system is thought to have been established at the beginning of the Miocene and was dominated by a vast lacustrine complex in Western Amazonia, known as the Pebas megawetland. This system favored the existence of a rich and diverse aquatic fauna including a wide array of crocodylians and mollusks (e.g. Wesselingh et al. 2001, Wesselingh and Salo 2006,

Salas-Gismondi et al. 2015). The Pebas system was most likely a barrier for the dispersal of terrestrial faunas between northern and southern South America given the faunistic associations between coeval mammals from northern and southern areas of the continent (Tejada-Lara et al. 2015 a, b). A peak in the uplift of central and northern

Andes during the late Miocene, around 12 Ma, triggered the disappearance of this system and promoted the development of alluvial megafans, ultimately resulting in the establishment of the Amazon River system around 11 Ma (Hoorn et al. 2010, Figuereido et al. 2010). Following the disappearance of the Pebas megawetland, the modern

Amazon drainage starts with the Acre system (fluvio-tidal dominated wetland) which is thought to have lasted until around 7 Ma, when the modern Amazon River became fully established (Figuereido et al. 2009; Hoorn et al. 2010). The Acre phase probably reunited continental areas previously fragmented by the Pebas megawetland (Tejada-

Lara et al. 2015 a, b). Molecular phylogenies root the diversification of modern clades now distributed in northern South America to the Middle Miocene (Hoorn et al. 2010) while the fossil record indicates that the transition from the Pebas to the Acre system was a time of biotic turnover (Salas-Gismondi et al. 2015). Hence Miocene fossiliferous localities in this region are of fundamental importance to better understanding the history of modern biodiversity in Amazonia.

Fossiliferous localities in tropical South America are, however, rare, with La

Venta (Colombia) and Fitzcarrald (Peru) are the only two sites recognized at low- latitudes within the Laventan SALMA interval (Madden et al. 1997; Tejada-Lara et al.

2015a). Other localities, such as Urumaco (Venezuela) and Acre (Brazil) belong to the subsequent paleo-Orinoco and Acre ecosystems and correspond to the Huayquerian

SALMA (Sanchez-Villagra and Aguilera 2006; Cozzuol 2006). Quebrada Honda

(Bolivia), on the other hand, although Laventan in age, is located at mid-latitude and has closer faunal affinities to high-latitude localities in Argentina (Croft 2007). In terms of forest structure, a rainforest is assumed to have already been present in the Miocene, in the area now occupied by Amazonia, because of the similar humid climate conditions

(Kaandorp et al. 2005) and plant taxonomic composition (Pons and De Franceschi

2007; Jaramillo et al. 2010) with modern Amazonia (Hoorn et al. 2010).

The fossils analyzed here come from the northwestern Amazon Basin in Peru, from localities in the Iquitos and Fitzcarrald areas (Figure 1-1). The localities are assigned to a late Middle Miocene age and belong to the Pebas system, based on vertebrates, pollen, ostracod, and molluscan biozones (Wesselingh et al. 2006, Tejada-

Lara et al. 2015a; Salas-Gismondi et al. 2015). In Iquitos, most localities included (IQ

26, IQ 114, IQ 115) correspond to very fossiliferous lignitic bonebeds. IQ 125 is part of the upper Pebas Fm and does not correspond to the same depositional environment.

They are located in the Iquitos Arch, which corresponds to the modern northwestern

Amazonian foreland basin (Roddaz et al. 2005). Fossils from Fitzcarrald come from the

Inuya-Mapuya localities (DTC 32, DTC 37, IN 10, and Quebrada Grasa) which correspond to the less deformed part of the Fitzcarrald Arch (Figure 1-1). These localities are also correlated with the Laventan SALMA based on the presence of taxa defining the “Miocochilius assemblage zone” in La Venta, Colombia (Tejada-Lara et al.

2015a).

Analysis of freshwater bivalve shells recovered from the same localities in Iquitos yielded oxygen isotopic signatures consistent with modern Amazonian patterns of

precipitation implying that humid climatic conditions sufficient to sustain a rainforest ecosystem already existed in the region at that time (Kaandorp et al. 2005). Fossil plants from the same Middle Miocene localities in Iquitos belong to genera and/or families present today in modern Amazonia. Moreover, the fossil plant assemblage evokes lowland rainforest flora (“Hylaea Amazonia”) and “terra firme” forests of modern

Amazon delta and surroundings (Pons and De Franceschi 2007). Mean annual temperature (MAT) estimates based on δ18O from fossils of the coeval La Venta locality in Colombia (Honda Group, late Middle Miocene) indicate a range between 30-34°C

(Hoerner et al. 2013). If ecosystem components influencing isotopic signals of animals

(e.g., precipitation, plant composition, and temperature) were the same in the Miocene than in the present, should we expect fossil mammals from the same time-period to behave, isotopically, like modern mammals from tropical rainforests? Moreover, if the

Miocene forest structure was quite similar to that of today and if analogs of modern herbivore mammal guilds existed in the Miocene, we would expect overlaps in δ13C values of fossil and modern mammals from Amazonia.

Isotopic Analyses: Interest, Previous Studies, and Challenges

Isotopic analyses have become a frequently used technique to infer ecology of extinct animals due to the reliable patterns in which stable isotopes are distributed in organisms (Martínez del Rio and Wolf 2005). Literature on stable isotopes and animal paleoecology is abundant and deals with a broad variety of research questions including the reconstruction of dietary preferences (e.g. MacFadden 2000), the evaluation of resource partitioning within a community (e.g. Cerling et al. 2004), niche differentiation

(e.g. MacFadden et al. 2004), assignation of trophic levels (e.g. Bocherens et al. 1991), migratory behavior (e.g. Hoppe et al 1999), and osmoregulation (e.g. Roe et al. 1998).

Previous studies on stable isotopes on proto-Amazonia have used fossil mollusks to reconstruct seasonal rainfall patterns (e.g. Kaandorp et al. 2005). In other localities in modern tropical South America, isotopic studies include the inference of prehistoric human diets (e.g. Roosevelt 1980) and the stratification of δ13C in the dense forest by analyzing plants and air at different heights of the canopy (van der Merwe and

Medina 1991). This last phenomenon, also known as the “canopy effect”, is, by definition, a gradient in δ13C values from the forest floor to the canopy, with the most depleted δ13C values near the ground. If the canopy effect is present, the 13C depletion is expected to be passed along the foodchain, provided there are fauna feeding on plants on the lower strata of the canopy. These isotopic differences were observed in modern mammals from the Ituri forest (Democratic Republic of Congo, Africa), suggesting vertical niche differentiation within the canopy (Cerling et al. 2004). Because no other modern rainforest has been isotopically characterized (in both flora and fauna), the isotopic results of this single case study have been used to identify closed canopy habitats and feeding niches in the geological record (e.g. Secord et al. 2008).

Preliminary results on modern mammals from a rainforest of western Amazonia (Madre de Dios region, Peru) show different patterns of isotopic segregation suggesting different mammalian ecological behaviors, and a different isotopic mean for the mammal assemblage (see later in this work). These preliminary results motivated the author to delve deeper in the isotopic characterization of mammals from the Amazon region, which is the first attempt of this kind in this region.

Diagenesis, Rare Earth Elements Analysis, and Carbon Isotope Enrichment

Isotopic studies on fossil mammals are usually performed on dental enamel bioapatite because it is less susceptible to diagenetic alteration than are either dentine

or bone. Bioapatite in these materials differ in crystallite size and the degree of porosity and amount of organic content in these tissues determine recrystallization and influence diagenetic susceptibility (Kohn and Cerling 2002). During fossilization, enamel is least likely to have been diagenetically altered because it has large apatite crystals (hundreds of nanometers in length), is compact, and contains <5% of organic collagen. In contrast, bone has small apatite crystals (tens of nanometers in length), is porous, and high in organic content (collagen represents ~35% of unaltered bone). Dentine has intermediate characteristics, with a similar crystal size to bone but less collagen (~20%; see Kohn and Cerling 2002 for further details). Enamel is therefore preferred for isotopic analyses and the associated geochemical data are likely biologically meaningful.

Problematic cases arise when including xenarthrans, a group that includes mammals without teeth (anteaters) or, relevant to the present work, mammals with teeth but lacking dental enamel, e.g. sloths and armadillos (MacFadden et al. 2010).

Thus, despite the reliability and usefulness of stable isotope analyses to infer ancient ecologies, this technique has been only cautiously applied to sloths because of their lack of dental enamel. Toothed xenarthrans (sloths and armadillos) have, in lieu of enamel, an outer layer of hard dentine, analogous of other mammals’ enamel but different in mineralogy and composition (e.g. MacFadden et al. 2010). Because of that, for the few studies that have dealt with stable isotopes of xenarthrans, results have been equivocal (e.g. Kohn et al 2005; Ruez 2005). However, xenarthrans represent around 30% of non-primate terrestrial South American Tertiary mammal assemblages

(Croft 2007) and include large bodied herbivores. Therefore, the exclusion of this clade in paleoecological analysis will most likely result in misleading paleoenvironmental

reconstructions and in an inaccurate understanding of the synecology of Tertiary mammals in South America.

Because this work includes data from both fossil and modern sloths, two significant problems arise: (1) as mentioned previously, the reliability of sloths’ outer dentine in preserving the original biological signal of the animal, and (2) the untested fractionation factor between diet and dental tissue in this group, assumed to be the same as in other mammals (~14‰) in previous studies (e.g., Kohn et al. 2005; Ruez

2005; Czerwonogora et al. 2011).

REE Analysis

To address the first problem, I have used the rare earth elements index or “REE index”, a proxy proposed by MacFadden et al. (2010) to calculate relative diagenesis for a given tissue (e.g. enamel, dentine, bone) as normalized to bone for a given specimen.

The rationale of this proxy is that bone, being the tissue most prone to diagenesis, will give an estimate of the maximum expected alteration relative to other tissues (Zanazzi et al. 2007). Although there is debate about the suitability of this method to evaluate diagenesis due to the potential decoupling between isotopic and REE alteration (e.g.

Kohn and Cerling 2002; Fricke 2007), there is, at present, no unambiguous way to measure diagenesis. Still, trace element composition in fossil bones, including REE, reflects the early diagenetic environment and is useful as a taphonomic indicator

(Trueman 2007). Furthermore, although other techniques such as Fourier transform infrared (FTIR) spectroscopy or x-ray diffraction (XRD) could give insights about qualitative and quantitative mineralogy, these are inapplicable to these data because of the amount of sample needed (at least 1 g of sample just for qualitative mineralogy).

That means that even completely destroying some of the fossil teeth here analyzed

(which is unfeasible), it would not be possible to obtain a large enough sample.

Consequently, and pending the development of more efficient and reliable techniques that could be used together with REE data or other geochemical and sedimentological analyses, this work relies on the REE index proposed by MacFadden et al. (2010) as the proxy to assess diagenesis.

Carbon Isotope Enrichment

The carbon isotopic composition of an animal reflects its diet (Kohn and Cerling

2002). In order to be able to interpret the isotopic data archived in its tissues, however, we need to know the isotopic enrichment between diet and tissue (e.g. bioapatite). In mammals there is a several parts per mil enrichment in 13C of the bioapatite carbonate

(in bones or teeth) relative to the ingested diet (Ɛ*bioapatite-diet). Most studies on fossil mammals assumed an isotopic enrichment of ~14.1‰, at least for mammals larger than

5 kg (Cerling and Harris 1999). This enrichment factor was calculated on ruminants, and since ruminants are the dominant component of modern mammal faunas (at least in

Africa), this value has been extrapolated for most fossil mammals. In addition to studies on the African ungulates, other works have measured the isotope enrichment between enamel bioapatite and diet in voles (~11.5‰), rabbits (~12.8‰), and pigs (~13‰), taxa in which controlled feeding experiments are relatively easily performed (e.g. Cerling and

Harris 1999; Passey et al. 2005). In these groups, a range of ~5‰ enamel bioapatite- diet variation has been identified. These differences have been mostly attributed to differences in digestive physiology, i.e., methane production is a major determinant of variances among different clades (Passey et al. 2005). An increase in this Ɛ*bioapatite-diet variation would be expected in mammals with very different physiologies such as sloths, a group of particular concern in this work because they are included in the isotopic

analyses. There is to date no previous work dealing with this question which is therefore currently unknown.

Figure 1-1. Map of Peru with the location of the two sites where the fossil vertebrates used in this study were found, Iquitos (A) and Fitzcarrald (B). Mapped geological formations modified from Rebatta et al. (2006) and Wesselingh et al. (2006) (Iquitos), and Tejada-Lara et al. (2015) (Fitzcarrald).

CHAPTER 2 MATERIALS AND METHODS

Specimens of both fossil and modern taxa analyzed in this study are housed at the Department of Vertebrate Paleontology and the Department of Mammalogy of the

Museo de Historia Natural of the Universidad Nacional Mayor de San Marcos (MUSM) in Lima, Peru. Modern sloths used for the analysis of isotope fractionation came from the Zoologico de Huachipa (Lima-Peru) and from Tampa’s Lowry Park Zoo (Florida-

USA). Specific data for each specimen used in this work is provided in the Appendix.

Statistics were done with R (version 3.0.1) and PAST (version 2.17c) using both parametric (T-test, ANOVA) and non-parametric (Mann Whitney U, Kruskal Wallis) equivalent tests for significance. The probability levels of these equivalent tests for significance are noted in the text as “significantly different” when p-values are less than

0.05 for both tests; if p-values are different, these are reported separately.

Taxa and Teeth Analyzed for Isotope and REE Analyses

Isotopic analyses were performed in both modern and fossil taxa. This work includes fossil samples from four major clades of South American native mammals:

Astrapotheria (n=10), Toxodontia (n=26), Folivora (n=24), and Rodentia (n=3). Samples that are demonstrated to be diagenetically altered (based on REE index) were later removed from the analyses (see Table A-1). The selection of taxa was based on sample size availability and feasibility (e.g., teeth of very small rodent taxa were initially included but an insufficient amount of enamel was obtained preventing the extraction of enough

CO2). Folivores were subdivided in five groups: (1) Hapalopsinae/Megalonychidae, (2)

Mylodontidae non-Pseudoprepotherium (referred in the text as “big mylodontines”), (3)

Pseudoprepoterium, (4) Orophodontidae, and (5) Megalonychidae (big). Modern

samples include the following taxa: Mazama americana (n=3), Agouti paca (n=3),

Tapirus terrestris (n=6), Tayassu pecari (n=3), Choloepus sp. (n=3), Alouatta seniculus

(n=4), and Hydrochoerus hydrochaeris (n=2). Specific information about provenance, tooth sampled, and catalog numbers is provided in Table 3-1. When possible, samples were taken from the last molar to ensure that the isotopic signatures were reflecting the post-weaning diet of the animal (Boisserie et al. 2005).

Concerning the fossil material, because the fragmentary nature of most of the samples prevented a specific or generic identification, they have been grouped in higher taxonomic categories. In the case of astrapotheres and toxodonts, most of the samples were identified as Granastrapotherium sp. and as Pericotoxodon platignathus respectively. Although other non-diagnostic samples most likely represent the same taxa, they are referred as “astrapotheres” and “toxodonts”. The group referred to as

“Hapalopsinae/Megalonychidae” contains fossil material identified as hapalopsine, megalonychid, or indistinguishable between them based on isolated teeth. The group referred as “big mylodontines” includes samples of Urumacotherium and other isolated teeth of mylodontines of about the same size and clearly different from

Pseudoprepotherium. Finally, the group referred as “dynomids” included Drytomomys aequatorialis and/or teeth similar, but unassignable to, this genus given the fragmentary nature of the material. These current groups therefore likely do not necessarily reflect monophyly (e.g., Hapalopsinae/Megalonychidae). Potential interspecific ecologic variation has been assumed negligible, thereby taking only into consideration the intergeneric or suprageneric differences.

Rare Earth Elemental (REE) Analysis

In order to provide a measure of diagenesis of fossil sloth bone and teeth, I analyzed a total of 54 samples of bone (n=15), enamel (n=18), and outer dentine (n=21) of fossil sloths and other non-sloth fossil mammals for their REE signatures. REE values of outer dentine (fossil sloths) were compared to REE values of bone and enamel from the same locality. Ideally, the REE Index would be calculated on dental tissue and bone from the same specimen. However, because most of our samples consisted of isolated material, this was not always feasible. Instead, the REE Index was calculated using a single REEN bone value per locality.

About 0.1–0.5 mg of cortical bone, dentine, or enamel were removed from each fossil specimen using a Dremel™ rotary drill. The treatment of the samples followed the same protocol described in MacFadden et al. (2010). REE analyses were performed on a Thermo Finnigan ELEMENT2 Inductively Coupled Plasma Mass Spectrometer

(ICPMS) in the Department of Geological Sciences at the University of Florida. All measurements were performed in medium resolution with Rhenium used as internal standards. Quantification of results was done by external calibration using a set of gravimetrically prepared REE standards and SRM 1400 (bone ash) standard. The analytical error on the reported REE concentrations is better than 5% based on long- term analyses of USGS standards. Fourteen of the 15 REE (excluding Pm

[Promethium], Z=61) are analyzed during this procedure. In order to compensate for the

Oddo–Harkins even–odd abundance effect, the REE concentrations reported here are normalized to PAAS (Post-Archean Australian Shale; McLennan, 1989), and indicated by REEN.

Isotopic Analysis

Prior to sampling, teeth were cleaned of any superficial sediment. Isotopic analyses were done using at least 0.5 g of powdered enamel (for enamel bearing mammals) or outer dentine (sloths) collected from teeth using a Dremel® drill and carbide dental burrs. Both bulk and serial sampling was done: three fossil specimens

(toxodonts) and three modern specimens (tapirs) were analyzed for serial sampling.

Serial samples were collected from grooves drilled perpendicular to the growth axis of the tooth. All other specimens were sampled for bulk isotopic analyses.

Powdered samples were first treated with H2O2 to remove organic contaminants, followed by weak (0.1 N) acetic acid to remove any secondary carbonates. Because samples showed a strong reaction to the H2O2 the first step was repeated twice.

Samples were finally analyzed using a VG Prism mass spectrometer in the Department of Geological Sciences at the University of Florida.

Isotopic data were compared using the conventional delta (δ) for carbon (δ13C) where:

Rsample δ13C (parts per mil, ‰) = [( ) − 1] x 1000 Rstandard

and

R = 13C/12C for carbon

Although oxygen and nitrogen isotope data are also reported, I am not discussing them in this thesis because they are not part of the intended research questions.

13 Dental Tissue-to-Diet C Enrichment of Modern Sloths (Ɛ*bioapatite-diet)

The basic design for this experiment was to collect dental samples of dead sloths that were fed a homogeneous diet. In order for the dental samples to be a good recorder of the diet that they were eating, the dental tissue had to be mineralized during the period of controlled diet. The collection of samples for this experiment was not an easy task. After multiple failed attempts to recover dead sloths from different zoos, one dead specimen of Choloepus and two Bradypus from the Zoologico de Huachipa (Lima,

Peru), plus one more specimen of Choloepus from the Tampa’s Lowry Park Zoo

(Florida, USA) were finally obtained. Both zoos provided the foodstuffs the animals ate while alive. Specimens of Choloepus were both old adults, and although none of them were born in captivity they lived for more than five years in captivity. The same is true for one of the Bradypus specimens, which was an old female that lived for more than four years at the Huachipa Zoo under controlled feeding conditions. The second

Bradypus specimen was a sub-adult that was born at the Huachipa Zoo but died at 1.5 years of age. Although this individual was weaned before it died, given the dental ontogeny it is possible that its teeth archived a pre-weaning isotope signal.

The Choloepus specimens had mixed diets consisting of pellets, greens, fruits, and even quinoa and boiled eggs for the specimen from Peru. Dried samples were milled in a Spex 67000 liquid nitrogen mill to homogenize them. These were then analyzed using the same instrument described for the fossil samples. The two specimens of Bradypus came from the Huachipa Zoo and were fed exclusively on sprouts of Ficus elastica (rubber plant). With exception of the specimen from Tampa, from which only one tooth was provided, the complete cadavers of the other three specimens from the Huachipa Zoo were donated to the osteological collection of the

Department of Vertebrate Paleontology of the Natural History Museum in Lima. They are therefore available for future replications of this experiment.

Because of the small size of the sloths’ teeth, no more than 0.1 g of powdered outermost dentine was obtained for all the four specimens. Powdered samples were obtained as described in section 2.3 for the fossil specimens. Because of the limited sample amount, an abbreviated treatment was performed as follows: samples were left for three hours in H2O2, rinsed three times with distilled water, then put in CH3COOH

(0.1 N) for half an hour, rinsed three times again with distilled water followed by a fourth rinse with methanol, and finally dried. About 50% of each sample was lost during this treatment, leaving just enough sample for analysis in the mass spectrometer. Because the entire sample of the Tampa specimen was lost during this treatment, I decided to repeat the experiment with the remaining tooth. The same was done to the specimen

(JTL-2014-2-11), which was the only one available at the time, in order to observe differences in the δ13C between treated and untreated samples.

The isotope enrichment (Ɛ*) value was calculated by following Passey et al.

(2005), which consists of two parts:

(1) The fractionation factor (α) between diet and animal tissue:

푅퐴 1000 + 훿퐴 훼퐴−퐵 = = 푅퐵 1000 + 훿퐵

(2) The isotope enrichment (Ɛ*) between diet and animal tissue:

∗ 휀 퐴−퐵 = [훼퐴−퐵 − 1]1000

CHAPTER 3 RESULTS

REE

Results of REEN concentrations for all four localities (IQ 26, IQ 114, DTC 32, and

IN 10) and tissues (enamel, outer dentine, bone) of our pooled sample are shown in

Figure 3-1. Plots are compiled from data presented in the Appendix. Because the timescale of REE uptake into bone post mortem is relatively short in geological terms, on the order of 103 years (Trueman and Tuross 2002) it is reflecting early diagenetic environment of burial. This implies that bones fossilized together in the same depositional environment should take up the same trace element signal. Results of this work (Fig 3-2) show a quite similar REE uptake behavior between the four localities analyzed being the median REEN values of all samples around 10 PAAS.

Consequently, they suggest that there are relatively similar porewater geochemical conditions for all four localities, especially among the two localities from Iquitos and among the two localities in Fitzcarrald.

To assess relative diagenesis for dental tissue (enamel and dentine) normalized to bone (the most altered tissue), the REE Index was calculated for 38 enamel/bone

(n=17) and outer dentine/bone (n=21) pairs from the four localities where fossil sloths included in this study were collected. The mean REE Index of enamel (0.07) is significantly less (p=0.004, Mann-Whitney; although p=0.08, t-test) than that of outer dentine (0.26), indicating that, as expected, enamel is less altered than outer dentine

(Fig 3-3). However, most of the samples resulted in REE Index values of less than 0.1 or 0.2 (Fig 3-4), below the REE Index limit (0.35) considered reliable (MacFadden et al.

2010), and are not significantly different from corresponding enamel values. Most of the

outer dentine samples show nonsignificant differences with enamel, or fall below the

REE index limit considered reliable. Considering that enamel is widely acknowledged to preserve biochemical meaningful data, it is therefore assumed here that the signal preserved in the sloths’ outer dentine (with low REE indices) is biologically meaningful and therefore we will rely on the isotopic values recorded in the teeth. The three samples whose REE indices were above 0.5 were eliminated from any subsequent analysis because they were interpreted to be highly altered.

Isotope Enrichment

Isotope data for bioapatite and food are summarized on Table 3-2. Dental bioapatite values for the Choloepus specimens gave a ε*bioapatite-diet of 8.61‰ ± 0.99 whereas the ε*bioapatite-diet result for the Bradypus specimens were 16.72‰ ± 1.59. These results suggest that the ε*bioapatite-diet between Bradypus and Choloepus are significantly different, and both of them are also non-overlapping with other mammals for which isotope enrichment was calculated. Moreover, Bradypus and Choloepus plot on opposite sides of the spectrum of ε*bioapatite-diet of mammals. Passey et al. (2005) found that ε*bioapatite-diet of cattle were at the upper limit of that spectrum (14.6‰) and voles at the lower limit (11.5‰), with pigs (13.3‰) and rabbits (12.8‰) in between these values.

Inter-species variation in ε*bioapatite-diet are attributed to differences in digestive physiology, with the methane production being a major determinant (Passey et al.

2005). Therefore, if the fraction of ingested carbon lost as methane is the most important factor influencing ε*bioapatite-diet, then cattle’s fractional methane production is, in ascending order, greater than pigs, rabbits, and voles. Assuming this is correct, and ruling out other potential factors influencing ε*bioapatite-diet (such as preferential digestion

of isotopically different dietary components in animals with mixed diets), then Bradypus’ methane production would be greater than that of cattle, and that of Choloepus lower than voles, in proportion to their body masses.

Sloths are foregut fermenters and, like advanced ruminants, have compartmentalized stomachs (Stevens 1988). Sloths have been described as having stomachs consisting of three major divisions (Stevens 1988) or four divisions

(Montgomery and Sunquist 1978). Although studies on sloths’ digestive physiology are based on Bradypus, the stomach of Choloepus is described to be somewhat similar but

“less complicated than that of Bradypus” (Stevens 1988, pp. 59), differing mainly in the size of the first compartment and arrangement of internal septa (Flower 1872).

Compartmentalized stomachs and foregut fermentation (observed in both sloths and ruminants) is an adaptive response to a diet composed exclusively of leaves. It is considered the most derived of the mammalian digestive anatomies and physiologies

(Chivers and Langer 1994). The end-products of microbial metabolism during fermentation of plant cellulose consist of fatty-acids, carbon dioxide, and methane. The concentration of fatty-acids in the stomach of Bradypus was found to be “hardly different” from other foregut fermenters, although the rate of fermentation is considerably slower (Foley et al. 1995). The condition in Choloepus is currently not known.

The high ε*bioapatite-diet value obtained for Bradypus is in agreement with the morphological and physiological similarities in its digestive system and with the food types ingested with that of advanced ruminants, such as cattle. Although methane production has not been calculated in Bradypus, our results indicate that it is a greater

methane producer, in proportion to its body mass, than cattle. The morphology of the stomach and digestive physiology of Choloepus has been less studied and generally extrapolated from studies on Bradypus. Known differences between Bradypus and

Choloepus lie in their minimal thermal conductance and basal rate of metabolism, both aspects lower in the former than in the latter (McNab 1985). Choloepus is known for having a broader dietary predilection (under wild and captivity conditions) including higher concentrations of digestible energy than Bradypus. Because Choloepus includes food of better nutritional quality (including fruits and insects), and consequently incorporates less leaves than Bradypus in its diet, we would expect a lower methane production, more similar to that of generalist herbivores. Our results, support this scenario because Choloepus show a much lower ε*bioapatite-diet value than Bradypus, and actually to any other mammal for whom these values have been determined.

Isotopic Structure (δ13C) of Mammals from Modern Amazonia

Knowing the isotopic structure of the mammal assemblage from modern

Amazonia, as well as the isotopic variation within the existing C3 consumers, would provide a baseline to interpret the isotopic composition of fossil mammals from proto-

Amazonia. To date, the only modern mammal assemblage characterized isotopically from a closed canopy forest is the Ituri Forest in Africa (i.e. Cerling et al. 2004). Isotopic data from this modern rainforest have been used to infer canopy structure in fossil sites

(e.g. Secord et al. 2008), albeit differences in mammalian community structure between

African and South and Central American rainforests also have been recognized (Louys et al. 2011). The taxa selected here for this analysis include: Mazama americana (red brocket), Cuniculus paca (lowland paca), Tapirus terrestris (Brazilian tapir), Tayassu pecari (white-liped pecari), Choloepus sp. (two-toed sloth), Alouatta seniculus (red

howler monkey), and Hydrochoerus hydrochaeris (capybara). The selection of mammal taxa from Amazonia was driven by differences in body sizes, dentition, chewing mechanics and availability. These differences are preserved in the fossil record and are expected to also reflect the different niches they have occupied.

The ε*bioapatite-diet in Choloepus was calculated in this study as 8.61‰. For the other mammals (excluding Alouatta) we are assuming an ε*bioapatite-diet of 13.7‰ which is based on a 65/35% composition of species ruminants and non-ruminants in modern ecosystems (e.g. Secord et al. 2008). In the case of Alouatta, the only primate included, an ε*bioapatite-diet of 12‰ is assumed which accounts for the 1-2‰ less in primates’

ε*bioapatite-diet compared to ungulates (Sponheimer and Cerling 2014). The results obtained from the recent mammals from Amazonia are summarized in Table 3-1. Figure

3-5 shows the results of δ13C obtained from the dental bioapatite. The δ13C values of the plants the animals would have consumed were calculated from the ε*bioapatite-diet

13 mentioned above. In order for the δ Cbioapatite results of Alouatta and Choloepus to be comparable to the other mammals with ε*bioapatite-diet of 13.7‰ we have applied a correction of 1.7‰ and 5.09‰ respectively (although the raw values are also shown in

Figure 3-5).

The corrected values range from (-18.81‰ to -13.24‰) with a mean of -16.11‰

13 for the whole mammalian community. The δ Cplants inferred for the plants would range between (-32.51‰ to -26.94‰) with a mean of -29.81‰, which is consistent with values obtained for tropical rainforests (e.g. Van der Merwe and Medina 1989; Cerling et al.

2004). ANOVA performed on corrected values reveal significant differences between

Mazama and Choloepus, Agouti and Choloepus, Tapirus and Choloepus, Tapirus and

Tayassu, and Tapirus and Hydrochoerus. Alouatta only shows significant differences with Choloepus indicating different feeding preferences between them and preventing resource competition of these taxa living in the same forest stratum.

Mazama americana (red brocket deer), Cuniculus paca (lowland paca or agouti), and Tayassu pecari (white-lipped pecari) are generalist herbivores, which accounts for

13 the non-significant differences among their δ Cbioapatite values (means of -16.39‰,

-16.59‰, and -15.29‰ respectively). They all include fruits and leaves in their diets

(Asquith et al. 1999, Beck-King et al. 1999, Gayot 2004, Mayer and Wetzel 1987).

Cuniculus and Tayassu also incorporates seeds and tubers, whereas Tayassu consumes mushrooms, worms, and insects, occasionally including small vertebrates

(such as frogs, lizards, snakes, eggs of birds and turtles) and carrion (Mayer and Wetzel

1987).

Tapirus terrestris (Brazilian tapir) is preferentially a nocturnal browser. Although known as a generalist herbivore, it seems to prefer specific forage plants such as mombins (Anacardiaceae), huito (Genipa americana, a species of Rubiaceae endemic to southern Peru, and moriche palm (Aracaceae) (Nowak 1999). This might explain why it shows significant differences with Tayassu, another generalist browser. The

13 δ Cbioapatite of Tapirus is the most depleted of the species sampled with a mean value of

-17.81‰.

Hydrochoerus hydrochaeris (capybaras) are only found in areas where water is easily accessible: flooded grasslands are a favored habitat, as are marsh edges and lowland forests where grass is plentiful and there is water year-round. Capybaras feed mainly on grasses and aquatic plants, but bark and fruit are consumed occasionally

13 (Dunston and Gorman 1998). The δ Cbioapatite of Hydrochoerus (mean of -14.62‰) overlaps with almost all the other species analyzed showing only significant differences with Tapirus.

The two species inhabiting the top canopy layer of the forest included here are

Alouatta cuniculus (red howler monkey) and Choloepus sp. (two-toed sloth), which

13 show significant differences in their corrected mean δ Cbioapatite values (-13.7‰ and

-16.17‰ respectively). Both species are described as primarily folivorous, occasionally including other plant parts such as fruits and/or flowers (e.g. Devore 1965; MacDonald

1985; Gilmore et al. 2001). These dietary similarities are in fact very coarse, because

13 according to their δ Cbioapatite signatures, they are exploiting different food resources, and in so doing, minimizing ecological competition.

Isotopic Signatures of Fossil Mammals from Proto-Amazonia: δ13C

Table 3-3 shows all the δ13C and δ18O values for the fossil mammal species studied, whereas descriptive statistics are reported in Table 3-4. Results reported exclude samples that appeared to be diagenetically altered based on the REE Index analysis (MacFadden et al. 2010). This work aims to reveal differences in the feeding habits of the fossil mammals, but because we are comparing δ13C of specimens coming from different localities we first need to be sure that results reflect differences among taxa, and not among localities. The only taxon recorded in almost all localities (IQ 125,

DTC 32, DTC 37, and IN 10) was Toxodontia. Results of both ANOVA and Kruskal-

Wallis tests based on toxodont specimens from these localities showed non-significant differences. Similarly, based on results from megalonychid sloths, localities IQ 114 and

IQ 26 were found to be not significantly different.

13 The non-sloth mammal with the most depleted δ Cbioapatite values is the toxodont,

13 with a mean δ Cbioapatite of -12.64‰ and values ranging between -11.37‰ and

13 -13.76‰. Astrapotheres, on the other hand, showed the least depleted δ Cbioapatite

13 values of the non-sloth mammals analyzed with a mean δ Cbioapatite of –10.24‰ and

13 values ranging between -8.89‰ and -11.04‰. The mean δ Cbioapatite obtained for the dynomids was intermediate between toxodonts and astrapotheres (-11.44‰) with values ranging between -9.07‰ and -13.56‰. Given the small sample size and because the values obtained span such a large range, conclusions based on the results

13 of the dynomid are not warranted. The mean δ Cbioapatite of these three clades give a signature of -12.23‰ ± 1.18, placing these animals in a C3 browsing context, but with more positive values than that obtained for the modern mammals analyzed from

Amazonia.

The results of the δ13C for the fossil sloths show non-significant differences between Pseudoprepotherium and the group including hapalopsines/megalonychids

(groups with the least depleted δ13C). In contrast, these two groups show significant differences with big mylodontines (group with the most depleted δ13C values). Although the δ13C results of the one sample of orophodontid tooth and the one big megalonychid are shown, given the impossibility to perform statistical analyses, these samples were excluded from further discussion. Nonetheless, if they are not outliers and their δ13C are normally distributed, then orophodontids would be more similar in terms of feeding habits to hapalopsines/megalonychids and Pseudoprepotherium, whereas the “big megalonychid” would be closer to “big mylodontines” such as Urumacotherium (Figure

3-6).

Because our studies on Bradypus and Choloepus showed no phylogenetic signal, nor direct correlation between body mass and the ε* between bioapatite and diet, the δ13C values of the fossil sloths can be equally corrected using the isotope enrichment obtained for Bradypus (16.72‰) or the isotope enrichment for Choloepus

(8.61‰). Their final δ13C values, as expected, would be very different depending upon which ε* is used (Figure 3-6).

Indeed, if we assume that the fossil sloths experienced an ε*bioapatite-diet similar to

13 that of Choloepus, then the mean δ Cbioapatite for big mylodontines would be of -7.94‰ ±

1.28, for hapalopsines/megalonychids -2.76‰ ± 0.91, and -2.59‰ ± 0.99 for

13 Pseudoprepotherium. These results would place the δ Cbioapatite signature of hapalopsines and Pseudoprepotherium as that of typical C4 grazers, and the

13 δ Cbioapatite signature of big mylodontines like that of a mixed feeder. On the other hand,

13 if we assume them to have the ε*bioapatite-diet of Bradypus, then the mean δ Cbioapatite signature of mylodontines would be -16.05‰ ±1.28, for hapalopsines/megalonychids-

10.87‰ ± 0.91, and for Pseudoprepotherium -10.7‰ ± 0.99. These values correspond to animals feeding on C3 plants. Moreover, the δ13C signature of big mylodontines would overlap the δ13C values of modern Amazonian mammals, such as generalist herbivores Agouti, Mazama or Alouatta.

As mentioned in the introduction, the vegetation structure, climate, and environmental characteristics retrieved from different fossil proxies, seem to support the existence of a tropical rainforest in Amazonia during the Middle Miocene. This interpretation, however, would be at odds with the results obtained had the fossil sloths had an ε*bioapatite-diet similar to that of Choloepus. On the other hand, the isotopic signal of

the fossil sloths is consistent with that of a C3 rainforest if they had the ε*bioapatite-diet of

Bradypus. Consequently, we favor the hypothesis that fossil sloths had an ε*bioapatite-diet similar to that of Bradypus, and their δ13C results will be interpreted based on the assumption that they had an isotope enrichment of 16.72‰ compared to their diets.

When all the six fossil taxa are compared (after correcting the data of fossil sloths with the ε* of Bradypus), ANOVA shows significant differences between astrapotheres and toxodonts, and between mylodontines versus all the other taxa. Kruskall-Wallis, on the other hand, shows additional significant differences between toxodonts and

Pseudoprepotherium and Hapalopsines, whereas it indicates non-significant differences between mylodontines compared with astrapotheres and dynomids.

Figure 3-1. Rare earth element (REEN) signatures for the four localities containing fossil sloths analyzed in this study.

Figure 3-2. Plots of median REEN concentrations for enamel, outer dentine, and bone for each locality.

Figure 3-3. Plots of median REEN concentrations for enamel, outer dentine, and bone for all four localities.

Figure 3-4. Histogram showing distribution of REE Index values for the 38 enamel/bone (n=17) and outer dentine/bone (n=21) pairs from the four localities with fossil sloths. Data from Appendix 2.

Table 3-1. Isotopic signatures (δ13C and δ18O) of dental bioapatite of modern mammals from Peruvian Amazonia. Samples of modern taxa come from the Department of Mammalogy (DM-MUSM) or the Department of Vertebrate Paleontology (DPV-MUSM) of the Natural History Museum of the Universidad Nacional Mayor de San Marcos (MUSM). Abbreviations: l=left, r=right, M=upper molar, m=lower molar.

Sample code Catalog Species Material δ13C δ18O number JT-A2013-1 DM MUSM Mazama americana l m3 -15.39 -4.8 15470 JT-A2013-2 DM MUSM Mazama americana l m3 -16.23 -5.39 15469 JT-A2013-3 DM MUSM Mazama americana l m3 -17.54 -7.23 15448 JT-A2013-4 DM MUSM Agouti paca l m3 -16.32 -5.93 15710 JT-A2013-5 DM MUSM Agouti paca l M3 -17.01 -6.92 15603 JT-A2013-6 DM MUSM Agouti paca l m3 -16.44 -4.43 15695 JT-A2013-7 DM MUSM Tapirus terrestris l m3 -18.81 -4.61 23076 JT-A2013-8 DM MUSM Tapirus terrestris l m3 -16.69 -4.61 15540 JT-A2013-9 DM MUSM Tapirus terrestris l m3 -18.17 -6.30 15546 JT-A2014- DM MUSM Tapirus terrestris r M2 -16.67 -5.40 8A-D 15549 JT-A2014- DM MUSM Tapirus terrestris - -18.44 -5.45 9A-D 15545 JT-A2014- DM MUSM Tapirus terrestris r m3 -18.09 -6.07 10A-D 15546 JT-A2013-10 DM MUSM Tayassu pecari l m3 -16.02 -5.06 15482

Table 3-1. Continued. Sample code Catalog Species Material δ13C δ18O number JT-A2013-11 DM MUSM Tayassu pecari l m3 -15.14 -5.62 15486 JT-A2013-12 DM MUSM Tayassu pecari l m3 -14.70 -5.54 15480 JT-A2013-13 DM MUSM Choloepus sp. l m3 -18.84 -2.49 11079 JT-A2013-14 DM MUSM Choloepus sp. l m3 -18.33 -2.29 6111 JT-A2013-15 - Choloepus sp. r m3 -19.19 -3.48 JT-A2014-1 DM MUSM Alouatta seniculus r m3 -19.74 -4.74 15572 JT-A2014-2 DM MUSM Alouatta seniculus l m3 -17.55 -2.22 15561 JT-A2014-3 DM MUSM Alouatta seniculus r m3 -16.64 -3.3 5364 JT-A2014-4 DM MUSM Alouatta seniculus l m3 -17.56 -2.5 15551 JT-A2014-5 DM MUSM Hydrochoerus r m3 -13.71 -7.91 2648 hydrochaeris JT-A2014-6 - Hydrochoerus M2 -15.53 -4.75 hydrochaeris

Table 3-2. Isotopic signatures of the sloths and their food analyzed to calculate the ε*diet-enamel. “P” denotes pretreated sample, “U” denotes untreated sample.

A. Samples of modern sloths Sample Sample Provenance Material Type δ13C ε* code JTL 2014-2- Choloepus Huachipa M2 P -13.6 7.61 01 sp. Zoo JTL 2014-2- Choloepus Lowry Park lower U -13.45 9.61 14 sp. Zoo molariform JTL 2014-2- Bradypus Huachipa m2 P -15.16 17.75 02 sp. Zoo JTL 2014-2- Bradypus Huachipa lower U -15.37 17.52 11 sp. Zoo molariform (juvenile) JTL 2014-2- Bradypus Huachipa lower P -17.93 14.88 11 sp. Zoo molariform (juvenile)

B. Samples of food Sample Material Provenance δ13C δ15N code JTL 2014- Food for Choloepus from Huachipa Huachipa -21.05 4.23 2-12 Zoo (mix of greens, fruits, quinoa, Zoo pellets, boiled egg) JTL 2014- Food for Bradypus from Huachipa Huachipa -32.33 1.65 2-13 Zoo (Ficus elastica leaf sheaths) Zoo JTL-2014- Food for Choloepus from Tampa’s Lowry Park -22.84 1.52 2-15 Lowry Zoo (pellets for primates + Zoo mix of fruits and greens)

Figure 3-5. Carbon isotope data from modern mammals of Amazonia (Madre de Dios, Peru). Values for Alouatta and Choloepus have been corrected according to their estimated isotope enrichments, but raw values are shown in light grey. The data used here are from Table 3-1.

Table 3-3. δ13C and δ18O of tooth enamel and outer dentine of fossil mammals from Miocene proto-Amazonia, e=enamel, od= outer dentine.

Lab MUSM Taxa Locality Material δ13C δ18O code 2006-4 Astrapotheria IQ 114 e, tooth -10.54 -5.4 2007-01 NA Astrapotheria IQ 114 e, tooth -10.48 -4.23 2012-2 NA Astrapotheria IQ 114 e, canine -11.04 -4.03 2012-16 989 Astrapotheria IQ 26 e, M3 -8.89 -3.56 2006-2 NA Toxodontia IQ 125 e, tooth -12.66 -4.98 2006-3 NA Toxodontia IQ 125 e, tooth -12.38 -4.35 2006-10 NA Toxodontia IQ 125 e, tooth -12.41 -3.82 2006-11 NA Toxodontia IQ 125 e, tooth -12.38 -5.65 2006-12 NA Toxodontia IQ 125 e, tooth -12.12 -6.06 2006-13 NA Toxodontia IQ 125 e, tooth -12.68 -4.44 2006-14 NA Toxodontia IQ 125 e, tooth -12.66 -5.57 2006-15 NA Toxodontia IQ 125 e, tooth -13.35 -4.57 2006-17 NA Toxodontia IQ 125 e, tusk -12.84 -3.32 2012-19 NA Toxodontia IQ 125 e, tooth -13.37 -4.85 2012-17 NA Toxodontia DTC 32 e, canine -12.57 -4.62 2013-22 1500 Toxodontia DTC 32 e, P4 izq -13.76 -4.88 2013-23 922 Toxodontia DTC 32 e, m1 izq -12 -1.3 2013-24 1498 Toxodontia DTC 32 e, P2/P3 -13.32 -5.67 2013-36 NA Toxodontia DTC 32 e, tooth -11.68 -2.95 2013-27 1502 Toxodontia IN 10 e, I1 izq -13.51 -4.36 2013-28 NA Toxodontia IN 10 e, i1 izq -12.85 -3.86 2013-29 1503 Toxodontia IN 10 e, I2 der -12.8 -0.68 2013-32 1501 Toxodontia DTC 37 e, p2/3 izq -12.97 -2.01 2013-33 1506 Toxodontia DTC 37 e, I2 izq -12.9 0.01 2013-34 NA Toxodontia DTC 37 e, tooth -12.98 -4.8 2013-35 NA Toxodontia Qda e, tooth -11.97 -3.17 Grasa 2012-18 NA Toxodontia DTC 14 e, m1/2 -12.57 -3.21 2014-12 2386 Toxodontia IQ 114 e, tooth -11.37 -3.16 2014-13 2396 Toxodontia IQ 114 e, M3 -12.02 -4.18 2008-03- NA Pseudoprepotherium IQ 115 od, m1/2 -7.41 -5.04 OD-1 & 2 2012-6 1924 Pseudoprepotherium IQ 114 od, r m4 -9.03 -2.86 2012-7 1923 Pseudoprepotherium IQ 114 od, r M5 -7.65 -3.09 2013-14 1922 Pseudoprepotherium IQ 114 od, m3 -7.08 -4.26 2013-15 2261 Pseudoprepotherium IQ 114 od, m4 -6.33 -4.58 2014-11 1782 Pseudoprepotherium IQ 114 od, m1 -8.6 -4.04

Table 3-3. Continued. Lab MUSM Taxa Locality Material δ13C δ18O code 2012-5 660 Megalonychidae/ IQ 114 od, tooth -7.47 -2.2 Hapalopsinae 2012-8 1925 Megalonychidae/ IQ 114 od, tooth -7 -3.3 Hapalopsinae 2012-14 2260 Megalonychidae/ IQ 114 od, tooth -8.18 -3.09 Hapalopsinae 2008-05- 2257 Megalonychidae/ IQ 26 od, tooth -8.24 -3.52 OD-1 & Hapalopsinae 2 2012-11 2255 Megalonychidae/ IQ 26 od, tooth -7.21 -2.26 Hapalopsinae 2012-12 1747 Megalonychidae/ IQ 26 od, m4? -8.64 -3.85 Hapalopsinae 2012-10 2254 Megalonychidae/ IQ 26 od, tooth -6.66 -3.56 Hapalopsinae 2013-6 2258 Megalonychidae/ IQ 26 od, tooth -9.36 -4.1 Hapalopsinae 2013-26 904 Megalonychidae DTC 32 od, M3 -13.02 -3.88 2012-4 659 Orophodontidae IQ 114 od, M4? -7.92 -3.36 2013-25 985 Mylodontidae DTC 32 od, tooth -13.74 -5.93 2013-30 938 Mylodontidae IN 10 od, tooth -11.55 -7.31 2013-31 947 Mylodontidae IN 10 od, M5 r -13.8 -6.95 2013-3 NA Dynomidae DTC 32 e, incisor -13.56 -9.27 2014-15 2397 Dynomidae IQ 114 e, incisor -9.07 -5.08 2014-25 NA Dynomidae IQ 26 e, incisor -11.68 -4.02

Table 3-4. Descriptive statistics for δ13C of fossil mammals. Fossil sloths have been corrected (-3.02‰) based on the isotope enrichment of Bradypus.

δ13C (‰) Taxon n Mean SD Range Astrapotheria 4 -10.24 0.93 -8.89 to -11.04 Toxodontia 25 -12.65 0.58 -11.37 to -13.76 Dynomidae 3 -11.44 2.25 -9.07 to -13.56 Mylodontinae “big” 3 -16.05 1.28 -14.57 to -16.82 Hapalopsinae/ 8 -10.87 0.91 -9.68 to -12.38 Megalonychidae Pseudoprepotherium 6 -10.7 0.99 -9.35 to -12.05

Figure 3-6. Isotopic signatures (δ13C) of the fossil mammals analyzed. Isotope data on fossil sloths have been corrected using the isotope enrichment obtained for Bradypus (16.72‰, in dark green), or the isotope enrichment for Choloepus (8.61‰, in light green).

CHAPTER 4 DISCUSSION

Madre de Dios (Peru, Amazonia) and Ituri (Congo, Africa): Two Different Closed- Canopy Forests

In the work about recents mammals from the Ituri forest, nine genera of ungulates were grouped by the stratum they occupy in the canopy: the subcanopy, the canopy, and the clearings or gaps (Cerling et al. 2004). The mammals feeding in the subcanopy (Okapia johnstoni, Hylochoerus meinertzhageni, and Neotragus batesi) possessed very negative δ13C values, significantly lower than mammals feeding on plants from the other two habitats within that forest. The isotopic structure of the Ituri mammalian community shows a wide range of δ13C signatures (11.9‰) and includes subcanopy mammals with distinctly negative signatures, which has been used as a parameter to identify closed-canopy forests in the fossil record (e.g. Secord et al. 2006).

The results obtained here for Amazonian mammals are different from those of the Ituri forest (Figure 4-1), with no indication of mammals feeding in the subcanopy and half the range of δ13C variation observed in Ituri (5.57‰). These results have great implications because they indicate that the absence of sub-canopy mammals is by no means indicator of absence of closed-canopy forests. In Amazonia, plants with δ13C values comparable to subcanopy vegetation in Ituri do exist (e.g., Van der Merwe and Medina

1989, 1991). However, modern Amazonian mammals would be using forest resources in a different fashion than mammals in Africa, given the observed absence of such negative signals. Although we must acknowledge, given our limited sample, the possibility that we have overlooked existing habitats in Amazonia, the exact same pattern (i.e. no mammals feeding in subcanopy and relatively narrow range of δ13C) was found in a closed-canopy forest from Venezuela (Secord et al. 2010).

The more negative δ13C mean of the Ituri mammalian community is due to the extreme negative δ13C values obtained for the subcanopy mammals. However, only one specimen per mammal taxon was used to define this habitat and the most negative taxon, the dwarf antelope Neotragus batesi, δ13C= -25.6‰, would had fed on plants with

δ13C signatures more negative than any plant measured in that forest or any other

(Cerling et al. 2004). In summary, this subcanopy habitat is affecting the range of δ13C variation of the Ituri forest. However, because this habitat is defined by only three specimens (one per taxon), subcanopy mammals from this forest should be reanalyzed to confirm or correct the δ13C signatures of mammals supposedly feeding in this forest stratum.

Feeding Ecology of Fossil Mammals from Proto-Amazonia

Results from δ13C indicate that fossil mammals from proto-Amazonia were feeding on C3 plants. In Fig 3-7 there is clear overlap of δ13C values between big mylodontines (such as Urumacotherium) and several of the modern mammals herein analyzed. The highly depleted δ13C signatures of these sloths (equivalent to those of

Tapirus, Tayassu, Cuniculus, and Mazama) correspond to generalist herbivores living deep inside the forest. Their δ13C signatures indicate they could have easily been inhabitants of modern Amazonia, feeding as most of extant Amazonian mammals from a wide array of plant types, such as leaves, fruits, barks, or seeds.

Toxodonts are the fossil animals with the second most depleted δ13C values.

Although significantly more enriched in 12C than modern Amazonian mammals, some of the obtained values were consistent with the δ13C variation observed in Choloepus.

Toxodonts like Pericotoxodon were most likely mixed feeders, eating an array of

dissimilar plants with a broad isotopic range, in their δ13C signatures. Proto-Amazonian toxodonts have δ13C signatures inconsistent with a life inside the deep forest (i.e. enriched in 12C). They would have inhabited the margins of the forest where tall vegetation is more scattered and where the resident plants, which receive higher light intensities than plants inside the forest and/or using a non-recycled CO2, have more positive δ13C values. Plants consumed by the toxodonts would have had δ13C signatures between -25.07‰ and -27.46‰, equivalent to values obtained for cassava leaves (Manihot esculenta) growing in a sunny clearing inside the upper Amazon Basin

(Van der Merwe and Medina 1991).

The groups of fossil mammals with the least depleted δ13C values were

Pseudoprepotherium, hapalopsines/megalonychids, and astrapotheres. Their relatively positive δ13C values (compared with the modern mammals from Amazonia) indicate these were not closed canopy inhabitants, but instead could have been living in an open canopy. Indeed, the signatures corresponding to the plants they must have been feeding on range from -22.59‰ to -26.08‰. Although terrestrial plants within this range are not easily found in the literature, similar values have been reported in C3 grasses from modern Amazonia (Medina et al. 1999) and in trees and C3 grasses from an open canopy in China (e.g. Ehleringer et al. 1987). Interestingly, these δ13C signatures are more common in aquatic plants such as those that constitute the diet of manatees in the springs of Florida (Ames et al. 1996). Moreover, similar δ13C signatures are reported from extant and fossil manatees (MacFadden et al. 2004). However, unlike the narrow range of variation in our samples, the incorporation of plants with extremely different

δ13C values, makes the δ13C range of variation of manatees enormous. Could proto-

Amazonian astrapotheres and sloths (such as Pseudoprepotherium or those included in our group of hapalopsines/megalonychids) have inhabited marshes and swamps of the

Pebas megawetland and fed on aquatic plants? Astrapotheres have long been considered associated with amphibious habits (e.g. Riggs 1935; Webb 1978) whereas the extraordinarily rich and diverse fossil history of sloths includes the aquatic sloth

Thalassocnus (De Muizon et al. 2004). Aquatic plants might have represented an abundant and exploitable resource for these animals given that most of the area now occupied by the Amazon rainforest was long-covered by the Pebas megawetand.

Amazonia vs Proto-Amazonia Canopy Structure

Attempts to infer the canopy structure of such a vast region like proto-Amazonia based on a tiny portion of the mammal community is tenuous because the number of species is not high enough to detect the potential inhabitants of all the layers and niches of the canopy. Nevertheless, the assemblage of all the available data, including that presented in the present paper, contributes to the knowledge of the elusive history of proto-Amazonia.

Previous contributions suggest that western proto-Amazonia was a tropical rainforest during the Miocene, with a vegetative landscape and environmental conditions similar to today. This interpretation is based on the archetypal traits defining modern tropical rainforests, such as precipitation patterns and seasonal variation

(Kaandoorp et al. 2005), basic plant taxonomic composition (Pons and De Franceschi

2007; Jaramillo et al. 2010), and temperature (Hoerner et al. 2013). In isotopic terms, closed-canopy forests are defined by depleted δ13C values and the recognition of the canopy effect. In this last respect, the data presented here partially support this reconstruction. The only δ13C data that support the interpretation of a closed canopy

forest is that of the big mylodontines (e.g. Urumacotherium), with δ13C values as depleted as modern Amazonian mammals. The other taxa discussed are above the mean of modern Amazonian mammals. Some of the δ13C signatures of proto-

Amazonian toxodonts (such as Pericotoxodon) coincide with some individuals of

Choloepus, the modern Amazonian mammals most enriched in 12C. Equivalent values in plants are found in clearings within the rainforest. Astrapotheres,

Pseudoprepotherium, and hapalopsines/megalonychids were definitively not closed- canopy inhabitants because their δ13C signatures do not exist in that type of ecosystem in the present. Instead, they could have lived in riparian areas feeding on 12C enriched aquatic plants, in an analogue feeding ecology to manatees with C3 diets from Florida.

Unfortunately, neither aquatic plants nor manatees from Amazonia have been analyzed isotopically as published in the literature.

An important fact that should not be overlooked in any attempt to reconstruct

Miocene proto-Amazonia is the presence of the Pebas megawetland, a complex system of swamps, marshes, estuarine areas, and dysoxic lakes that covered more than one million km2 (Wesselingh et al. 2001; Wesselingh and Salo 2006; Salas-Gismondi et al.

2015). These sets of aquatic environments might have been predominant in some areas of this biome, which is evidenced by the extensive lacustrine deposits of the Pebas

Formation from the Iquitos area (e.g. Wesselingh et al. 2001; Wesselingh and Salo

2006). These bodies of water most likely fragmented the forested areas and provided more open environments than those observed in modern Amazonia. These open patches, deprived of dense and tall vegetation, might have allowed for the penetration of more light and facilitated the mixing of the air, making more 12C available from the

atmospheric CO2 for the photosynthesis of the plants, therefore increasing their general mean δ13C, and consequently, of those animals feeding on them. In this ecosystem, recording the canopy effect would be less likely and more positive isotopic signatures

(such as those here obtained) would probably be broadening the observed range of

δ13C variation in modern tropical rainforests.

Salas-Gismondi et al. (2015) observed high endemism in the crocodyilian community inhabiting the swamps of the Pebas Formation in the Iquitos area. They proposed that the localities IQ 26 and IQ 114, the same localities where some of the samples herein analyzed originated, represent aquatic environments different from others in coeval areas within the same Pebas system. Because our samples come from a set of coeval localities (Figure 1-1), differences in the carbon isotope data could also reflect differences in the habitats within the same biome. For instance, all the samples of big mylodontines, the only group with δ13C values consistent with a closed-canopy forest, come from the Fitzcarrald area. On the other hand, the groups with the least depleted δ13C signatures, i.e. those of astrapotheres, Pseudoprepotherium, and hapalopsines/megalonychids, all come from deposits interpreted to represent anoxic lakes and marshes in the Iquitos area (Salas-Gismondi et al. 2015).

Figure 4-1. Comparison of mammal community structure between an Amazonian forest (Madre de Dios, Peru) and the Ituri forest (Congo, Africa).

Figure 4-2. Comparison of δ13C values of modern and fossil mammals from western Amazonia. Fossil mammals are shown in sepia.

CHAPTER 5 SUMMARY AND CONCLUSIONS

Stable isotope analysis is a valuable proxy capable of revealing feeding ecologies and habitat occupation, particularly when morphological and ecological data are lacking in both fossil and modern mammal communities and ecosystems. The isotopic data presented here are unique in providing direct and strong evidence for resource partitioning in fossil mammals from tropical South America and the identification of different habitats existing in Miocene proto-Amazonia. One of the most important outcomes of this project was the successful inclusion of fossil sloths in isotopic analysis. However, fossil sloth data must be evaluated by carefully scrutinizing the results and any potential for diagenesis. In this sense, new and more efficient techniques to confidently measure diagenesis will be critical in advancing the knowledge of the ecology of organisms currently excluded from these type of analysis.

The inclusion of fossil sloths in this work required the estimation of the previously unknown isotope enrichment between diet and bioapatite (ε*). Our a priori assumption that sloths, being mammals with very distinct and peculiar physiologies, could have an isotope enrichment different than other mammals was confirmed. However, finding that the two genera of living sloths, Bradypus and Choloepus, had widely divergent results in the spectrum of known isotope enrichments was unexpected. The results showed that

Bradypus has an ε* of 16.72‰ ± 1.596, above the mean of ε* estimated for medium sized terrestrial herbivores (~14.1‰), whereas Choloepus was placed well below this value with an ε* of 8.61‰ ± 0.998. Differences in isotope enrichment have been attributed to differences in digestive physiology, namely methane production. If this is the case, then Bradypus would be a higher methane producer than Choloepus and the

former even higher, in proportion to its body mass, than advanced ruminants. This inference is supported by differences in the stomach morphology and feeding preferences between Bradypus and Choloepus. Living sloths are foregut fermenters and the stomach of Bradypus is compartamentalized and as derived as those of advanced ruminants. The stomach in Choloepus has not been well studied but is described as “less complicated” than that of Bradypus. It is known that Bradypus has a more restricted diet than Choloepus, incorporating food of poorer nutritional quality which might account for its higher methane production. Choloepus, on the contrary, feed on more nutritious foods, including leaves, fruits, and even insects in its diet (e.g.,

Gilmore et al. 2001).

These results lead to the following conclusions: (1) there is no phylogenetic signal in the isotope enrichment of mammals, and (2) there is no correlation between isotope enrichment and body mass, but potentially with methane production. Although body mass and methane production might certainly be correlated in some cases, the facts that the two living sloths, Bradypus and Choloepus, having pretty much the same body mass and ecology, yet have so different isotope enrichments indicates that this correlation is not always meet. From the first consequence it is also deduced that fossil sloths could have had the isotope enrichment of Bradypus, that of Choloepus, or in between that broad range between these two genera. Such a wide spectrum of variation has not been identified before within any mammalian clade and implies at least the same wide array of ecological and physiological strategies for fossil relatives. This physiological versatility might be crucial to understand the extreme diversification

(morphological, phylogenetic, and spatial) attained by this clade.

Numerous sources of evidence support the existence of a C3 tropical rainforest for the Miocene in proto-Amazonia (e.g., Kaandorp et al. 2005, Pons and De

Francheschi 2007). The δ13C values of the astrapotheres and toxodonts analyzed here also indicate a C3 type of ecosystem. The isotope data of fossil sloths are consistent with these results if they had an isotope enrichment equivalent to that of Bradypus.

Because of all the associated evidence supporting a C3 tropical rainforest, this hypothesis is favored here. With this assumption, mylodontines such as

Urumacotherium might have had a feeding ecology similar to generalist herbivorous mammals of modern Amazonia (such as Cuniculus, Tayassu, or Mazama) and lived deep inside the closed canopy. Toxodonts such as Pericotoxodon, with δ13C signatures bordering the upper edge of observed variation of modern Amazonian mammals, were most likely mixed feeders and might have been marginal inhabitants of the forest.

Finally, fossil mammals with the most positive δ13C signatures (tropical astrapotheres, hapalopsines/megalonychids, and Pseudoprepotherium) were feeding on plants with

δ13C signatures comparable to aquatic vegetation. Considering the prevailing environmental conditions in proto-Amazonia, this work proposes that these taxa could have inhabited the marginal aquatic settings.

Based on seven taxa of herbivorous mammals analyzed here, the mean δ13C of this fossil mammal assemblage is significantly different (more positive) than that obtained for those of modern Amazonia. These differences might reveal a broader range of habitats within the proto-Amazonian biome in the Miocene, including closed- canopy forests fragmented by open non-forested areas probably representing the set of aquatic ecosystems that characterized the Pebas megawetland.

APPENDIX RARE EARTH ELEMENTS (REE) ANALYSIS

REE Data

Table A-1. REE data (normalized to PAAS) for specimens analyzed during this study. Uncat= uncatalogued specimen, od=outer dentine, b=bone, enamel.

Taxon MU Mate Samp La Ce Pr Nd Sm Eu Gd Tb Dy Ho Er Tm Yb Lu ∑ REE SM rial le# norm IQ 26

Megalonyc 225 od 2013- 3.5801 5.5568 7.0529 7.7073 8.9037 8.5818 7.4602 8.1497 7.9435 7.0835 6.9228 7.3832 8.0280 7.6548 102.00 hidae/ 4 1 7136 4189 8397 7186 6921 9134 2644 8023 647 7728 869 2516 5612 6477 9211 Hapalopsin ae Megalonyc 225 od 2013- 0.8525 1.0865 1.2668 1.4072 1.6640 1.7013 1.6195 1.8104 2.0026 2.0093 2.1284 2.3572 2.7045 2.8004 25.411 hidae/ 5 2 5819 0768 5624 7181 2361 0378 6568 971 8174 1855 9805 5827 2651 902 36 Hapalopsin ae Megalonyc 174 od 2013- 0.8899 1.3604 1.5816 1.7256 1.9747 1.9431 1.7695 1.9232 2.0068 1.9514 2.0438 2.2466 2.6182 2.6823 26.717 hidae/ 7 3 3642 3345 5597 4311 0458 7579 9311 8511 1018 2395 739 0085 8395 6405 7844 Hapalopsin ae Hapalopsin 225 od 2013- 5.7594 9.0847 11.560 12.538 14.737 14.274 12.507 13.998 14.047 12.392 12.087 12.738 13.949 13.489 173.16 ae juvenil 6 4 9436 4958 9713 0545 8982 9014 2279 2804 111 6575 4827 7013 2576 6387 6427 Megalonyc 225 od 2013- 1.5772 2.4449 2.9329 3.0574 3.5196 3.4214 3.0362 3.2605 3.2543 3.0693 3.1170 3.3334 3.8108 3.8707 43.706 hidae/ 7 5 4949 3886 4196 1186 5018 2125 8393 62 1486 1533 473 728 2808 3888 1768 Hapalopsin ae Megalonyc 225 od 2013- 3.5606 4.4685 5.1156 5.1557 5.4591 5.4176 5.0126 5.3953 5.4068 5.2176 5.2802 5.6734 6.3419 6.4230 73.928 hidae/ 8 6 3859 581 8398 6845 5617 9939 83 0922 9502 8181 083 8313 8452 7621 8259 Hapalopsin ae Megalonyc 137 b RB20 3.3519 3.7572 4.5373 5.6764 8.0719 11.859 12.361 12.227 12.550 11.046 10.526 9.4205 8.3963 7.4633 121.24 hidae/ 7 14-2 5726 655 1234 7069 1911 1064 3959 5766 2643 9142 1593 3827 175 9302 659 Hapalopsin ae Megalonyc 174 b RB20 16.330 21.648 23.236 28.202 40.748 60.580 59.121 57.567 57.288 48.862 46.050 40.876 35.932 31.170 567.61 hidae/ 2 14-5 6476 0544 6281 4086 428 83 1822 087 5961 4773 9439 9309 3536 2349 6803 Hapalopsin ae Toxodontia 239 e RE20 7.0902 6.9662 8.2165 10.372 14.765 21.773 24.386 24.606 26.462 24.593 23.936 21.409 18.961 17.176 250.71 (juvenile) 4 14-1 8829 1763 4938 155 3025 6645 2079 6558 09 6509 0116 2099 5786 2558 5838 Toxodontia 239 b RB20 15.168 16.347 18.698 23.335 32.466 47.886 53.197 52.670 55.844 51.300 49.558 44.362 39.033 35.574 535.44 (juvenile) 4 14-1 2858 4827 3602 9607 1896 9718 1206 0052 9093 1958 0239 4321 3721 1419 3452 Astrapoher 658 e RE20 2.6413 2.6188 3.0168 3.4737 4.4181 5.8876 6.2242 5.4958 5.0134 4.1596 3.8873 3.3149 2.8714 2.4888 55.512 ia 14-4 8753 01 4145 9056 5125 8091 3927 7013 8523 9929 1544 5556 3786 8372 5392

Table A-1. Continued Taxon MU Mate Sam La Ce Pr Nd Sm Eu Gd Tb Dy Ho Er Tm Yb Lu ∑ REE SM rial ple# norm Astrapoheria 658 b RB20 10.871 8.1608 8.6110 10.244 11.858 17.036 21.024 17.934 17.756 16.795 16.123 13.569 11.646 10.823 192.45 14-4 9662 2219 043 9983 5229 0745 9712 5922 728 004 5649 884 3896 7116 8234 Dinomyidae unc e RE20 2.6994 2.4494 2.8319 3.5633 4.5722 6.9136 7.7218 6.9743 7.1497 6.6899 6.4581 5.6356 4.8714 4.3964 72.927 at 14-3 2442 425 2027 45 2 5 2639 0909 6273 667 3228 2469 6964 3488 5286 (P- 200 8- 40) Dinomyidae unc e RE20 0.5176 0.4665 0.5730 0.7430 0.9528 1.3803 1.6874 1.4582 1.4570 1.3604 1.2892 1.1158 0.9266 0.8301 14.758 at 14-6 3708 673 0951 535 1607 7727 6931 3636 3136 4904 4842 9383 3786 5116 5781 (P- 200 6- 83) IQ 114

Orophodontid 659 od 2013- 1.9594 3.8099 5.3098 5.8346 7.1943 6.7934 5.6690 6.4012 6.0430 5.2249 4.9545 5.0158 5.3326 4.8612 74.404 ae cf. 7 7219 0868 2891 7841 6962 5655 014 7961 143 1189 2836 9828 6828 5992 2764 Octodontobra dys Megalonychi 660 od 2013- 1.2546 1.7924 2.2037 2.4738 3.1334 3.1386 2.7660 3.1563 3.1150 2.7934 2.7396 2.9105 3.1908 2.9790 37.647 dae/ 8 1562 2934 947 8178 4948 1462 8556 5706 4486 9078 8615 6334 1745 939 9246 Hapalopsina e Pseudoprepo 192 od 2013- 2.0958 3.6705 4.9119 5.3058 6.5164 6.3387 5.5191 6.2424 6.3730 5.9319 5.9471 6.4051 7.1950 7.1941 79.647 therium 4 9 8765 8912 8572 3568 7339 9779 2972 7213 161 5816 2096 0008 2922 0965 5054 Pseudoprepo 192 od 2013- 0.9049 1.6031 2.0877 2.4029 3.0479 3.0937 2.6822 3.1269 3.2883 3.1286 3.1839 3.4822 3.9770 3.9239 39.933 therium 3 10 8782 0541 208 2177 5783 4078 258 5025 2781 0296 4601 0607 8276 8171 7578 Megalonychi 192 od 2013- 1.8850 3.6429 5.1335 5.6801 7.3062 6.9957 6.0748 7.0410 7.0726 6.4604 6.4395 6.9852 7.7939 7.6986 86.210 dae/ 5 11 0788 4387 4764 9452 4427 6851 1075 8121 7483 3962 9648 4146 5647 5725 1648 Hapalopsina e Megalonychi 225 od 2013- 22.691 42.969 58.050 64.800 79.608 80.785 65.381 75.918 83.048 76.594 75.583 80.610 89.748 87.654 983.44 dae/ 9 12 181 9787 5916 6097 1696 8037 1786 5347 6141 6863 9526 6701 4057 5467 6923 Hapalopsina e Megalonychi 226 od 2013- 2.4498 3.9637 5.2594 5.9818 7.3943 7.3847 6.4922 7.5119 7.8397 7.2004 7.2326 7.8650 8.6888 8.5452 93.810 dae/ 0 13 0066 6374 2497 8344 2794 9945 0353 2717 2309 33 6878 6817 7548 2435 1238 Hapalopsina e Pseudoprepo 192 od 2013- 0.4634 0.7367 0.9503 1.0739 1.3204 1.2898 1.1256 1.2431 1.3336 1.2068 1.2610 1.3210 1.5342 1.4198 16.280 therium 2 14 6641 8809 9264 9915 3877 5219 8808 4832 4837 5652 1078 6317 7933 5382 4856 Pseudoprepo 226 od 2013- 1.4637 2.3610 3.0712 3.3249 3.9800 3.8296 3.4529 3.8256 4.0231 3.6616 3.7172 3.8416 4.1567 3.9218 48.631 therium 1 15 5506 0995 4002 3109 1388 1688 442 1334 83 6637 323 2413 3001 4994 4102 Pseudoprepo 238 od RO20 9.5660 12.325 15.208 18.417 25.766 34.722 35.484 33.086 32.182 27.048 25.040 21.928 18.822 15.995 325.59 therium 3 14-10 6487 2965 0386 0014 5695 3082 9646 7091 382 1635 7428 0617 9579 9674 5228 Pseudoprepo 178 od RO20 2.4446 2.2924 2.6350 3.0680 3.8075 5.1315 5.6227 4.8785 4.8047 4.4734 4.5214 4.1254 3.7508 3.5507 55.107 therium 2 14-11 9332 6753 9955 9656 1571 4091 8004 2857 1159 7023 7895 9383 9464 9535 5668 Octodontobra 239 b RB20 19.395 24.318 29.762 36.064 48.875 65.665 70.275 64.643 61.676 52.380 48.085 40.995 35.426 30.374 627.94 dys 5 14-8 1614 8645 498 631 5073 6691 2234 9597 485 1231 5235 6519 2243 6953 0217 Pseudoprepo 178 b RB20 6.8650 6.7861 7.6981 8.9012 11.051 14.577 15.867 14.012 13.845 12.453 12.331 11.199 10.058 9.2593 154.90 therium 2 14-11 5184 0958 5549 1444 6521 4845 0918 339 618 9233 0333 6247 3307 093 6938

Table A-1. Continued Taxon MU Mate Samp La Ce Pr Nd Sm Eu Gd Tb Dy Ho Er Tm Yb Lu ∑ REE SM rial le# norm G. snorki unc e 2013- 1.6294 2.3974 2.8866 2.9761 3.4614 3.3361 3.0140 3.2700 3.4323 3.1758 3.2606 3.5505 3.9536 3.9392 44.283 at 16 5577 6073 4096 1568 3693 9241 9256 7202 1612 2192 1168 0741 6665 581 6489 (P- 200 6- 40) G. snorki unc e 2013- 1.1132 1.7136 2.0005 2.1472 2.5328 2.3884 2.1342 2.2968 2.3848 2.1681 2.2690 2.4306 2.8153 2.7604 31.155 at 17 0534 7358 272 4543 812 0579 6563 8071 7425 8056 4373 6092 5101 8977 6851 (P- 200 6- 89) G. snorki 988 e 2013- 0.8594 1.2238 1.4001 1.4924 1.7346 1.6719 1.5211 1.6479 1.7443 1.6030 1.6716 1.7881 2.0442 1.9947 22.397 18 9141 0579 1264 5247 1675 4031 3311 8988 4328 8716 8797 6844 2764 3125 7881 G. snorki unc e 2013- 1.1374 1.8325 2.1525 2.2971 2.6767 2.4325 2.1055 2.2487 2.2709 1.9979 2.0143 2.1794 2.4667 2.3289 30.141 at 19 4089 2744 3459 1692 2795 1022 9805 7187 2499 5621 0134 5444 6931 2126 5555 (P- 200 6- 36) G. snorki unc e 2013- 0.8338 1.3087 1.5020 1.6071 1.9064 1.7826 1.6061 1.7289 1.7310 1.6106 1.6773 1.8223 2.1288 2.1228 23.369 at 20 6772 032 2179 7905 1775 0791 6632 0155 4177 5564 6016 4763 7539 9287 0388 (P- 200 6- 15) G. snorki unc b RB20 20.851 23.689 28.139 34.447 47.134 61.161 64.402 57.938 54.778 46.014 42.246 36.533 31.409 27.714 576.46 at 14-14 5282 0458 8195 4991 4154 7109 9558 061 6502 5136 5765 5383 44 793 2547 (P- 200 6- 15) Toxodontia 238 e RE20 2.2560 2.9452 3.7440 4.4188 6.5348 8.4434 7.9180 7.4723 6.6775 5.0340 4.4849 3.8324 3.3331 2.6874 69.782 6 14-12 1395 4664 6886 4088 9518 2 4957 1039 9545 1211 2632 6667 1571 4884 4106 Toxodontia 239 e RE20 0.4362 0.5537 0.7363 0.9378 1.4693 2.0631 2.0237 1.9830 1.9336 1.6088 1.4629 1.2832 1.0927 0.9539 18.539 6 14-13 8713 3685 9819 4131 3482 0091 4936 7013 9 5974 8246 2963 8214 4884 0115 Toxodontia 239 b RB20 16.721 20.143 25.358 32.304 46.963 64.365 69.048 65.196 64.467 55.820 51.133 43.827 37.705 32.829 625.88 6 14-13 2678 8478 0717 2358 3621 0345 5781 2156 805 775 9905 5037 8361 3791 5903 Dinomyidae 239 e RE20 2.3403 2.9239 3.6101 4.4623 6.2240 8.4948 8.9778 8.3474 8.1791 7.0103 6.5006 5.7410 4.9544 4.3527 82.119 "Olenopsis" 7 14-15 6937 8009 9207 9091 7036 8 2296 1818 7045 1786 3579 5185 3429 8605 5202 sp. large Dinomyidae 239 b RB20 13.036 16.123 19.308 23.907 33.719 47.782 51.052 48.845 49.326 42.939 39.890 35.756 30.758 26.648 479.09 "Olenopsis" 7 14-15 0361 9001 6755 8718 597 2691 4412 339 4348 1443 4102 9284 1346 9628 6145 sp. large DTC 32

Mylodontid 985 od 2013- 1.6745 2.6604 2.8551 2.8577 3.1693 3.1336 2.4545 2.4445 2.2586 1.9670 1.8898 1.7593 1.7756 1.6024 32.503 ae 25 4611 8552 4116 7794 658 2737 9773 9683 1143 498 6478 7635 5006 6019 1511 (Urumacoth erium) Megalonyc 904 od 2013- 1.1974 1.2973 1.3230 1.3533 1.4118 1.3599 1.2900 1.3036 1.3567 1.3216 1.4034 1.4329 1.5594 1.5573 19.168 hidae (big) 26 5062 1837 9919 4666 4239 0787 6402 1873 8634 8775 6557 9437 3038 0077 313 Megatheroi 981 b RB20 8.4422 6.6670 6.7514 7.6297 9.2303 12.796 14.120 12.076 11.701 10.506 10.013 8.5638 7.1389 6.4340 132.07 dea 14-18 1921 322 3556 6056 9054 0736 6311 8935 715 5893 4702 4444 3786 2791 3021

Table A-1. Continued Taxon MU Mate Samp La Ce Pr Nd Sm Eu Gd Tb Dy Ho Er Tm Yb Lu ∑ REE SM rial le# norm Megalonyc unc b RB20 9.6408 9.4285 8.5823 10.017 12.475 19.445 20.313 18.046 18.057 15.958 14.883 12.409 10.208 8.7617 188.22 hidae/ at 14-20 4266 9029 3114 7967 1561 2955 903 1325 3714 0212 8253 2148 2596 3023 847 Hapalopsin (F- ae 200 5- 58) Pericotoxo 150 e 2013- 0.0220 0.0262 0.0251 0.0258 0.0264 0.0322 0.0248 0.0255 0.0256 0.0259 0.0272 0.0295 0.0320 0.0338 0.3827 don 0 22 1109 6572 4927 5148 6081 6599 5091 4026 8759 8339 1056 1286 5007 7604 1603 Pericotoxo 922 e 2013- 0.0972 0.1085 0.0849 0.0840 0.0794 0.0879 0.0838 0.0838 0.0852 0.0905 0.0944 0.0994 0.1005 0.1052 1.2855 don 23 6432 8725 7231 5615 9786 8718 2107 8361 6219 7128 8615 3502 3972 3157 9567 Pericotoxo 149 e 2013- 0.0851 0.1147 0.0989 0.1030 0.1077 0.1162 0.1102 0.1164 0.1194 0.1190 0.1200 0.1251 0.1303 0.1341 1.6008 don 8 24 5837 0475 3282 6075 9169 4549 4111 682 3298 9932 8696 6642 5641 4301 8829 Pericotoxo 149 b RB20 21.159 22.333 21.680 24.839 30.146 42.470 43.045 35.638 32.359 26.856 23.734 18.044 13.893 11.495 367.69 don 3 14-17 115 0383 8277 7168 5043 9927 4187 7403 7023 9889 3951 1284 8132 4837 8865 IN 10

Mylodontid 938 od 2013- 1.1890 1.2535 1.2194 1.2725 1.2432 1.1903 1.3172 1.2193 1.2625 1.1753 1.1833 1.0217 1.0058 0.9015 16.455 ae 30 7712 9865 6642 2177 5336 5019 7158 4327 2155 8628 4028 1167 2244 6799 2325 (Scelidothe riinae) Mylodontid 947 od 2013- 1.1008 1.0322 1.4801 1.5859 1.7554 1.6953 1.6535 1.6983 1.7916 1.6269 1.6420 1.6113 1.7209 1.6407 22.035 ae 31 8872 1924 559 2027 9722 0119 2313 8563 1215 0198 6591 9477 9725 845 6479 Pericotoxo 150 e 2013- 0.5732 1.2839 1.2805 1.4437 1.8692 1.9222 1.8548 1.9479 1.8836 1.5772 1.3686 1.0665 0.9793 0.7422 19.793 don 2 27 3684 3202 5342 7929 2102 2727 9393 0021 6039 0433 982 1669 4677 4142 4118 Pericotoxo unc e 2013- 0.0947 0.1349 0.1478 0.1548 0.1707 0.1715 0.1594 0.1711 0.1813 0.1721 0.1775 0.1926 0.2078 0.2167 2.3535 don at 28 0412 6935 4872 4029 61 7734 2875 9058 8721 5368 0696 3065 119 112 2175 (F- 200 5- 18) Pericotoxo 150 e 2013- 0.2705 0.2687 0.2174 0.2162 0.1781 0.2604 0.3032 0.3309 0.4077 0.4417 0.4511 0.4343 0.3944 0.3670 4.5422 don 3 29 3196 0909 9229 709 6597 8775 431 551 0721 6134 0649 4993 6634 4847 9594 Toxodontia 148 b RB20 45.663 34.055 57.689 69.816 91.623 123.46 150.45 127.51 112.64 90.265 71.729 48.010 32.632 25.268 1080.8 0 14-22 0199 5814 581 1382 4213 0844 2428 4782 3701 2533 2804 0074 2168 4279 2468 Notoungula unc b RB20 11.666 8.9309 8.7465 9.6914 11.011 14.911 17.816 14.542 13.833 12.130 11.049 8.7868 6.9143 6.0174 156.04 ta at 14-23 212 3755 4972 9669 7839 1391 6918 9701 1745 4682 3614 7901 8143 9302 9539 (F- 201 4- 23) Modern e A201 0.0010 0.0012 0.0012 0.0015 0.0023 0.0184 0.0065 0.0030 0.0025 0.0021 0.0018 0.0018 0.0019 0.0016 0.0475 sample 3- 7479 8391 7814 3528 8554 4785 1948 3091 2714 9298 8889 2857 814 7489 (Bos 17G taurus)

REE Indices

Table A-2. REE Indices

Taxon MUMS # Materia Sample Locality ∑ REE REE Index l # norm Megalonychidae/Hapalopsinae 2254 od 2013-1 IQ 26 102.00921 0.3472371 1 8 Megalonychidae/Hapalopsinae 2255 od 2013-2 IQ 26 25.411357 0.0864997 4 2 Megalonychidae/Hapalopsinae 1747 od 2013-3 IQ 26 26.717784 0.0909467 4 7 Hapalopsinae juvenil 2256 od 2013-4 IQ 26 173.16642 0.5894548 7 2 Megalonychidae/Hapalopsinae 2257 od 2013-5 IQ 26 43.706176 0.1487748 8 9 Megalonychidae/Hapalopsinae 2258 od 2013-6 IQ 26 73.928825 0.2516521 9 4 Astrapoheria 658 e RE2014- IQ 26 55.512539 0.1889635 4 2 Dinomyidae uncat (P- e RE2014- IQ 26 72.927528 0.2482437 2008-40) 3 6 5 Dinomyidae uncat (P- e RE2014- IQ 26 14.758578 0.0502378 2006-83) 6 1 8 Orophodontidae cf. 659 od 2013-7 IQ 114 74.404276 0.1509648 Octodontobradys 4 3 Megalonychidae/Hapalopsinae 660 od 2013-8 IQ 114 37.647924 0.0763869 6 1 Pseudoprepotherium 1924 od 2013-9 IQ 114 79.647505 0.1616032 4 4 Pseudoprepotherium 1923 od 2013-10 IQ 114 39.933757 0.0810248 8 2 Megalonychidae/Hapalopsinae 1925 od 2013-11 IQ 114 86.210164 0.1749187 8 5 Megalonychidae/Hapalopsinae 2259 od 2013-12 IQ 114 983.44692 1.9953946 3 7 Megalonychidae/Hapalopsinae 2260 od 2013-13 IQ 114 93.810123 0.1903389 8 2 Pseudoprepotherium 1922 od 2013-14 IQ 114 16.280485 0.0330327 6 9 Pseudoprepotherium 2261 od 2013-15 IQ 114 48.631410 0.0986721 2 8 Pseudoprepotherium 2383 od RO2014 IQ 114 325.59522 0.6606263 -10 8 8 Pseudoprepotherium 1782 od RO2014 IQ 114 55.107566 0.1118121 -11 8 8 G. snorki uncat (P- e 2013-16 IQ 114 44.283648 0.0898506 2006-40) 9 6 G. snorki uncat (P- e 2013-17 IQ 114 31.155685 0.0632142 2006-89) 1 8 G. snorki 988 e 2013-18 IQ 114 22.397788 0.0454446 1 8 G. snorki uncat (P- e 2013-19 IQ 114 30.141555 0.0611566 2006-36) 5 3 G. snorki uncat (P- e 2013-20 IQ 114 23.369038 0.0474153 2006-15) 8 2 Toxodontia 2386 e RE2014- IQ 114 69.782410 0.1415871 12 6 5 Toxodontia 2396 e RE2014- IQ 114 18.539011 0.0376152 13 5 9

Table A-2. Continued. Taxon MUMS # Material Sample Locality ∑ REE REE Index # norm Dinomyidae "Olenopsis" sp. 2397 e RE2014- IQ 114 82.1195202 0.16661891 large 15 Mylodontidae (Urumacotherium) 985 od 2013-25 DTC 32 32.5031511 0.14172878 Megalonychidae big 904 od 2013-26 DTC 32 19.168313 0.08358272 Pericotoxodon 1500 e 2013-22 DTC 32 0.38271603 0.00166882 Pericotoxodon 922 e 2013-23 DTC 32 1.28559567 0.00560579 Pericotoxodon 1498 e 2013-24 DTC 32 1.60088829 0.00698061 Mylodontidae (Scelidotheriinae) 938 od 2013-30 IN 10 16.4552325 0.02660777 Mylodontidae 947 od 2013-31 IN 10 22.0356479 0.03563119 Pericotoxodon 1502 e 2013-27 IN 10 19.7934118 0.03200554 Pericotoxodon uncat (F- e 2013-28 IN 10 2.35352175 0.0038056 2005-18) Pericotoxodon 1503 e 2013-29 IN 10 4.54229594 0.0073448

Samples averaged for bone REE values For IQ 26 ∑ REE norm Average (REE norm) Megalonychidae 1377 121.24659 293.773876 Hapalopsinae 1742 567.616803 Astrapotheria 658 192.458234 For IQ 114 Octodontobradys 2395 627.940217 492.85835 Pseudoprepotherium 1782 154.906938 Astrapotheria uncat (P-2006-15) 576.462547 Toxodontia 2396 625.885903 For DTC 32 Megatheroidea 981 132.073021 229.333452 Megalonychidae/Hapalopsinae uncat (F-2005-58) 188.22847 Pericotoxodon 1493 367.698865 For IN 10 Toxodontia 1480 1080.82468 618.43711 Notoungulata uncat (F-2014-23) 156.049539

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BIOGRAPHICAL SKETCH

Julia Tejada is a Peruvian biologist. She grew up surrounded by books and always felt a strong passion by apparently dissimilar academic fields such as literature and sciences. After a long and arduous deliberation she decided to study biology, a decision she has not regretted.

She studied biological sciences, with especial focus in zoology, at the

Universidad Nacional Mayor de San Marcos, in Lima- Peru. As an undergraduate student, she discovered paleontology and spent her free time preparing and studying fossils at the Department of Vertebrate Paleontology at the Natural History Museum in

Lima, Peru. Her association with this institution gave her a strong background in field work, vertebrate anatomy, and fossil preparation, and allow her to interact and collaborate with many paleontologists from around the world. Her field work experience includes numerous expeditions to rich marine vertebrate localities on the coast of Peru,

Andean caves preserving Pleistocene mammals, Paleogene and Neogene fossiliferous localities in Peruvian Amazonia and Andean regions, and vertebrate-bearing Miocene strata along the Panama Canal.

Julia received her M.S. in zoology in 2015 from the University of Florida with a thesis entitled: “Feeding ecology of ancient and modern mammals from Amazonia: an isotopic approach”. At the Florida Museum of Natural History she received the Lucy

Dickinson Fellowship in Vertebrate Paleontology for outstanding students. She has led and co-authored more than 10 peer-reviewed publications and more than a dozen abstracts.