Stable Isotope and Trace Element Paleoecology of the Rudabánya II Fauna: Paleoenvironmental Implications for the Late Miocene Hominoid, Rudapithecus Hungaricus

Home , Anapithecus, Hispanopithecus, Micromeryx, Parachleuastochoerus, Rudapithecus

Stable Isotope and Trace Element Paleoecology of the Rudabánya II Fauna: Paleoenvironmental Implications for the Late Miocene Hominoid, Rudapithecus hungaricus

Laura Campbell Eastham

A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Anthropology University of Toronto

Stable Isotope and Trace Element Paleoecology of the Rudabánya II Fauna: Paleoenvironmental Implications for the Late Miocene Hominoid, Rudapithecus hungaricus

Laura C. Eastham

Doctor of Philosophy

Graduate Department of Anthropology University of Toronto

2017 Abstract

The Late Miocene extinction of great apes in Europe has generally been regarded as the consequence of environmental changes that occurred in correlation with global Late Miocene cooling. However, given the range of dietary and locomotor adaptations observed among the different hominoid genera it is unlikely that the same environmental factors can account for the decline of the entire group. To better understand the factors that influenced the extinction of

European Miocene apes it is necessary to evaluate their paleoecology on a regional scale. This research utilizes stable carbon and oxygen isotope (δ13C and δ18O) and strontium/calcium (Sr/Ca) trace element ratios measured in fossil ungulate tooth enamel to reconstruct the paleoecology and paleoclimate of Rudabánya II (R. II), an early Late Miocene (~10 Ma) hominoid locality in northeastern Hungary. The fossiliferous deposits at R. II preserve abundant samples of the extinct great ape Rudapithecus hungaricus. Primary aims of this research include: 1) evaluating the types of habitats present in terms of forest canopy cover, 2) examining trophic niche dynamics among the diverse ungulate community, and 3) estimating key climatic variables including mean annual temperature (MAT), mean annual precipitation (MAP), and degree of seasonality. Stable isotope and Sr/Ca values indicate the presence of a heterogeneous wetland- ii forest environment, with a gradient of more open to closed canopy habitats. Significant differences in stable isotope and Sr/Ca values were observed among the sampled ungulate fauna, supporting the interpretation of resource specialization and partitioning. A MAP of 1030-1333 mm/yr, and a MAT of 14°C were calculated from the average δ13C and δ18O values of the equid

Hippotherium intrans. Intra-tooth δ18O values revealed low amplitudes of variation indicating that seasonal changes in temperature and precipitation were relatively mild. The paleoenvironment that Rudapithecus inhabited was similar to that of contemporaneous hominoids in Western Europe, but strikingly different from that of hominoids in the Eastern

Meditterranean. While adaptations to fallback feeding and efficient suspensory arboreality would have allowed Rudapithecus to endure some degree of environmental deterioration, the progressive restriction and fragmentation of humid wetland-forests following the retreat of Lake

Pannon would have eventually led to its extinction.

iii

Acknowledgments

I am incredibly grateful to the many people who supported me over the course of my doctoral research. First and foremost, I recognize my supervisor, David Begun, for his tremendous guidance throughout my time at the University of Toronto. I am deeply appreciative of the freedom I was given to develop my thoughts, as well as the continued encouragement and patience while I worked through them. Thank you, David. The DRB abides.

I would like to thank Robert Feranec for being a wonderful mentor and friend. You have consistently encouraged me to maintain high expectations of my own abilities. I have learned a great deal through your guidance, expertise, and passion for science. It’s not often that you email someone asking about their paper and they reply offering to teach you all of the geochemical methods required for your doctoral research. I hope to be able to do that for a student in the future. You have shown me the importance of not only being a good scientist, but also a good person.

I must also thank my core committee members, Jochen Halfar and Shawn Lehman. Your thoughtful and constructive comments throughout my doctoral program have improved my dissertation each step of the way. Further, your diverse expertise and insights have greatly broadened the scope of my research. I am thankful for the comments and support provided by my internal examiner, Mary Silcox. Your critical appraisal of my work and guidance on future research and career path has been extremely helpful. I also thank my external examiner, Fred Longstaffe, whose exceptionally insightful and encouraging appraisal of my dissertation has reinforced my belief in my own research and enthusiasm for stable isotope paleoecology. I’ll never look at clouds the same way, Fred. I would like to express my sincere gratitude to the entire faculty and staff of the Anthropology Department at U of T. In particular, I would like to acknowledge Bence Viola, Heather Miller, Michael Schillaci, Sherry Fukuzawa, Trevor Orchard, Natalia Krencil, Josie Alaimo, and Sophia Cottrell.

I am grateful for my home away from home in the School of the Environment at U of T. My time spent teaching and conducting research at the School has profoundly influenced the way I perceive the human-environment relationship. I thank David Powell, Sarah Finklestein, and Kim Strong for their support. I will never have the words to thank Douglas Macdonald for all he has

iv done. Our research has changed the way I look at paleoecology and human evolution. Your genuine concern for the environment and interest in effecting positive change in the world will always inspire me. Thank you so much for your friendship and guidance.

I would like to acknowledge the sources of funding for my dissertation: Ontario Graduate Scholarship, General Motors Women in Science and Mathematics Award, Geological Society of America Graduate Research Award, University of Toronto Fellowship, University of Toronto Department of Anthropology Pilot Dissertation Fund, University of Toronto School of Graduate Studies Travel Grant, and University of Toronto Department of Anthropology Doctoral Completion Award. Without this support, I would not have been able to do this research.

So many amazing friends have seen me through the ups and downs of graduate school. I would like to thank the following people who have made this journey one to remember: Karyne Nancy Rabey (Mentor), Stephanie Kozakowski (Kozzel), Amber MacKenzie (Unicorn), Peter Bikoulis (Peta Joules), Joel Cahn (HurriCahn), Lelia Watamaniuk, Sarah Ranlett, Anastasia Hervas, Travis Steffens, Keriann McGoogan, Achinie Wijesinghe, Alana Peters, Cooper Campbell, and Nicole Delaney. I would also like to thank past and present members of the Begun Lab for their support and feedback on my work throughout my time at U of T. I am grateful for (Big) Dave Bovee whose humour, geological know-how, and cowboy coffee always made fieldwork highly excellent.

I sincerely thank Dave Boutilier for putting up with the Miocene and me for this long. You have helped me far more than you know. I am so thankful that you are in my life.

Finally, thank you to my mother, Anne Eastham, whose unwavering support, love, and sense of humour has kept me going throughout the years. You have always been my number one supporter. Without you none of this would have been possible. You’re the best AnneHam!

I dedicate this dissertation to my friend and mentor, Douglas Macdonald, who taught me to look beyond the fossils.

Table of Contents

1 Context and Objectives……………………………………………………………………1

1.1 Late Miocene Environmental Change and the Extinction of Hominoids in Europe………….………………………………………………………………….1

1.2 Objectives and Organization of this Dissertation…………………………………6

References…………………………………………………………………………………9

2 Stable Isotopes Show Resource Partitioning Among the early Late Miocene Herbivore Community at Rudabánya II: Paleoenvironmental Implications for the Hominoid, Rudapithecus hungaricus…………………………………………………….21

1 Introduction………………………………………………………………………22

2 Background………………………………………………………………………25

2.1 Rudabánya: Geology, Paleontology, and Paleoecology…………………25

2.2 Stable Carbon Isotope Values in Mammalian Enamel…………………..27

2.3 Stable Oxygen Isotope Values in Mammalian Enamel……….…………29

3 Materials and Methods………………………….………………………………..30

4 Results……………………………………………………………………………32

4.1 Stable Carbon Isotope Values……………………………………………32

4.2 Stable Oxygen Isotope Values…………………………………………...32

5 Discussion………………………………………………………………………..33

5.1 Mammalian Paleoecology: Resource Use and Partitioning……………...33

5.1.1 Mammalian Paleoecology in Open Canopy Habitats……………………34

vii

5.1.2 Mammalian Paleoecology in Closed Canopy Habitats…………………..38

5.2 The Paleoenvironment of Rudapithecus hungaricus…………………….39

5.3 Comparative Paleoecology of Late Miocene Hominoids in Western Eurasia……………………………………………………………………42

6 Conclusions………………………………………………………………………44

References……………………………………………………………………..…45

3 Trace Element Analysis Provides Insight into the Diets of early Late Miocene Ungulates from the Rudabánya II Locality (Hungary)…………………………………..68

1 Introduction………………………………………………………………………69

2 Geological Setting………………………………………………………………..71

3 Materials and Methods…………………………………………………………...73

4 Results……………………………………………………………………………76

5 Discussion………………………………………………………………………..77

6 Conclusions………………………………………………………………………81

References…………..……………………………………………………………82

4 Paleoclimate of the early Late Miocene Rudabánya II (R. II) Primate Locality Inferred from the Stable Isotope Compositions of Equid Enamel Apatite………………95

1 Introduction………………………………………………………………………96

2 Background………………………………………………………………………99

2.1 Geology and Paleontology……………………………………………….99

2.2 Carbon Isotope Values in Mammalian Enamel………………………...100

2.3 Oxygen Isotope Values in Mammalian Enamel………………………..101 viii

2.4 Intra-tooth Isotopic Variation and Seasonality…………………………102

3 Materials and Methods………………………………………………………….104

4 Results…………………………………………………………………………..105

4.1 Bulk Carbon Isotope Values and Mean Annual Precipitation (MAP)…………………………………………………………………..105

4.2 Bulk Oxygen Isotope Values and Mean Annual Temperature (MAT)……………………………….………………………………….106

4.3 Intra-tooth Variation in Isotope Values and Seasonality……………….109

5 Discussion………………………………………………………………………111

5.1 Climatic Interpretations: Mean Annual Precipitation (MAP)…………..111

5.2 Climatic Interpretations: Mean Annual Temperature (MAT)…………..112

5.3 Climatic Interpretations: Seasonality…………………………………...114

5.4 Paleoecological Implications for the Rudabánya Primates……………..116

6 Conclusions……………………………………………………………………..120

References………………………………………………………………………121

5 Conclusions and Directions for Future Research……………………………………….143

5.1 Summary and Perspectives……………………………………………………..143

5.2 Directions for Future Research…………………………………………………146

References………………………………………………………………………148

List of Tables

13 18 Table 2.1 Descriptive δ CE and δ OE statistics for the R. II ungulates…………………...30

13 18 Table 2.2 Significant differences in δ CE and δ OE values among the R. II ungulates……31

Table 3.1 Descriptive Sr/Ca statistics for the R. II ungulates………………………………73

Table 3.2 Significant differences in Sr/Ca ratios among the sampled R. II ungulates……..76

18 13 Table 4.1 Bulk δ OE and δ CE compositions of Hippotherium intrans. Conversion of 18 18 δ OEnamel carbonate value to drinking water δ O value and calcuation of mean annual air temperature………………………………..………….……………..104

18 13 Table 4.2 Serial δ OE and δ CE profiles of Hippotherium intrans………………………109

Table 4.3 Mean annual precipitation (MAP) and mean annual temperature (MAT) estimates obtained from previous paleoclimatic studies and the results of this isotopic study……………………………………………………………………………111

List of Figures

Figure 2.1 The Pannonian Basin with estimated paleoshoreline of Lake Pannon…………..25

13 18 Figure 2.2 Scatter plot of mean values and total ranges of δ CEnamel and δ OEnamel from the R. II fauna…………………………………………………………...…………...33

Figure 3.1 The Pannonian Basin with estimated maximum extension of Lake Pannon…….71

Figure 3.2 Mean value ± 1 standard deviation plots of Sr/Ca enamel ratios of the R. II ungulates…………………………………………………………………………75

Figure 4.1 Geographic location of the study area……………………………………………98

13 18 Figure 4.2 Intra-tooth variation in δ CEnamel and δ OEnamel compositions along the third molars of Hippotherium intrans………………………………………………...110

xii

List of Appendices

13 18 Appendix A δ CEnamel and δ OEnamel values from the sampled R. II fauna..………………..154

Appendix B Sr/Ca ratios of ungulate dental enamel samples from R. II………….………...156

xiii 1

Chapter 1

Context and Objectives

The research comprising this dissertation is motivated by a continuing desire to more fully understand the complex relationship between hominoid evolution and environmental change. Specifically, my current interests involve examining the ecological factors that contributed to the local extinction of great apes in Europe during the Late Miocene. In this dissertation, I utilize stable isotope and trace element ratios measured in fossil tooth enamel to reconstruct the paleoecology and paleoclimate at Rudabánya II (R. II), an early Late Miocene (early Vallesian) (~10 Ma) hominoid locality in northeastern Hungary. The fossiliferous deposits at R. II preserve extensive samples of Rudapithecus hungaricus, an extinct member of the great ape and human clade, on the basis of numerous cranial and postcranial features (Begun, 1992; Kordos and Begun, 2002; Deane and Begun, 2008; Begun, 2009; Kivell and Begun, 2009). The purpose of this chapter is to introduce the contrasting Late Miocene paleoecology of European great apes, and to provide context for the research presented in the remainder of this dissertation.

1.1 Late Miocene Environmental Change and the Extinction of Hominoids in Europe

Following an initial radiation in Africa during the Early Miocene, hominoids dispersed into Eurasia where they diversified into more than 10 genera from ca. 16.5 Ma onwards (Begun, 2007, 2009). Currently, it is unclear why hominoids became locally extinct in Europe during the Late Miocene, while they survived in Asia and Africa until present. The decrease in diversity and subsequent extinction of European great apes has generally been regarded as the consequence of environmental changes that occurred in correlation with global Late Miocene cooling (Zachos et al., 2001; Mosbrugger et al., 2005; Bruch et al., 2007; Darby, 2008; Utescher et al., 2009). However, it is unlikely that the same environmental factors can account for the decline of hominoids throughout Europe, not only because the different genera show a range of dietary and locomotor adaptations, but also because the environmental response to Late Miocene

2 cooling differed significantly based upon geographic region. For this reason it is critical to evaluate the paleoecology of European great apes on a regional scale.

In Western Europe, the decline of hominoids occurred during the late Vallesian (9.7 – 9 Ma) and has been related to increasingly seasonal climatic conditions and the progressive loss of humid forests (Agustí et al., 2003; Alba, 2012; Marmi et al., 2012; DeMiguel et al., 2014). Hispanopithecus laietanus and H. crusafonti were large-bodied, suspensory frugivores, found in association with wetland to humid subtropical forests in the Vallès-Penedès Basin, Spain (Begun, 1992; Ungar and Kay, 1995; Ungar, 1996; Moyà-Solà and Köhler, 1996; Agustí et al., 2003; Almécija et al., 2007; Alba et al., 2010ab; Marmi et al., 2012; DeMiguel et al., 2014). Paleobotanicals indicate the presence of warm-temperate mixed forests that included evergreen laurels, leguminous trees and shrubs, and a significant proportion of deciduous elements during the early Vallesian (11.2 – 9.7 Ma) (Sanz de Siria Catalán, 1994, 2001; Agustí et al., 2003; Marmi et al., 2012). From the late Vallesian onwards many evergreen taxa disappeared and deciduous tree species became dominant (Agustí et al., 2003; Marmi et al., 2012). Analysis of the oxygen stable isotope composition (δ18O) of fossil equid enamel from the Iberian Peninsula revealed a 5°C decrease in mean annual temperature (MAT) from the early Vallesian to present (van Dam and Reichart, 2009). Domingo et al. (2013) found a significant increase in the carbon stable isotope values (δ13C) of Iberian ungulate enamel between the early and late Vallesian, suggesting an increase in aridity and the openness of the landscape. These authors calculated a 200 mm/yr decrease in mean annual precipitation (MAP) during this period (Domingo et al., 2013). Changes in the composition of small mammal and herpetofaunal communities during the late Vallesian also indicate a significant decrease in MAP (van Dam, 2006; Böhme et al., 2008). Linear enamel hypoplasia, a dental developmental defect observed in Hispanopithecus, suggests repeated episodes of physiological stress (Skinner, 1995). These hypoplasias were initially attributed to malarial infection (Skinner, 1995), but have more recently been attributed to periods of malnutrition during seasonal fluctuations in resource abundance (Eastham et al., 2009). Hispanopithecus shows locomotor and dietary adaptations that might have allowed for temporary survival during seasonal periods of resource scarcity (Begun, 1992; Almécija et al., 2007; Alba et al., 2010ab; Alba, 2012; DeMiguel et al., 2014). Ultimately, however, it is hypothesized that these adaptations could not prevent the extinction of this fossil ape as

3 seasonality increased and humid forests became progressively discontinuous (Agustí et al., 2003; Marmi et al., 2012; DeMiguel et al., 2014).

A similar ecological scenario has been suggested to account for the extinction of Rudapithecus in Central Europe (Begun, 2002, 2009; Merceron et al., 2010; DeMiguel et al., 2014; Eastham et al., 2016). Like Hispanopithecus, this early Vallesian hominoid was a large- bodied frugivore with adaptations for efficient suspensory locomotion (Begun, 1988, 1992, 2007; Ungar, 1996; 2005; Teaford and Ungar, 2000; Kordos and Begun, 2002; Deane and Begun, 2008; Kivell and Begun 2009; Deane et al., 2013; DeMiguel et al., 2014). Rudapithecus is associated with humid wetland to subtropical forest environments in Hungary (Kordos and Begun, 2002; Harzhauser et al., 2004; Nargolwalla et al., 2006; Merceron et al., 2007; Andrews and Cameron, 2010; Hably and Erdei, 2013; Eastham et al., 2016). In Central Europe, the effects of global Late Miocene cooling (Zachos et al., 2001; Mosbrugger et al., 2005; Bruch et al., 2007; Darby, 2008; Utescher et al., 2009) may have been buffered by the presence of Lake Pannon (Merceron et al., 2010; Ivanov et al., 2011; Hably and Erdei, 2013; Utescher et al., 2017). This large water body (c. 290,000 km2) formed at approximately 11.6 Ma when a glacio-eustatic sea- level drop caused the final disintegration of the Paratethys Sea (Kázmér, 1990, Rögl, 1998; Magyar et al., 1999; Popov et al., 2004). During the early Vallesian coastal environments were characterized by extensive marshes grading into forested-wetlands, and mixed evergreen and deciduous forest (Harzhauser et al., 2007; Hably and Erdei, 2013). Paleobotanical data indicates humid to subhumid conditions in Central Europe throughout the Vallesian (Quan et al., 2014; Utescher et al., 2017). Following its maximum extension at approximately 10 Ma, Lake Pannon regressed in several phases and retreated from its northwestern margin (Magyar et al., 1999). As the lake retreated more open and seasonal woodlands gradually replaced humid wetland-forests (Lueger, 1978; Bernor et al., 1996; Daxner-Höck, 2004; Harzhauser et al., 2004; 2007; Merceron et al., 2010; Daxner-Höck et al., 2016; Utescher et al., 2017). During late Vallesian and early Turolian (8.9 – 7.5 Ma) the faunal record reflects the increasing occurrence of open country taxa (Bernor et al., 1996; Harzhauser et al., 2004; Nargolwalla et al., 2006; Vislobokova, 2006, 2007; Merceron et al., 2010). Isotopic analysis of equid enamel from the Pannonian Basin revealed higher δ13C values during the late Vallesian and throughout the Turolian, indicating the presence of open to water-stressed environments (Johnson and Geary, 2016). The Central European hominoids show cranial and post-cranial characteristics indicating adaptations to fallback feeding

4 on harder fruiting resources and efficient suspensory arboreality, which would have allowed for their temporary survival as environmental conditions began to deteriorate (Begun, 1988; Kordos and Begun, 2002; Deane and Begun, 2008; Kivell and Begun 2009; Deane et al., 2013; DeMiguel et al., 2014). However, the progressive restriction and fragmentation of humid wetland-forests during the late Vallesian would have greatly influenced their continuing survival (Franzen and Storch, 1999; Kordos and Begun, 2002; Eronen and Rook, 2004; Nargolwalla et al., 2006; Merceron et al., 2007; Eastham et al., 2016).

Unlike hominoids in Western and Central Europe, the decline Ankarapithecus meteai and Ouranopithecus macedoniensis in the Eastern Mediterranean (Turkey and Greece) was likely unrelated to forest fragmentation, and instead occurred in correlation with an increase in aridity and bushy sclerophyllous vegetation (Merceron et al., 2010; 2013; DeMiguel et al., 2014; Kaya et al., 2016). The Eastern Mediterranean hominoids show cranial and post-cranial characteristics that indicate hard-object feeding and adaptations for terrestrial locomotion (Bonis and Koufos 1993; 1997; Begun and Güleç, 1998; Merceron et al., 2005; Begun 2007; DeMiguel et al., 2014).

Molar microwear suggests that Ouranopithecus had a diet that included roots, tubers, and C3 graminoids, similar to extant Papio hamadryas (Merceron et al., 2005). Paleoenvironmental data indicate that both Ankarapithecus and Ouranopithecus occupied open savannah-like environments with low tree cover and an abundant herbaceous layer (Fortelius et al., 1996; Bonis et al., 1999; Merceron et al., 2005; 2010; 2013; Koufos, 2006; Jiménez -Moreno et al., 2007; Ivanov et al., 2011; Koufos and Konidaris, 2011; Rey et al., 2013; Kaya et al., 2016). Rey et al. (2013) calculated a MAT of 14°C and a MAP of 700 mm/yr from the enamel carbon and oxygen stable isotope ratios of late Vallesian equids from the Axois Valley and Chalkidiki localities in northern Greece. Serial oxygen isotope analysis of late Vallesian bovid enamel revealed that Ouranopithecus lived under a strongly seasonal climatic regime (Merceron et al., 2013). Merceron et al. (2013) calculated an annual range of temperature between 5 and 20+°C, suggesting that Ouranopithecus endured colder winters than any modern great ape, with the exception of mountain gorillas (Rowe, 1996; Merceron et al., 2013). While isotopic studies by Merceron et al. (2013) and Rey et al. (2013) revealed a decrease in MAP (890 to 470 mm/yr) and increase in MAT (13 to 17°C) between the Vallesian and latest Turolian (5.3 Ma), these studies found no evidence indicating a major climatic change around the Valleisan/Turolian boundary (8.9 Ma), when hominoids are suggested to have become extinct in this region. In contrast,

5 meso- and microwear data from fossil ruminants suggests a change in vegetation structure occurring close to the Vallesian/Turolian boundary that involved the expansion of bushy sclerophyllous vegetation over areas previously occupied by C3 graminoids (Merceron et al., 2010). The paleobotanical record further supports the spread of sclerophyllous vegetation during this period (Axelrod, 1975; Agustí et al., 2003; Cherubini et al., 2003). This type of environmental change would have had a significant impact on the survivability of terrestrial hominoids that were dependent on graminaceous resources (Merceron et al., 2010; 2013; DeMiguel et al., 2014). Nevertheless, the recent discovery of Ouranopithecus-like hominoids in association with early Turolian mammals in Turkey, (Gü leç et al., 2007), Bulgaria (Spassov et al., 2012), and Iran (Suwa et al., 2016) suggests a less abrupt extinction for great apes in this region.

The last Miocene hominoid in Europe, Oreopithecus bambolii, became extinct in Italy during the middle Turolian (~6.7 Ma; Rook et al., 2011). Paleoenvironmental data indicates that Oreopithecus inhabited a subtropical to warm-temperate mosaic environment within the Tusco- Sardinia archipelago (Harrison and Harrison, 1989; Carnieri and Mallegni, 2003; Matson et al., 2012; Nelson and Rook, 2016). Evolving in conditions of insularity between approximately 8.5/8 Ma and 7/6.7 Ma (Casanovas-Vilar et al., 2011a), this hominoid shows a peculiar mixture of primitive and derived characters making the interpretation of its phylogeny as well as diet and locomotion a source of continued debate (Delson, 1986; Moyà-Sola et al., 1999, 2005; Alba et al., 2001; Sussman, 2004, 2005; Begun, 2007). Locomotor behaviours ranging from suspensory arboreality to arboreal bipedality have been suggested on the basis of postcranial features (Köhler and Moyà-Solà, 1997; Moyà-Solà et al., 1999; 2005; Rook et al., 1999; Susman, 2004; Begun, 2007). A folivorous diet requiring high bite forces but relatively little extractive foraging has traditionally been assumed for Oreopithecus (Ungar, 1995; 1996; Kay and Ungar, 1997; Begun, 2007). More recent microwear and stable isotope studies indicate that soft fruit feeding (DeMiguel et al., 2014) and possibly hard-object feeding (Williams, 2013; Nelson and Rook, 2016) characterized at least a portion of its diet. Species interactions are considered as the most likely ecological factor to have influenced the decline Oreopithecus and many other members of the endemic Maremma fauna (Agustí, 2007; Abbazzi et al., 2008; Chesi et al., 2009; Rook, 2009; Casanovas-Vilar et al., 2011b). The last appearance of this fauna occurs close to the tectonic collision of the Tusco-Sardinia paleobioprovince with mainland Italy (~ 7 Ma) and the arrival of

6 mammals from continental Europe, including saber-toothed felids of the genus Machairodus (Rook, 2009; Bernor et al., 2011). Paleobotanical and ostracod data indicate a shift in climatic regime from constantly warm and humid conditions to inconsistent conditions with alternating dry and moist cycles around the time Oreopithecus went extinct (Harrison and Harrison, 1989; Benvenuti et al., 1994; Ligios et al., 2008). A recent enamel stable isotope study by Nelson and Rook (2016) showed an increase in forest canopy density and reduction of wetland habitats between the time when the hominoid was present and shortly after it became extinct. These authors suggest that Oreopithecus was dependent on access to aquatic plant resources and that the replacement of wetland habitats by expanding forests directly influenced its extinction. Given the current evidence it appears most likely that both environmental change and interactions with non-indigenous species contributed to the demise of Oreopithecus.

Ultimately, the Late Miocene extinction of great apes in Europe was related to habitat loss and an increase in environmental uniformity (Merceron et al., 2010; DeMiguel et al., 2014). In Western and Central Europe, increasing seasonality and the progressive fragmentation of humid subtropical forests contributed to the decline of Hispanopithecus and Rudapithecus. The extinction Ankarapithecus and Ouranopithecus in the Eastern Mediterranean occurred during a period of gradually increasing aridity and the spread of sclerophyllous vegetation. A more complex scenario involving change in several ecological variables (climate, vegetation, interactions with non-indigenous species) likely influenced the demise of the last European Miocene ape, Oreopithecus. The vulnerability of hominoids to Late Miocene environmental change appears to have been closely related to their hyperspecialized adaptations to regionally specific trophic niches (DeMiguel et al., 2014).

1.2 Objectives and Organization of this Dissertation

The goal of this dissertation is to reconstruct the paleoecology and paleoclimate of R. II during the early Late Miocene, in order to better understand the environment in which Rudapithecus lived. To address this objective, I use stable carbon and oxygen isotope ratios, and the ratio of strontium to calcium (Sr/Ca) trace elements preserved in fossil ungulate tooth enamel. It is my hope that the work presented here will build upon previous paleoenvironmental studies of Rudabánya (e.g. Kretzoi et al., 1976; Kordos, 1991; Kordos and Begun, 2002; Damuth

7 et al., 2003; Bernor et al., 2004; Armour-Chelu et al., 2005 Merceron et al., 2007; Andrews and Cameron, 2010; Halby and Erdei, 2013; Utescher et al., 2017) and contribute a more detailed understanding of the environmental context for Miocene hominoid evolution in Europe. Following this introductory chapter are three chapters presented as manuscripts, each of which are currently either published (Chapter 2) or in various stages of revision with academic journals (Chapters 3 and 4). Chapter 5 provides a brief summary of the primary results and perspectives from the geochemical investigations presented here, and an overview of future research plans resulting from the work undertaken in this dissertation.

Chapter 2., “Stable isotopes show resource partitioning among the early Late Miocene herbivore community at Rudabánya II: Paleoenvironmental implications for the hominoid, Rudapithecus hungaricus”, explores trophic niche dynamics among the ungulate community at R. II, and reconstructs the types of habitats present in terms of forest canopy cover. Evaluating resource use and partitioning in ancient mammal communities provides critical information for understanding patterns of species diversity and assembly through time. In Central and Western Europe, forest-adapted mammalian communities reached exceptionally high levels of species richness during the early Vallesian (~ 11.2 – 9.7 Ma; Vallesian Optimum) (Agustí et al., 1997, 2003, 2013; Franzen and Stroch, 1999; Daxner-Höck, 2004; Casanovas-Vilar et al., 2016). Because of the high faunal diversity and unique paleoenvironmental and paleoclimatic situation, the paleoecosystem at R.II is an ideal site to examine questions related to mammalian resource use and partitioning. Significant differences in stable isotope values were observed among the sampled ungulate species, supporting the interpretation of resource specialization and partitioning. An abundance of plant resources likely allowed for the coexistence of this diverse community of predominantly browsing herbivores. The results of this research indicate a gradient of more open to closed canopy forest habitats without sharp ecotonal boundaries. Within the gradient of more open to closed canopy forest, it is likely that Rudapithecus occupied dense closed canopy habitats where access to fruit was relatively continuous. This chapter was published in Palaeogeography, Palaeoclimatology, Palaeoecology (Eastham et al., 2016).

Chapter 3., “Trace element analysis provides insight into the diets of early Late Miocene ungulates from the Rudabánya II locality (Hungary)”, further evaluates resource use and partitioning among the R. II ungulates using Sr/Ca ratios. Sr/Ca ratios provide insight into the relative dietary contribution of certain plants and plant parts, which can be difficult to discern in

ancient C3-ecosystems using stable carbon isotopes alone. This study represents the second to date using Sr/Ca ratios to examine dietary ecology in a European Miocene mammalian community. The results show significant differences in dietary resource use, implying that the different ungulate species did partition resources by selecting different plants and plant parts. Trophic behaviours interpreted from Sr/Ca ratios were mostly consistent with those derived from stable carbon and oxygen isotope ratios (Chapter 2) and other proxies (crown height, meso- and microwear). Higher Sr/Ca ratios were found in the bovid Miotragocerus sp. than in the gomphothere Tetralophodon longirostris, which is incongruent with morphological and stable isotope data indicating leaf browsing by both taxa. This finding is likely the result of a difference in digestive physiology (ruminant vs. monogastric) rather than a difference in trophic behaviour. Interestingly, the Sr/Ca ratios of the small-bodied tragulid M. flourensianus were significantly lower than those of the large-bodied bovid Miotragocerus sp. These results were unexpected given that both species were ruminants thought to have browsed on leaves and fruit, which are Sr-poor plant resources. It is possible that the unique digestive adaptations of extant small-bodied ruminant frugivores could help to explain this finding. This chapter was recently accepted for publication in journal Geologica Acta.

Chapter 4., “Paleoclimate of the early Late Miocene Rudabánya II (R. II) primate locality inferred from the stable isotope compositions of equid enamel apatite”, investigates the paleoclimatic regime under which Rudapithecus lived in terms of MAT, MAP, and degree of seasonality. This study also examines the climatic factors that could have acted to influence the co-occurrence of Rudapithecus and the pliopithecoid, Anapithecus hernyaki, at R. II. Despite the broad and penecontemporaneous distribution of hominoids and pliopithecoids during the Middle and early Late Miocene their co-occurrence in the Eurasian fossil record is extremely rare (Andrews et al., 1996; Harrison et al., 2002; Alba et al., 2011; Almécija et al., 2012; Sukselainen et al., 2015). Ecometric and ecological diversity studies suggest that humidity was a key environmental factor influencing the distribution of these primate groups (Eronen and Rook, 2004; Sukselainen et al., 2015). The results of this research indicate a MAP ranging between 1030 and 1333 mm/yr, which is consistent with estimates derived from other proxies, and a MAT ranging between 11°C and 14°C, which is lower than estimates calculated from small mammals and paleobotanicals (~14 - 16°C). Serial isotope analysis revealed relatively low average amplitudes of stable oxygen isotope variation, indicating that seasonal changes in

climate were relatively mild. The results of this study are generally concordant with previous research suggesting that the R. II primates experienced an equable humid and wet subtropical climate during the early Late Miocene. This research is significant in supporting the hypothesis that humidity was a key factor influencing the co-occurrence of hominoids and pliopithecoids. Chapter 4 is currently in revision with the Journal of Human Evolution.

References

Abbazzi, L., Delfino, M., Gallai, G., Trebini, L., Rook, L., 2008. New data on the vertebrate assemblage of Fiume Santo (North-western Sardinia, Italy), and overview on the Late Miocene Tusco-Sardinian paleobioprovince. Palaeontology 51, pp. 425–451.

Agustí, J., 2007. The biotic environments of the Late Miocene hominids. In: Henke, W., Tattersall, I. (Eds.), Handbook of Paleoanthropology. Springer, Berlin, pp. 979–1010.

Agustí, J., Cabrera, L., Garcés, M., Parés, J. M., 1997. The Vallesian mammal succession in the Valles-Penedes Basin (northeast Spain): Paleomagnetic calibration and correlation with global events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 133, pp. 149–180.

Agustí, J., Siria, A. S. d., Garcés, M., 2003. Explaining the end of the hominoid experiment in Europe. J. Hum. Evol. 45, pp. 145–153.

Alba, D.M., Moyà-Solà, S., Kӧhler, M., 2001. Canine reduction in the Miocene hominoid Oreopithecus bambolii: behavioural and evolutionary implications. J. Hum. Evol. 40, pp. 1– 16.

Alba, D.M., 2012. Fossil apes from the Vallès-Penedès Basin. Evol. Anth. 21, pp. 254–269.

Alba, D.M., Almécija, S., Moyà-Solà, S., 2010a. Locomotor inferences in Pierolapithecus and Hispanopithecus: reply to Deane and Begun. J. Hum. Evol. 59, pp. 143–149.

Alba, D.M., Fortuny, J., Moyà-Solà, S., 2010b. Enamel thickness in middle Miocene great apes Anoiapithecus, Pierolapithecus and Dryopithecus. Proc. R. Soc. Biol. 277, pp. 2237–2245.

Alba, D.M., Fortuny, J., DeMiguel, D., 2011. Preliminary paleodietary inferences in two

pliopithecid primates from the Vallès–Penedès Basin (NE Iberian Peninsula) based on relative enamel thickness as compared to microwear analyses [Abstract]. Paleontol. Evol. I International Symposium on Paleohistology: 47.

Almécija, S., Alba, D.M., Moyà-Solà, S., Köhler, M., 2007. Orang-like manual adaptations in the fossil hominoid Hispanopithecus laietanus: first steps towards great ape suspensory behaviours. Proc. R. Soc. Biol. 274, pp. 2375–2384.

Almécija, S., Alba, D.M., Moyà-Solà, S., 2012. The thumb of Miocene apes: new insights from Castell de Barberà (Catalonia, Spain). Am. J. Phys. Anthro. 148, pp. 436–450.

Andrews, P., Cameron, D., 2010. Rudabànya: Taphonomic analysis of a fossil hominid site from Hungary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 297, pp. 311–329

Andrews, P., Harrison, T., Martin, L., Delson, E., Bernor, R.L., 1996. Systematics and biochronology of European Neogene catarrhines. In: Bernor, R., Fahlbusch, V. (Eds.), Evolution of Neogene Continental Biotopes in Europe and the Eastern Mediterranean. Columbia University Press, pp. 168–207.

Armour-Chelu, M., Andrews, P., Bernor, R. L., 2005. Further observations on the primate community at Rudabánya II (Late Miocene, early Vallesian age), Hungary. J. Hum. Evol. 49, pp. 88–98.

Axelrod, D., 1975. Evolution and biogeography of the Madrean-Tethyan sclerophyll vegetation. Annals of the Missouri Botanical Garden 62, pp. 280–334.

Begun, D. R., 1988. Catarrhine phalanges from the Late Miocene (Vallesian) of Rudabánya, Hungary. J. Hum. Evol. 17, pp. 413–438.

Begun, D. R., 1992. Phyletic diversity and locomotion in primitive European hominids. Am. J. Phys. Anthro. 87, pp. 311–340.

Begun, D.R., 2002. The Pliopithecoidea. In: Hartwig, W.C. (Ed.), The Primate Fossil Record. Cambridge University Press, New York, pp. 221–240.

Begun, D.R., 2007. Fossil record of Miocene hominoids. In: Henke, W., Tattersall, I. (Eds.), Handbook of Paleoanthropology, Springer, Heidelberg, pp. 921–977.

Begun, D.R., 2009. Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade. Geodiversitas 31, pp. 789–816.

Begun, D. R., Güleç, E., 1998. Restoration of the Type and Palate of Ankarapithecus meteai: Taxonomic, Phylogenetic, and Functional Implications. Am. J. Phys. Anthro. 105, pp. 279– 314.

Benvenuti, M., Bertini, A., Rook, L., 1994. Facies analysis, vertebrate paleontology and palynology in the Late Miocene Baccinello-Cinigiano Basin (southern Tuscany). Italian Geological Society 48, pp. 415–423.

Bernor, R.L., Fahlbusch, V., Andrews, P., de Bruijn, H., Fortelius, M., Rögl, F., Steininger, F.F.,Werdelin, L., 1996. The evolution of European andWest Asian later Neogene faunas: a biogeographic and paleoenvironmental synthesis. In: Bernor, R., Fahlbusch, V., Mittmann, W. (Eds.), The Evolution of Western Eurasian Neogene Mammal Faunas.Columbia University Press, pp. 449–470.

Bernor, R.L., Kordos, L., Rook, L., Agustí, J., Andrews, P., Armour-Chelu, M., Begun, D.R., de Bonis, L., Cameron, D.W., Damuth, J., Daxner-Höck, G., Fessaha, N., Fortelius, M., Franzen, J.L., Gasparik, M., Gentry, A., Heissig, K., Hernyak, G., Kaiser, T.M., Koufos, G.D. Krolopp, E., Jánossy, D., Llenas, M., Meszáros, L., Müller, P., Renne, P.R., Rocek, Z., Sen, S., Scott, R.S., Szindlar, Z., Topál, G.Y., Ungar, P.S., Untescher, T., van Dam, J.A., Werdelin, L. & Ziegler, R., 2004. Recent advances on multidisciplinary research at Rudabanya, Late Miocene (MN9), Hungary: a compendium. Paleontographica Italia 89, pp. 3–36.

Bernor, R.L., Kaiser, T.M., Nelson, S. V., Rook, L., 2011. Systematics and palebiology of Hippotherium malpassii n. sp. (Equidae, Mammalia) from the latest Miocene of Baccinello V3 (Tuscany, Italy). Bollettino della Società Paleontologica Italiana 50, pp. 175–208.

Böhme, M., Ilg, A., Winklhofer, M., 2008. Late Miocene “washhouse” climate in Europe. Earth Plan. Sci. Lett. 275, pp. 393–401.

Bonis, L., Koufos, G., 1993. The face and mandible of Ouranopithecus macedoniensis: description of new specimens and comparisons. J. Hum. Evol. 24, pp. 469–491.

Bonis, L., Koufos, G., 1997. The phylogenetic and functional implications of Ouranopithecus macedoniensis. In: Begun D.R., Ward, C.V., Rose, M.D. (Eds.), Function, phylogeny and fossils: Miocene hominoid origins and adaptations. New York: Plenum Press, pp. 317–326.

Bonis, L.de, Bouvrain, G., Koufos, G.D., 1999. Palaeoenvironments of the hominoid primate Ouranopithecus in the Late Miocene deposits of Macedonia, Greece. In: Agusti, J., Rook, L., Andrews, P. (Eds.), Hominoid Evolution and Climatic Change in Europe: The Evolution of the Neogene Terrestrial Ecosystems in Europe. Cambridge University Press, New York, pp. 205–237.

Bruch, A. A., Uhl, D., Mosbrugger, V., 2007. Miocene climate in Europe - patterns and evolution. A first synthesis of NECLIME. Palaeogeogr. Palaeoclimatol. Palaeoecol. 253, pp. 1–7.

Carnieri, E., Mallegni, F., 2003. A new specimen and dental microwear in Oreopithecus bambolii. Homo 54, pp. 29–35.

Casanovas-Vilar, I., Alba, D.M., Garcés, M., Robles, J.M., Moyá-Solá, S., 2011a. Updated chronology for the Miocene hominoid radiation in western Eurasia. PNAS 108, pp. 5554– 5559.

Casanovas-Vilar, I., van Dam, J.A., Moyà-Solà, S., Rook, L., 2011b. Late Miocene insular mice from the Tusco-Sardinian palaeobioprovince provide new insights on the palaeoecology of the Oreopithecus faunas. J. Hum. Evol. 61, pp. 42–49.

Casanovas-Vilar, I., Madern, A., Alba, D., Cabrera, L., García-Paredes, I., van den Hoek Ostende, L., DeMiguel, D., Robles, J.M., Furió, M., van Dam, J., Garcés, M., Angelone, C., Moyà-Solà, S., 2016. The Miocene mammal record of the Vallès-Penedès Basin (Catalonia). Comptes Rendus Palevol, 15, 791–812.

Cherubini, P., Gartner, B.L., Tognetti, R., Bracker, O., Schoch, W., Innes, J.L., 2003. Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates. Biological Review 78, pp. 119–148.

Chesi, F., Delfino, M., Rook, L., 2009. Late Miocene Mauremys (Testudines, Geoemydidae) from Tuscany (Italy): evidence of terrapin persistence after a mammal turnover. J. Paleontol. 83, pp. 379–388.

Damuth, J., van Dam J.A., Utescher, T., 2003. Palaeoclimate proxies from biotic proxies. In: Bernor, R.L., Kordos, L., Rook, L. (Eds.), Recent Advances on Multidisciplinary Research at Rudabánya, Late Miocene (MN9), Hungary: A Compendium, Palaeontographica Italica 89, pp. 1–34.

Darby, D.A., 2008. Arctic perennial ice cover over the last 14 million years. Paleoceanography 23, PA1S07.

Daxner-Höck, G., 2004. Biber und ein zwerghamster aus Mataschen (unter-pannonium, steirisches becken). Joannea Geologie Und Paläontologie 5, pp. 19–33.

Daxner-Höck, G., Harzhauser, M., Göhlich, U., 2016. Fossil record and dynamics of the Late Miocene small mammal faunas of the Vienna Basin and adjacent basins. Austria. C.R. Palevol. 15, pp. 855–862.

Deane, A.S., Begun, D.R., 2008. Broken fingers: retesting locomotor hypotheses for fossil hominoids using fragmentary proximal phalanges and high-resolution polynomial curve fitting (HR-PCF). J. Hum. Evol. 55, pp. 691–701.

Deane, A.S., Nargolwalla, M.C., Kordos, L., Begun, D.R., 2013. New evidence for diet and niche partitioning in Rudapithecus and Anapithecus from Rudabánya, Hungary. J. Hum. Evol. 65, pp. 704–714.

Delson, E., 1986. An anthropoid enigma: historical introduction to the study of Oreopithecus bambolii. J. Hum. Evol. 15, pp. 523–531

DeMiguel, D., Alba, D., Moyà-Solà, S., 2014. Dietary specializations during the evolution of Western Eurasian hominoids and the extinction of great apes. PLoS ONE 9(5): e97442.

Domingo, L., Koch, P.L., Hernández Fernández. M., Fox, D.L., Domingo, M.S., Alberdi, M.T., 2013. Late Neogene and early quaternary paleoenvironmental and paleoclimatic conditions in southwestern Europe: isotopic analyses on mammalian taxa. PLoS ONE 8(5), E63739.

Eastham, L., Skinner, M.M., Begun, D.R., 2009. Resolving seasonal stress in the Late Miocene hominoid Hispanopithecus laietanus through the analysis of the dental developmental defect linear enamel hypoplasia. J. Vert. Paleo. 29 (Suppl. 3), 91A.

Eastham, L. C., Feranec, R.S., Begun, D.R., 2016. Stable isotopes show resource partitioning among the early Late Miocene herbivore community at Rudabánya II: Paleoenvironmental implications for the hominoid, Rudapithecus hungaricus. Palaeogeogr. Palaeoclimatol. Palaeoecol. 454, pp. 161–174.

Eronen, J., Rook, L., 2004. The Mio-Pliocene European primate fossil record: dynamics and habitat tracking. J. Hum. Evol. 47, pp. 323–341.

Fortelius, M., Werdelin, L., Andrews, P., Bernor, R.L., Gentry, A., Humphrey, L., Mittmann, H.- W., Viranta, S., 1996. Provinciality, diversity, turnover and palaeoecology in land mammal faunas of the Late Miocene of Western Eurasia. In: Bernor, R.L., Fahlbusch, V., Mittmann, H.-W. (Eds.), The evolution of Western Eurasian Neogene mammal faunas. Columbia University Press, New York, pp. 414–448.

Franzen, J. L., Storch, G., 1999. Late Miocene mammals from central Europe. Hominoid Evolution and Climatic Change in Europe 1, pp. 165–190.

Gü leç E.S., Sevim, A., Pehlevan, C., Kaya, F., 2007. A new great ape from the Late Miocene of Turkey. Anthropol. Sci. 115, pp. 153–158.

Hably, L., Erdei, B., 2013. A refugium of mastixia in the Late Miocene of eastern central Europe. Rev. Palaeobot. Palynol. 197, pp. 218–225.

Harrison, T.S., Harrison, T., 1989. Palynology of the late Miocene Oreopithecus bearing lignite from Baccinello, Italy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 76, pp. 45–65.

Harrison, T., 2002. Late Oligocene to middle Miocene catarrhines from Afro‐Arabia. In: Hartwig, W. (Ed.), The primate fossil record, pp. 311–338. Cambridge University Press, Cambridge.

Harzhauser, M., Mandic, O., 2004. The muddy bottom of Lake Pannon - A challenge for dreissenid settlement (Late Miocene; bivalvia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 204, pp. 331–352.

Ivanov, D., Utescher, T., Mosbrugger, V., Syabryaj, S., Djordjević-Milutinović, D., Molchanoff, S., 2011. Miocene vegetation and climate dynamics in Eastern and Central Paratethys (Southeastern Europe). Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, pp. 262–275.

Jiménez-Moreno, G., Popescu, S.M., Ivanov, D., Suc, J.P., 2007. Neogene flora, vegetation and climate dynamics in southeastern Europe and the northeastern Mediterranean. In: Williams, M., Haywood, A.M., Gregory, F.J., Schmidt, D.N. (Eds.), Deep-Time Perspectives on Climate Change: Marrying the Signal from Computer Models and Biological Proxies. The Micropalaeontological Society, London, pp. 503–516.

Johnson, M., Geary, D., 2016. Stable isotope ecology of Hippotherium from the Late Miocene Pannonian Basin system. Palaeogeogr. Palaeoclimatol. Palaeoecol. 459, pp. 44–52.

Kaya, F., Kaymakci, N., Eronen, J., Pehlevan, C., Erkman, A., Langereis, C., Fortelius, M., 2016. Magnetostratigraphy and paleoecology of the hominid-bearing locality Corakyerler, Tuğlu Formation (Çankiri Basin, Central Anatolia). J. Vert. Paleo. 36, e1071710.

Kay, R.F., Ungar, P.S., 1997. Dental evidence for diet in some Miocene catarrhines with comments on the effects of phylogeny on the interpretation of adaptation. In: Begun, D.R., Ward, C.V., Rose, M.D. (Eds.), Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations. Plenum Press, New York, pp. 131–151.

Kivell, T. L., Begun, D. R., 2009. New primate carpal bones from Rudabánya (Late Miocene, Hungary): Taxonomic and functional implications. J. Hum. Evol. 57, pp. 697–709.

Kӧhler, M., Moyà-Sola, S., 1997. Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. PNAS. 94, pp. 11747–11750.

Kordos, L., 1991. Le Rudapithecus hungaricus de Rudabànya (Hongrie). L'Anthropologie 95, pp. 343–362.

Kordos, L., Begun, D. R., 2002. Rudabánya: A Late Miocene subtropical swamp deposit with evidence of the origin of the African apes and humans. Evol. Anth. 11, pp. 45–57.

Koufos, G.D., 2006. Palaeoecology and chronology of the Vallesian (Late Miocene) in the Eastern Mediterranean region. Palaeogeogr. Palaeoclimatol. Palaeoecol. 234, pp. 127–145.

Koufos, G.D., Konidaris, G.E., 2011. Late Miocene carnivore of the Greco-Iranian Province: Composition, guild structure and paleoecology. Palaeogeogr. Palaeoclimatol. Palaeoecol. 305, pp. 215–226.

Kretzoi, M., Krolopp, E., Lörincz, H., Pálfalvy, I., 1976. A Rudabanyai alsopannonai prehominidas lelohely floraja, faunaja es retegtani helyzete. Annual Report of the Hungarian Geological Institute, pp. 365–394.

Ligios, S., Benvenuti, M., Gliozzi, E., Papini, M., Rook, L., 2008. Late Miocene palaeoenvironmental evolution of the Baccinello-Cinigiano Basin (Tuscany, central Italy) and new autoecological data on rare fossil fresh- to brackish-water ostracods. Palaeogeogr. Palaeoclimatol. Palaeoecol. 264, pp. 277–287.

Lueger, J.P., 1978. Klimaentwicklung im Pannon und Pont desWiener Beckens aufgrund von Landschneckenfaunen. Anzeiger der math.-naturw. Klasse der Österreichischen Akademie der Wissenschaften 6, pp. 137–149.

Magyar, I., Geary, D. H., Müller, P., 1999. Paleogeographic evolution of the Late Miocene Lake Pannon in central Europe. Palaeogeogr. Palaeoclimatol. Palaeoecol. 147, pp. 151–167.

Marmi, J., Casanovas-Vilar, I., Robles, J.M., Moyà-Solà, S., Alba, D.M., 2012. The paleoenvironment of Hispanopithecus laietanus as revealed by paleobotanical evidence from the Late from the Late Miocene of Can Llobateres 1 (Catalonia, Spain). J. Hum. Evol. 62, pp. 412–423.

Matson, S.D., Rook, R., Oriol, O., Fox, D.L., 2012. Carbon isotopic record of terrestrial ecosystems spanning the Late Miocene extinction of Oreopithecus bambolii, Baccinello Basin (Tuscany, Italy). J. Hum. Evol. 63, pp. 127–139.

Merceron, G., Blondel, C., de Bonis, L., Koufos, G.D., Viriot, L., 2005. A new method of dental microwear analysis: application to extant primates and Ouranopithecus macedoniensis (Late Miocene of Greece). Palaios. 20, pp. 551–561.

Merceron, G., Schulz, E., Kordos, L., Kaiser, T. M., 2007. Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: Evidence from dental meso- and micro-wear analyses of large vegetarian mammals. J. Hum. Evol. 53, pp. 331–349. Merceron, G., Kaiser, T.M., Kostopoulos, D.S., Schulz, E., 2010. Ruminant diets and the Miocene extinction of European great apes. Proc. R. Soc. Biol. 277, pp. 3105–3112.

Merceron, G., Kostopoulos, D.S., Bonis, L.d., Fourel, F., Koufos, G.D., Lécuyer, C., Martineau, F., 2013. Stable isotope ecology of Miocene bovids from Northern Greece and the ape/money turnover in the Balkans. J. Hum. Evol. 65, pp. 185–198.

Mosbrugger, V., Utescher, T., Dilcher, D. L., 2005. Cenozoic continental climatic evolution of central Europe. PNAS. 102, pp. 14964–14969.

Moyà-Solà, S., Köhler, M., 1996. A Dryopithecus skeleton and the origins of great ape locomotion. Nature 379, pp. 156–159.

Moyà-Solà, S., Köhler, M., Rook, L., 1999. Evidence of hominid-like precision grip capabilities in the hand of the Miocene ape Oreopithecus. PNAS. 96 pp. 313–317.

Moyà-Solà, S., Köhler, M., Rook, L., 2005. The Oreopithecus thumb: a strange case in hominoid evolution. J. Hum. Evol. 49, pp. 395–404.

Nargolwalla, M.C., Hutchison, M.P., Begun, D.R., 2006. Middle and Late Miocene terrestrial vertebrate localities and paleoenvironments in the Pannonian Basin. Beiträge zur Paläontologie, 30, pp. 347–360.

Nelson, S.V., Rook, L., 2016. Isotopic reconstruction of habitat change surrounding the extinction of Oreopithecus, the last European ape. Am. J. Phys. Anth. 160, 254–271.

Rey, K., Amiot, R., Lécuyer, C., Koufos, G.D., Martineau, F., Fourel., F., Kostopoulos, D.S., Merceron, G., 2013. Late Miocene climatic and environmental variations in northern Greece inferred from stable isotope compositions (δ18O, δ13C) of equid teeth apatite. Palaeogeogr. Palaeoclimatol. Palaeoecol. 388, pp. 48–57.

Rook, L., Bondioli, L., Kӧhler, M., Moyà-Sola, S., Machiarelli, R., 1999. Oreopithecus was a bipedal ape after all: evidence from the iliac cancellous architecture. PNAS. 96, pp. 8795– 8799.

Rook L, Oms O, Benvenuti M, Papini M. 2011. Magnetostratigraphy of the Late Miocene Baccinello-Cinigiano basin (Tuscany, Italy) and the age of Oreopithecus bambolii faunal assemblages. Palaeogeogr. Palaeoclimatol. Palaeoecol. 305, pp. 286–294.

Rowe, N., 1996. The Pictorial Guide to the Living Primates. Pogonias Press, East Hampton.

Sanz de Siria Catalán, A., 1994. La evolución de las paleofloras en las cuencas cenozoicas catalanas. Acta Geologica Hispanica 29, pp. 169–189.

Sanz de Siria Catalán, A., 2001. Flora y vegetación del Mioceno medio de la depresión del Vallès-Penedès. Paleontology 33, pp. 79–92.

Skinner, M.F., Dupras, T.L., Moyà-Solà, S., 1995. Periodicity of linear enamel hipoplasia among Miocene Dryopithecus from Spain. J. Paleopath. 7, pp. 195–222.

Spassov, N., Geraads, D., Hristova, L., Markov, G.N., Merceron, G., Tzankov, T., Stoyanov, K., Böhme, M., Dimitrova, A., 2012. A hominid tooth from Bulgaria: the last pre-human hominid of continental Europe. J. Hum. Evol. 62, pp. 138–145.

Sukselainen, L., Fortelius, M., Harrison, T., 2015. Co-occurrence of pliopithecoid and hominoid primates in the fossil record: An ecometric analysis. J. Hum. Evol. 84, pp. 25–41.

Sussman, R.L., 2004. Oreopithecus bambolii: an unlikely case of hominid like grip capability in a Miocene ape. J. Hum. Evol. 46, pp. 105–117.

Sussman R.L., 2005. Oreopithecus: still ape-like after all these years. J. Hum. Evol. 49, pp. 405– 411.

Suwa, G., Kunimatsu, Y. Ataabadi, M., Orak, Z., Sasaki, T., Fortelius, M., 2016. The first hominoid from the Maragheh Formation, Iran. Palaeobiodivers. Palaeoenviron. 1–9.

Teaford, M.F., Ungar, P.S., 2000. Diet and the evolution of the earliest human ancestors. PNAS. 97, pp.13506–13511.

Ungar, P.S., Kay, R.F., 1995. The dietary adaptations of European Miocene catarrhines. PNAS. 92, pp. 5479–81.

Ungar, P.S., 1996. Dental microwear of European Miocene catarrhines: evidence for diets and tooth use. J. Hum. Evol. 31, pp. 335–66.

Ungar, P.S., 2005. Dental evidence for the diets of fossil primates from Rudabánya, northeastern Hungary with comments on extant primate analogs and “noncompetitive” sympatry. Palaeontographia Italica 90, pp. 97–112.

Ungar, P.S., Kay, R.F., 1995. The dietary adaptations of European Miocene catarrhines. PNAS. 92, pp. 5479–5481.

Utescher, T., Ivanov, D., Harzhauser, M., Bozukov, V., Ashraf, A. R., Rolf, C., 2009. Cyclic climate and vegetation change in the Late Miocene of western Bulgaria. Palaeogeogr. Palaeoclimatol. Palaeoecol. 272, pp. 99–114.

Utescher, T., Erdei, B., Hably, L., Mosbrugger, V., 2017. Late Miocene vegetation of the Pannonian Basin. Palaeogeogr. Palaeoclimatol. Palaeoecol. 467, pp. 131-148.

van Dam, J. A., 2006. Geographic and temporal patterns in the late Neogene (12-3 Ma) aridification of Europe: The use of small mammals as paleoprecipitation proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, pp. 190–218.

van Dam, J.A., Reichart, G.J., 2009. Oxygen and carbon isotope signatures in late Neogene horse teeth from Spain and application as temperature and seasonality proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 274, pp. 64–81.

Vislobokova, I. A., 2006. Associations of ruminants in Miocene ecosystems of Eastern Alpine Region. Paleontological Journal. 40, 438–447.

Vislobokova, I. A., 2007. New data on Late Miocene mammals of Kohfidisch, Austria. Paleontological Journal. 41, 451–460.

Williams, F., 2013. Enamel microwear texture properties of IGF 11778 (Oreopithecus bambolii) from the Late Miocene of Baccinello, Italy. J. Anthropol. Sci. 91, pp. 201-217.

Zachos, J., Pagani, M., Sloan, L., Thomas, E., Billups, K., 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292, 686-693.

Chapter 2

Stable Isotopes Show Resource Partitioning Among the early Late Miocene Herbivore Community at Rudabánya II: Paleoenvironmental Implications for the Hominoid, Rudapithecus hungaricus

Laura C. Easthama, Robert S. Feranecb, David R. Beguna aAnthropology Department, University of Toronto, 19 Russell Street, Toronto, ON M5S 2S2, Canada bResearch and Collections, New York State Museum, 3140 Cultural Education Center, Albany, New York, 12230, United States

Published in: Palaeogeography, Palaeoclimatology, Palaeoecology (2016) 454, pp. 161–174.

Examining how species use and partition resources within an environment can lead to a better understanding of community assembly and diversity. The rich early Late Miocene (early Vallesian) deposits at Rudabánya II (R. II) in northeastern Hungary preserve an abundance of forest dwelling taxa, including the hominoid Rudapithecus hungaricus. Here we use the carbon and oxygen stable isotope compositions of tooth enamel carbonate from 10 genera of medium to large-bodied mammals to evaluate resource use and partitioning among the herbivore community, and to reconstruct the palaeoenvironment of Rudapithecus. The range of stable 13 18 carbon and oxygen isotope values (δ CE and δ OE) displayed by the R. II fauna indicates a variable forest environment, which included both open and closed canopy habitats. The 13 18 relatively low δ CE and δ OE values found in all sampled taxa are consistent with high levels of precipitation and humidity. Significant differences in stable isotope values were observed among the sampled fauna, supporting the interpretation of resource specialization and 13 partitioning. Higher δ CE values found in Acerathrium incisivum (Rhinocerotidae), Lucentia aff. peirensis (Cervidae), Hippotherium intrans (Equidae), Tetralophodon longirostris

(Gomphotheriidae), Propotamochoerus palaeochoerus and Parachleuastochoerus kretzoii 13 (Suidae) suggest foraging in more open canopy habitats, while lower δ CE values found in Miotragocerus sp. (Bovidae), Dorcatherium naui (Tragulidae), and Micromeryx flourensianus (Moschidae) imply a preference for more densely canopied habitats. Several of the sampled taxa 18 13 yielded relatively higher δ OE and δ CE values indicative of fruit consumption, including the small ruminants, cervid, and bovid. The analyzed isotope values reflect a moderate degree of dietary niche overlap between taxa. An abundance of plant resources likely allowed for the coexistence of this diverse community of predominantly browsing herbivores. Within the gradient of more open to closed canopy forest, it is likely that Rudapithecus occupied dense closed canopy habitats where access to fruit was relatively continuous. The progressive fragmentation and replacement of humid forests by more open and seasonal woodlands during the late Vallesian would have had a significant influence on the extinction of this fossil ape.

1 Introduction

Evaluating resource use and partitioning in ancient mammal communities provides critical information for understanding patterns of species diversity and assembly through time. Interspecific competition is considered to be a major selective force encouraging the differential use of resources as well as variation in the morphology and behavior of sympatric species (Pianka, 1981; Cody, 1974; Schoener 1974,). The niche partitioning hypothesis predicts that ecologically similar species can coexist by partitioning their resources (Schoener, 1974). Sympatric mammalian herbivores partition resources by using different habitats, selecting different plants or plant parts, and being active at different times (Gartlan and Struhsaker, 1972; Schoener, 1974; Pianka, 1981). Studies of modern herbivore communities have demonstrated increased dietary niche overlap during periods of resource abundance. The low levels of feeding competition that occur during these periods promote the coexistence of morphologically similar species (Pyke et al., 1977; Gordon and Illius, 1989; Stevenson et al., 2000; Prins et al., 2006; Stroms et al., 2008; Levine and HilleRisLambers 2009; Singh et al., 2011; Djagoun et al., 2013; Landman et al., 2013; Kartzinel et al., 2015).

Stable isotope analysis of modern and fossil tooth enamel has proven to be a useful method for evaluating dietary preference, habitat use, and resource partitioning (Ambrose and DeNiro, 1986; Quade et al., 1995; Cerling and Sharp, 1996; Feranec and MacFadden, 2000;

Sponheimer et al., 2005; Urton and Hobson, 2005; Feranec, 2007; Feranec et al., 2009; Tütken and Vennemann, 2009). Over the past two decades there has been an increased focus on the study of isotope ecology in ancient C3 ecosystems (Bocherens et al., 1994a, 1994b; 1995; Quade et al., 1995; Bocherens, 2000; MacFadden and Higgins, 2004; Feranec and MacFadden, 2006; Hernández-Fernández et al., 2006; Tütken et al., 2006; 2013; DeSantis and Wallace, 2008; Domingo et al., 2009; Tütken and Vennemann, 2009; Maung-Maung-Thein et al., 2011; Rey et al., 2013; Aiglstorfer et al., 2014). Globally, plants utilizing the C4 photosynthetic pathway were only abundant from the Late Miocene (Cerling et al., 1997; 1998; Ehleringer et al., 1997; Kohn and Cerling, 2002). However, C4 plants never became widespread in Europe (Quade et al., 1994; Cerling et al., 1997; van Dam and Reichart, 2009; Domingo et al., 2009; Tütken et al., 2013) and today make up only 5% of species (Collins and Jones, 1986). The isotopic values of herbivorous mammals from Late Miocene Europe indicate a diet of pure C3 vegetation (Bocherens et al., 1994b; Hernández-Fernández et al., 2006; Merceron et al., 2006, 2013; Tütken et al., 2006; 2013; Domingo et al., 2009; 2012; Tütken and Vennemann, 2009; Rey et al., 2013; Aiglstorfer et al., 2014). While it is not easy to distinguish C3 grazers from browsers within a C3-dominated 13 13 ecosystem, variations in δ C enamel values (δ CE) can be used to examine resource partitioning and habitat differences (Drucker et al., 2003; Cerling et al., 2004; Feranec and MacFadden, 2006; Feranec, 2007; Tütken and Venneman, 2009; Domingo et al., 2009; 2013; Tütken et al., 2013; Aiglstorfer et al., 2014). In this study we use stable carbon and oxygen isotope ratios of tooth enamel carbonate to evaluate patterns of resource use and partitioning at Rudabánya II (R. II), an early Late Miocene (early Vallesian) (~10 Ma) hominoid locality in northeastern Hungary.

Forest-adapted mammalian communities in Central and Western Europe reached high levels of species richness during the early Vallesian (~ 11.2 – 9.7 Ma) (Agustí et al., 1997, 2003, 2013; Franzen and Stroch, 1999; Daxner-Höck, 2004; Casanovas-Vilar et al., 2016). More than 60 species of mammals have been recorded at the localities of Can Llobateres 1, Can Ponsic, and Rudabánya II. This period of optimum diversity was followed by the gradual decline of forest dwelling browsers and rise of woodland adapted mixed feeders and grazers, characteristic of the later Neogene (Fortelius et al., 2002). An important phase in this faunal transition was the Vallesian Crisis (~9.7 Ma), which saw the abrupt decline of many humid forest-adapted faunal elements, including the hominoids (Agustí and Moyà-Solà, 1990; Agustí et al., 1999, 2003, 2013; Fortelius and Hokkanen, 2001; Fortelius et al., 2002; Begun, 2007). The Vallesian Crisis

24 has been linked to increasing seasonality and the replacement of subtropical evergreen forests with deciduous woodlands (Agustí et al., 2003; van Dam, 2006). However, several recent studies indicate that the decline of forest dwelling taxa did not occur in an abrupt turnover event, but instead took place gradually through a series of extinction events that began in the late Vallesian/early Turolian (Franzen et al., 2013; Casanovas-Vilar et al., 2014; 2016; Daxner-Höck et al., 2016). The faunal assemblage at R. II preserves an abundance of forest-dwelling taxa, including the hominoid Rudapithecus hungaricus. Rudapithecus is an extinct member of the great ape and human clade, on the basis of numerous cranial and postcranial features (Begun, 1992; Kordos and Begun, 2002; Deane and Begun, 2008; Begun, 2009; Kivell and Begun, 2009). Both the morphology and life history pattern of this fossil ape suggest it was a large-bodied, suspensory frugivore, which would have been highly dependent on forested conditions and year- round access to fruit resources (Begun, 1992, Ungar and Kay, 1995; Ungar, 1996; 2005; Kordos and Begun, 2002; Kivell and Begun, 2009; Smith et al., 2009; Deane et al., 2013; DeMiguel et al., 2014). Because of the high faunal diversity and unique paleoenvironmental and paleoclimatic situation, the paleoecosystem at R.II is an ideal site to examine questions related to mammalian resource use and partitioning. Here we aim to: (1) evaluate resource use and partitioning among mammal species in an evaluation of the niche partitioning hypothesis and (2) to better understand the paleoecological setting in which Rudapithecus lived.

Figure 2.1 The Pannonian Basin with estimated paleoshoreline of Lake Pannon at ca. 10 Ma indicated by white dashed line. White diamond marks position of Rudabánya. White circles indicate position of Belgrade, Bucharest, Budapest, Vienna, and Zagreb for reference (modified from Rögl, 1998; Magyar et al., 1999; Popov et al., 2004).

2 Background 2.1 Rudabánya: Geology, Paleontology, and Paleoecology

Rudabánya is located within the Pannonian Basin, on the western flank of the northern Carpathian Mountains, in northeastern Hungary (N48°22'48.13", E20°37'43.57"). The fossiliferous deposits at Rudabánya accumulated in a shallow valley near the shoreline of Lake Pannon, a relict of the Paratethys Sea, which formed approximately 11.6 Ma (Kázmér, 1990, Rögl, 1998; Magyar et al., 1999; Popov et al., 2004) (Figure 2.1). As lake levels gradually rose, the Rudabánya range and adjacent valleys were flooded, creating a variety of lacustrine and peri- lacustrine environments including swamp, wetland, and riparian forest. Lake Pannon reached its maximum extent (c. 290,000 km2) between 10.5 – 10 Ma, during a period of high precipitation and humidity (Magyar et al., 1999; Harzhauser and Mandic, 2004, 2008; Harzhauser et al., 2007,

2008). There are a number of fossiliferous localities within the Rudabánya complex; here we focus on fauna from the R. II locality, where the majority of primate material has been recovered. Cyclic layers of clay, mud, and lignite totaling 8–12 meters characterize the depositional sequence at this locality. While the sequence is too short to tie into the geomagnetic time scale, having likely accumulated within a few thousand years or less, the evolutionary stage of the fauna suggests it belongs near the top of the MN9 land mammal zone (10 – 9.8 Ma) (Kordos, 1991; Andrews et al., 1996; Bernor et al., 2003; Andrews and Cameron, 2010; Casanovas-Vilar et al., 2011a).

The faunal assemblage at R. II is extraordinarily diverse with 112 vertebrate species, including 18 species of amphibians, 13 species of reptiles, 11 species of birds, and 69 species of mammals. Ungulate taxa are dominated by morphologically inferred browsers including Dorcatherium naui (Tragulidae), Micromeryx flourensianus (Moschidae), Miotragocerus sp. (Bovidae), Tapirus cf. priscus (Tapiridae), Chalicotherium aff. goldfussi (Chalioctheriidae), Hoploaceratherium belvederense, and Aceratherium incisivum, and Lartetotherium aff. sansaniensis (Rhinocerotidae) (Bernor et al., 2004). Meso- and microwear data indicate intermediate feeding (i.e., both browsing and grazing), which included the intake of C3 graminoids, in Hippotherium intrans (Equidae) and Lucentia aff. peirensis (Cervidae) (Merceron et al., 2007). This suggests some presence of more open canopy habitats, such as forest clearings, where higher levels of light penetration promote the development of an herbaceous layer. The gomphothere Tetralophodon longirostris likely also inhabited more open canopy habitats distal to the lake margin. Stable isotope and microwear analysis of Late Miocene gomphotheres from Central and Western Europe generally indicate intermediate feeding in woodland environments (Calandra et al., 2008; Domingo et al., 2009; 2012; Tütken and Venneman, 2009). The suids at R. II include a suine, Propotamochoerus palaeochoerus, first known from the Middle Miocene, and a primitive tetraconodont, Parachleuastochoerus kretzoii (Bernor et al., 2004). This locality represents one of the very few in Eurasia that preserves extensive samples of both a hominoid and pliopithecoid (Andrews et al., 1996: Harrison et al., 2002; Kordos and Begun, 2002; Armour-Chelu et al., 2005). Rudapithecus and Anapithecus hernyaki have been recovered from the same depositional layers although, interestingly, their frequency differs between layers (Andrews et al., 1997; Kordos and Begun, 2002; Armour-Chelu et al., 2005). The majority of hominoid (i.e., Rudapithecus) material has been recovered from

27 the black mud layer, while most of the pliopithecoid (i.e., Anapithecus) material derives from the gray marl layer. Kordos and Begun (2002) note the lack of faunistic difference between these depositional layers and suggest that they sample overlapping faunal communities. Similarly, Eastham et al. (2011) found no significant difference in the carbon and oxygen stable isotope values of fauna from the black mud and gray marl, supporting little, if any, difference in environmental conditions. This investigation analyzes fauna from the black mud and gray marl as one community.

The local vegetation at R. II reflects a swamp association dominated by deciduous taxa such as Osmunda parschlugiana, Ginkgo adiantoides, Glyptostrobus europaeus, Acer div. sp., Alnus div. sp., Banisteriaecarpum giganteum, Byttneriophyllum tifiifolium, Caprinus grandis, Cercidiphyllum crenatum, Daphnogene sp., Nyssa disseminata, Potamogenton martinianus, Salix varians, Stratiotes tuberculatus, Trapa silesiaca, Ulmus sp., Zelkova zelkovifolia, and a rare relict element, Daphnogene (Lauraceae) (Kretzoi et al., 1976; Halby and Erdei, 2013). Paleoclimatic estimates for Rudabánya were modeled by Utescher et al. (2017) using plant functional types (PFTs). Results suggest a mean annual temperature (MAT) of 16°C, and a mean annual precipitation (MAP) of over 1100 mm/yr. Clear seasonality was established at this time, with both a colder and dryer and a warmer and wetter season (Damuth et al., 2003). Rainfall and temperature estimates suggest a subtropical or at least humid warm-temperate climate compared to today. These data correspond with those for other nearby early Late Miocene localities (Bruch et al., 2006, 2007, Harzhauser et al., 2007; 2008; Kern et al., 2012; Utescher et al., 2017).

2.2 Stable Carbon Isotope Values in Mammalian Enamel

Stable isotope values of tooth enamel record an animal’s diet and drinking habits during tooth formation. Carbon isotope values reflect the isotopic composition of the plants eaten, with a consistent enrichment factor due to metabolic processes and equilibrium constraints. The enrichment factor for mammalian bioapatite ranges from 12‰ to 14‰ due to differences in the digestive physiology of herbivores (ruminant vs. non-ruminant; Lee-Thorp and van der Merwe, 1987; Lee-Thorp et al., 1989; Cerling and Harris, 1999; Passey et al., 2005). Cerling and Harris (1999) observed an average diet to enamel enrichment factor of 14.1‰±0.5‰ for large ruminant ungulates. These authors also report similar enrichment factors for large non-ruminant ungulates

28 such as rhinocerotids (14.4‰±1.6‰) (Cerling and Harris, 1999). A controlled feeding experiment by Passey et al. (2005) showed the influence of digestive physiology on the enrichment factor. Domestic cattle (ruminant) were shown to have a higher enrichment factor (14.6‰±0.7‰) than pigs 13.3‰±0.3‰ (non-ruminants) (Passey et al., 2005). To calculate the isotopic values present at R.II, following Passey et al. (2005), we applied an enrichment factor of 13.3‰±0.3‰ to the suids, and 14.1‰±0.5‰ to all other ungulate herbivores, after Cerling and Harris (1999).

13 Modern C3 plants have a global mean δ C value of −27‰ and range between −22‰ and 13 −36‰. This wide range of δ C values exhibited by C3 vegetation is the result of variation in environmental factors such as solar radiation, water and nutrient availability, and temperature (Farquhar et al., 1982; Ehleringer et al., 1987; O’Leary, 1988; van der Merwe and Medina, 1991; Ehleringer and Monson, 1993; Koch, 1998; Heaton, 1999; Diefendorf et al., 2010; Kohn, 2010). Open and closed canopy forests display a stratification of δ13C leaf values, wherein values decrease from the upper to lower canopy (van der Merwe and Medina, 1991; Cerling et al., 2004). This stratification has been related to decreased solar radiation and the recycling of 13C- depleted CO2 under the forest canopy (Vogel, 1978; Ehleringer et al., 1986; van der Merwe and 13 Medina, 1989; 1991; Hanba et al., 1997; Heaton, 1999). C3 plants typically display lower δ C values in closed canopy environments such as rainforests, and higher values in drier, open canopy environments such as woodlands (van der Merwe and Medina 1991; Cerling et al., 1999; Heaton, 1999; Cerling et al., 2004). Kohn (2010) complied the δ13C values of trees, shrubs, and 13 grasses from a broad range of modern C3 biomes and reports a monotonic increase in δ C values with decreasing MAP. Kohn (2010) also reported a correlation between MAP and the δ13C values of fossil tooth enamel and collagen, which could be used to assess moisture levels at ancient sites.

13 Both the CO2 concentration and the δ CCO2 value of the atmosphere have fluctuated through time, affecting the δ13C value of plants and ultimately mammalian tooth enamel (Friedli et al., 1986; Marino and McElroy, 1991; Marino et al., 1992). As a result of the Industrial 13 Revolution and fossil fuel burning mean atmospheric δ CCO2 values have become lower by about 1.5‰ over the last few hundred years (Friedli et al., 1986; Marino and McElroy, 1991; Marino et al., 1992). Using isotopic data derived from benthic foraminifera, Tipple et al. (2010) 13 reconstructed variation in δ CCO2 values for the Cenozoic. Following these measurements a

13 δ CCO2 value of –6‰ can be estimated for the Miocene (2‰ higher than the modern atmosphere) (Tipple et al., 2010). This means that Miocene mammals feeding on C3 plant 13 resources are expected to have δ CE values ranging between −22‰ and −6‰, with –22‰ to – 13‰ for those feeding under a relatively closed canopy, −13‰ to −8‰ in mesic woodland environments, and <–8‰ for more open/arid C3 vegetation (Cerling and Harris 1999; Bocherens 2003; Kohn et al., 2005).

2.3 Stable Oxygen Isotope Values in Mammalian Enamel

18 Oxygen isotope values of mammalian enamel (δ OE) can be used to reconstruct habitat preference, drinking behavior, and local climatic conditions (Kohn et al., 1996; Levin et al., 2006; Zanazzi and Kohn, 2008; Ecker et al., 2013). Herbivorous mammals obtain water either through drinking or the plants they consume. The δ18O values of meteoric water are influenced by variations in air temperature, relative humidity, and the amount of precipitation (Dansgaard, 18 1964; Ayliffe et al., 1992; Rozanski et al., 1993). Interpreting δ OE values is complicated by the complex nature of oxygen flux in mammals. Taxa that drink frequently generally reflect lower 18 18 δ OE values, whereas drought-tolerant animals usually have higher δ OE values because they obtain proportionally more water from 18O-enriched food sources such as leaves, fruits, or seeds (Kohn, 1996; Levin et al., 2006). The δ18O values of plant leaves are enriched compared to roots or stems due to evapotranspiration (Dongmann et al., 1974; Epstein et al., 1977; Yakir, 1992). A vertical enrichment gradient similar to the carbon isotope canopy effect has been observed for δ18O values in forested environments (Stemberg et al., 1989; Krigbaum et al. 2013). The highest δ18O values are typically observed in areas with increased solar radiation and decreased humidity, such as forest gaps, along the forest edge, and in the upper canopy, while the lowest δ18O values are associated with the humid and densely vegetated forest floor (Stemberg et al., 1989; Quade et al., 1995; Cerling et al., 2004; Feranec and MacFadden 2006). Cerling et al. 18 (2004) showed that fauna inhabiting closed-canopy forest or swampy habitats reflect lower δ OE values due to increased humidity, and thus decreased evapotranspiration.

Here, stable isotope data are reported in conventional delta (δ) notation for carbon (δ13C) 18 13 13 12 and oxygen (δ O), where δ C (parts per mil, ‰) = ((Rsample/Rstandard)-1)*1000, and R= C/ C; 18 18 16 and δ O (parts per mil, ‰) = ((Rsample/Rstandard)-1)*1000, and R= O/ O. The δ values are quoted in reference to international standards: V-PDB for carbon and oxygen, and for oxygen

Vienna Standard Mean Ocean Water (V-SMOW). If not noted otherwise, V-PDB values are used. δ18O values measured in V-PDB were converted to V-SMOW using the following

formula: δ18O (V-SMOW)=[δ18O (V-PDB) x 1.03086]+30.86.

Taxon Family N δ13CE (V-PDB, ‰) δ18OE (V-PDB, ‰) (V-SMOW, ‰)

Mean SD Range Mean SD Range Mean Aceratherium incisivum Rhinocerotidae 5 −11.3 1.1 −12.4 To −10.1 −9.0 0.5 −9.6 to −8.2 21.6 Chalicotherium aff. goldfussi Chalicotheriidae 1 −13.9 - - - - −4.7 - - - 26 Dorcatherium naui Tragulidae 4 −16.0 1.8 −17.0 To −13.4 −5.8 0.5 −6.2 to −5.1 24.9 Hippotherium intrans Equidae 12 −12.7 0.6 −13.2 To −11.0 −7.2 1.2 −8.3 to −4.2 23.4 Lucentia aff. pierensis Cervidae 13 −12.2 0.7 −13.3 To −11.0 −5.5 1.7 −8.2 to −2.6 25.2 Micromeryx flourensianus Moschidae 8 −13.7 0.7 −14.7 To −12.8 −5.9 2.3 −8.2 to −2.3 24.8 Miotragocerus sp. Bovidae 8 −13.2 0.8 −14.1 To −11.5 −6.2 1.6 −9.3 to −3.6 24.5 Parachleuastochoerus kretzoii Suidae 5 −12.3 0.4 −12.5 To −11.6 −7.5 0.7 −8.5 to −6.8 23.1 Propotamochoerus palaeochoerus Suidae 4 −10.5 0.9 −11.8 To −9.7 −7.3 0.9 −8.3 to −6.2 23.3 Tetralophodon longirostris Gomphotheriidae 2 −12.8 0.1 −12.8 To −12.7 −8.7 0.3 −8.9 to −8.4 21.9

Table 2.1 Descriptive statistics for the R. II fauna analyzed in this study.

3 Materials and Methods

We analyzed the tooth enamel of 62 specimens (Appendix A) from 10 genera (Table 2.1). Because the goal of our analysis was to examine variation in the diet of adult animals, we preferentially sampled teeth that are among the last to develop, mineralize, and erupt (Hillson, 2005). Enamel (~ 5–10 mg) was removed using a low speed FOREDOMTM drill and carbide dental burs. 2-3 mm wide samples were taken along the non-occlusal surface parallel to the growth axis across the entire length of the tooth, which provides average values of resource use during tooth development, typically representing many months to a few years. Powdered enamel samples were chemically pretreated prior to isotopic analysis using hydrogen peroxide (30%,

H2O2) to remove organics and weak acetic acid (0.1 M, CH3CO2H) to remove secondary carbonates. Samples were centrifuged at a high speed and rinsed in distilled water to neutral pH before proceeding with the next solution. This sampling procedure generally follows the methods of MacFadden and Cerling (1996) and Koch et al. (1997). Approximately 1-2 mg of treated enamel was used for carbon and oxygen analyses. This was performed using a Thermo-

Finnigan MAT 253 gas source isotope ratio mass spectrometer via a Finnigan Gas Bench at the Stable Isotope Laboratory of the University of Toronto (Canada).

The measured carbon and oxygen isotope compositions were calibrated using the NBS-19 standard then to V-PDB (PeeDee Belemnite) following the Vienna (V-) convention. Two replicate samples were analyzed in duplicate, with a precision of ±0.2‰.

sp.

Species pierensis

D. naui

H. intrans

P. kretzoii

aff.

A. incisivum

L. L. M. flouresianus

P. palaeochoerus Miotragocerus 0.000* D. naui 0.002* 0.002* 0.000* H. intrans 0.024 0.101 0.037 0.000* 0.147 L. aff. pierensis 0.000* 0.74 0.006 0.000* 0.000* 0.011 0.000* M. flouresianus 0.001* 0.887 0.06 0.539 Miotragocerus 0.000* 0.000* 0.21 0.012 0.222 sp. 0.001* 0.675 0.129 0.322 0.734 0.066 0.000* 0.324 0.911 0.004 0.057 P. kretzoii 0.114 0.083 0.677 0.012 0.059 0.11 0.169 0.000* 0.000* 0.001* 0.000* 0.000* 0.003 P. palaeochoerus 0.085 0.153 0.915 0.038 0.132 0.216 0.812 0.036 0.000* 0.913 0.379 0.165 0.533 0.466 0.003* T. longirostris 0.766 0.028 0.201 0.007 0.022 0.037 0.364 0.29

13 18 Table 2.2 Significant differences in δ CE (top) and δ OE (bottom) values among the R. II fauna. Values shown in bold indicate significance for α≤0.05 using Fisher’s least significant difference test. Pairs that were also significant using Tukey's post hoc test are indicated by asterisks.

Isotope values were compared among taxa using parametric (ANOVA, Fisher’s LSD, Tukey’s HSD) and non–parametric (Kruskal-Wallis) tests where appropriate. Statistical analyses were run on SPSS 22.0, with significance set at p ≤0.05.

4 Results 4.1 Stable Carbon Isotope Values

13 The δ CE values of the R. II fauna displayed a range between −17.0‰ and −9.7‰ and a 13 mean value of −12.7‰ (Table 2.1). The mean δ CE values of different taxa range between 13 −16.0‰ and −10.5‰. We found statistically significant differences in the δ CE values among 13 taxa (Table 2.2). The small tragulid Dorcatherium naui displayed the lowest δ CE values of all sampled taxa (x̅ = −16.0‰, n = 4, p = 0.000, Fisher’s LSD). The chalicothere Chalicotherium aff. golfussi (−13.9‰, n = 1), moschid Micromeryx flourensianus (x̅ = −13.7‰, n = 8), and 13 bovid Miotragocerus sp. (x̅ = −13.2‰, n = 8) showed comparable δ CE values and are not statistically significantly different. Sympatric suids, Propotamochoerus palaeochoerus (x̅ = −10.5‰, n = 4) and Parachleuastochoerus kretzoii (x̅ = −12.3‰, n = 5), as well as the rhinoceros Aceratherium incisivum (x̅ = −11.3‰, n = 5), and cervid Lucentia aff. pierensis (x̅ = 13 −12.2‰, n = 13) yielded relatively higher δ CE values. Propotamochoerus palaeochoerus 13 displayed significantly higher δ CE values than the other taxa analyzed, with the exception of Aceratherium incisivum (x̅ = −11.3‰, p = 0.169, Fisher’s LSD) (Table 2.2). The equid Hippotherium intrans (x̅ = −12.7‰, n = 12), and gomphothere Tetralophodon longirostris (x̅ = 13 −12.8‰, n = 2) yielded mean δ CE values almost equivalent with that of the locality mean (x̅ = −12.7‰).

4.2 Stable Oxygen Isotope Values

18 The δ OE values of the R. II fauna displayed a range between −9.6‰ and −2.3‰ (Table 18 2.1) and a mean value of −6.7‰. The mean δ OE values of the different taxa range between 18 −9.0‰ and −4.7‰. We found statistically significant differences in δ OE values among taxa 13 (Table 2.2), however, they were fewer than those found based on δ CE. The gomphothere T. longirostris (x̅ = −8.7‰, n = 2) and rhinoceros A. incisivum (x̅ = −9.0‰, n = 5) yielded the 18 18 lowest δ OE values of the sampled taxa. Aceratherium incisivum has significantly lower δ OE

33 values than all other taxa, with the exception of P. kretzoii, P. palaeochoerus, and T. longirostris (p = 0.114, 0.085, and 0.766, respectively, Fisher’s LSD) (Table 2.2). Miotragocerus sp. M. 18 flourensianus, and D. naui, share similarly higher δ OE values that range between −6.2‰ and −5.8‰. The cervid L. aff. pierensis (x̅ = −5.5‰, n = 13) and chalicothere C. aff. golfussi (x̅ = 18 −4.7‰, n = 1) displayed the highest mean δ OE values. Lucentia aff. pierensis yielded 18 significantly higher δ OE values than A. incisivum, H. intrans, P. kretzoii, P. palaeochoerus, and T. longirostris (p = 0.000, 0.006, 0.012, 0.038, and 0.007, respectively, Fisher’s LSD).

13 18 Figure. 2.2 Scatter plot of mean values and total ranges of δ CE and δ OE from the R. II fauna. Trends from more humid/closed canopy environment to dry/open environment are indicated.

5 Discussion 5.1 Mammalian Paleoecology: Resource Use and Partitioning

13 All of the R. II fauna included in this study have δ CE values consistent with a diet of C3 vegetation. This finding is in accordance with previous isotopic studies of Miocene ecosystems

34 in Europe (Bocherens et al., 1994b; Hernández-Fernández et al., 2006; Merceron et al., 2006, 2013; Tütken et al., 2006; 2013; Domingo et al., 2009; 2012; 2013; Tütken and Vennemann, 2009; Rey et al., 2013; Aiglstorfer et al., 2014). We found significant differences in the isotopic values of the sampled fauna (Figure 2.2) indicating that the R. II herbivores partitioned their resources by selecting different plant foods and occupying different habitats within the local environment. These results support the niche partitioning hypothesis, which predicts that ecologically similar species coexist by partitioning resources in at least one of the three primary 13 niche dimensions (food, space, time) (Schoener, 1974; Pianka, 1981). Lower δ CE values displayed by M. flourensianus(–14.7 to –12.8‰), Miotragocerus sp. (–14.1 to –11.5‰), and D. naui (–17.0 to –13.4) imply a preference for browsing under a more dense forest canopy, while relatively higher values displayed by A. incisivum (–12.4 to –10.1‰) , P. palaeochoerus (–11.8 to –9.7‰), P. kretzoii (–12.5 to –11.6‰) , L.. aff. pierensis (–13.3 to –11.0‰) and H. intrans (–13.2 to –11.0‰) likely indicate a preference for relatively more open canopy habitats. A similar range of isotopic values was measured for several taxa indicating some interspecific 13 competition for dietary resources. The two suids share similarly higher δ CE values with the 13 18 rhinoceros, while the equid, cervid, and bovid share an intermediate range δ CE and δ OE 13 18 values, and the two small ruminants share lower δ CE and relatively higher δ OE values. An abundance of plant resources within the local forest environment likely facilitated the coexistence of this diverse community of predominantly browsing herbivores.

5.1.1 Mammalian Paleoecology in Open Canopy Habitats

The isotope values of the suids, rhinoceros, gomphothere, equid, cervid, and chalicothere indicate the presence of more open canopy forest habitats at R. II. Propotamochoerus 13 palaeochoerus, the larger of the two suids sampled from R. II, has a mean δ CE value (x̅ = −10.5‰) that is 2.2‰ higher than the locality mean (x̅ = −12.7‰), and significantly higher than all other taxa, with the exception of the rhinoceros Aceratherium incisivum (x̅ = −11.3‰). After 13 accounting for dietary (13.3‰±0.3‰) and atmospheric (1.5‰) enrichment the average δ C value of plants consumed by P. palaeochoerus is −25.3‰, a value consistent with more open- 13 canopy C3 environment (Farquhar et al., 1989; Cerling et al., 2004). The range of δ CE values (−11.8‰ to −9.7‰) shown by P. palaeochoerus further supports a preference for feeding in 13 open canopy habitats, such as forest gaps or clearings. A similar range of δ CE values has been reported for Propotamochoerus hysudricus in Late Miocene Pakistan and in Myanmar (Nelson,

2007; Maung-Maung-Thein et al., 2011). Microwear analysis of P. hysudricus from the Late Miocene Siwaliks suggests an omnivorous diet similar to the extant bush pig Potamochoerus 13 porcus (Nelson, 2003). Isotopic analysis of modern P. porcus revealed a mean δ CE value of −9.4‰, which is comparable with that of P. palaeochoerus from R. II (Harris and Cerling, 2002). Armour-Chelu et al. (2003) examined the pattern of tooth emergence and wear in P. palaeochoerus and suggest many similarities to the highly omnivorous extant wild boar Sus scrofa, whose diet includes rhizomes, fruits, leaves, insects, and small mammals. P. 13 palaeochoerus has significantly higher δ CE values than the smaller peccary-like suid, Parachleuastochoerus kretzoii (x̅ = −12.3‰), which could indicate greater consumption of fruits and grasses, both of which are expected to have higher δ13C values. The calculated mean δ13C value of the plants consumed by P. kretzoii (x̅ = −27.1‰) is close to the global average for C3 18 plants (x̅ = −27.0‰). Both of the R. II suids have relatively low δ OE values, which could be attributed to the consumption of roots and tubers, as these resources are lower in 18O compared to leaf or fruit water (Dunbar and Wilson, 1983; Yakir; 1992) and would have been plentiful in the soft substrates surrounding Lake Pannon. Several authors have linked the lower oxygen isotope values of extant and fossil suids to a strong dependence on rhizomes (Bocherens et al. 1996; Sponheimer and Lee-Thorp 2001; Lee-Thorp and Sponheimer 2003; Tütken et al., 2006; 18 Domingo et al., 2009; 2012; Aiglstorfer et al., 2014). The average δ OE value of P. kretzoii (x̅ = −7.5‰) is slightly lower than that of P. palaeochoerus (x̅ = −7.3‰), and is comparable with those reported for other Middle and Late Miocene tetraconodontid suids (Parachleuastochoerus steinheimensis and Conohyus simorrensis) in Europe (Tütken et al., 2006; Domingo et al., 2009; 2012; Aiglstorfer et al., 2014). While it is likely that both of the R. II suids engaged in rooting, 13 18 the lower δ CE and δ OE values of P. kretzoii suggest a greater dependence on rhizomes. The drinking-dependent behavior of suids (Harris and Cerling, 2002) might also account for the 18 relatively low OE values in both P. palaeochoerus and P. kretzoii, as obligate drinking mammals tend to have the lowest δ18O values in terrestrial faunas (Kohn, 1996; Levin et al., 2006).

13 The δ CE values of the rhinoceros Aceratherium incisivum (x̅ = −11.3‰, n = 5) also indicate a preference for browsing in open canopy habitats. A. incisivum has significantly higher 13 δ CE values than all other taxa, with the exception of the suids. These values suggest a similar habitat preference to extant browsing rhinoceroses, such as the Javan rhinoceros, Rhinoceros

36 sondaicus, and the Sumatran rhinoceros, Diceros sumatrensis, which feed on fruits, shoots, and leaves in forest clearings and shrublands (Nowak, 1991). Several isotopic studies have documented variation in the ecology of browsing rhinoceroses in Europe during the Miocene, with Aceratini (Aceratherium sp., Plesiacertherium fahlbuschi, Hoploacertherium sp., Alicornops simorrense) occupying a niche between that of the more open-country adapted Rhinoceratini (Lartetotherium sansaniense), and more closed-forest adapted Teleoceratini (Brachypotherium, Prosantorhinus germanicus) (Tütken et al., 2006; Tütken and Vennemann, 13 2009; Domingo et al., 2012; Aiglstorfer et al., 2014). The δ CE values of A. incisivum from R. II are comparable with those reported for other Aceratherines from the Steinheim Basin and from Sandlezhausen, Germany (Tütken et al., 2006; Tütken and Vennemann, 2009). In contrast, the 18 δ OE values A. incisivum are approximately 1-2‰ lower than those reported from Steinheim and Sandelzhausen, which could indicate comparatively more humid and wet conditions at R. II. Similar humid wetland-forest conditions have been interpreted for A. incisivum at the slightly earlier Late Miocene Şupanu Formation in Eastern Romania (Tabara and Chirila, 2011).

A. incisivum and the gomphothere Tetralophodon longirostris share comparable mean 18 δ OE values (x̅ = −9.0‰ and −8.7‰, respectively), which are the lowest of the sampled R. II 18 fauna. Large-bodied browsing herbivores generally display lower δ OE values relative to coexisting mixed feeders or grazers because they have lower metabolic rates and drink frequently from less evaporated sources (Bryant and Froelich, 1995). While these 18 13 megaherbivores are similar in δ OE values, they differ significantly in δ CE values, suggesting a 13 difference in diet. The mean δ CE value of T. longirostris (x̅ = −12.8‰, n = 2) suggests 13 18 browsing on leaves and shoots under an open forest canopy. Both the δ CE and δ OE values of T. longirostris are lower than those that have been reported for gomphotheres at similarly aged localities in Europe (Tü tken et al., 2006; Tü tken and Vennemann 2009; Domingo et al. 2009, 2012), indicating a lower degree of mixed feeding in a more humid and wet environment. Interestingly, the isotopic values of T. longirostris are more similar to those reported for Late Miocene deinotheres, which are suggested to have browsed in mesic woodland environments (Aiglstorfer et al., 2014).

A wide spectrum of dietary and habitat preference has been shown amongst Neogene hipparionines (Eisenmann, 1998; MacFadden et al., 1999; Solounias and Semprebon, 2002; Bernor et al., 2003; Scott et al., 2005; Merceron et al., 2007; Merceron, 2009; Tütken et al.,

2013). Microwear data for Hippotherium intrans, a derived member of the Hippotherium primigenium lineage, is unlike that of any living browser and suggests the possibility of both 13 grazing and browsing (Merceron et al., 2007). H. intrans yields intermediate δ CE values (x̅ = −12.7‰), which are significantly higher than Dorcatherium naui and Micromeryx flouresianus, and lower than Aceratherium incisivum and Propotamochoerus palaeochoerus. An isotopic and meso- and microwear study by Tütken et al. (2013) showed significant inter-site differences in the enamel isotopic values of H. primigenium at four early Late Miocene localities in Western 13 18 Europe. Lower δ CE and δ OE values measured for the H. primigenium populations from Eppelsheim, Germany and Charmoille, Switzerland, suggest feeding in a predominantly forested 13 18 environment, while higher δ CE and δ OE values measured for the populations from Höwenegg,

Germany and Soblay, France, indicate feeding in more open and dry C3 habitats (Tütken et al., 13 2013). The δ CE values of H. intrans from R. II fall between those of the forested and more 18 open dwelling H. primigenium populations sampled by Tütken et al. (2013), while the δ OE are 13 more similar to those of the forest dwelling populations. At R. II the δ CE values of H. intrans are most similar to the cervid Lucentia aff. pierensis (x̅ = −12.2‰, n = 13), suggesting that both taxa foraged for leaves and shoots under a relatively open forest canopy. Lucentia aff. pierensis 18 has significantly higher δ OE values than H. intrans, indicating preferential feeding on vegetation exposed to higher levels of solar radiation and subject to greater evapotranspiration, such as grasses and fruits fallen from the forest canopy. Meso- and microwear data for L. aff. pierensis reflect intermediate or mixed feeding, similar to the flexible feeding habits of many 18 modern cervids (Merceron et al., 2007). The wide range of δ OE values displayed by L. aff. pierensis (−8.2‰ to −2.6‰) implies the use of varied sources of drinking water and an interpretation of a flexible feeding strategy.

The large-bodied, knuckle–walking, perissodactyl Chalicotherium aff. goldfussi is a rare faunal element at R. II, represented by a single individual in the current study. Chalicotheres are typically associated with forested settings; however, their presence does not necessarily indicate a dense forest canopy. It has been suggested that chalicotheres could stand bipedally, using their laterally compressed ungual phalanges and large claws to pull down leaves from the midcanopy 13 18 13 (Benton, 1990). The δ CE and δ OE values support this style of browsing. Similar δ CE and 18 δ OE values have been reported for Middle Miocene chalicotheres from Sandelzhausen (Tütken

38 and Vennemann, 2009), and Late Miocene chalicotheres from the Siwaliks, Pakistan (Nelson, 2007).

5.1.2 Mammalian Paleoecology in Closed Canopy Habitats

Isotope values of the bovid, tragulid, and moschid indicate the presence of more densely closed canopy forest habitats at R. II. The dietary and habitat preferences of modern bovid browsers are highly diverse, ranging from the folivorous dibatag (Ammodorcas clarkei) found in the arid lowlands of Ethiopia and Somalia, to the more frugivorous duiker (Cephalophus sp.) found in the lowland rainforests of western and central Africa (Yalden et al., 1984; Lumpkin and 13 Kranz, 1984; Nowak, 1999). The fossil bovid Miotragocerus sp. yielded a wide range of δ CE 18 (−14.1‰ to −11.5‰) and δ OE (−8.4‰ to −3.6‰) values, suggesting that this species foraged 13 and drank in a spectrum of closed and more open canopy habitats. The δ CE values of Miotragocerus sp. are significantly lower than A. incisivum, P. palaeochoerus, and L. aff. pierensis, and significantly higher than D. naui. Meso and microwear data for Miotragocerus sp. suggest a traditional style of browsing, with a small component of fruit and seed feeding 13 18 (Merceron et al., 2007). Higher δ CE and δ OE values could indicate the seasonal consumption of fruits, and these data support those of Merceron et al. (2007), as well as several other studies of Miotragocerus (Solounias and Dawson-Saunders, 1988; Spassov and Geraads, 2004; Merceron et al. 2006; Merceron, 2009).

13 The δ CE values of the tragulid Dorcatherium naui (x̅ = −16.0‰) and moschid Micromeryx flourensianus (x̅ = −13.7‰) are significantly lower than all other sampled taxa (Table 2.2) suggesting a preference for browsing in humid habitats under a closed forest canopy.

In this type of habitat, where light levels are low and there is recycling of CO2 (van der Merwe 13 and Medina 1989), mammals can yield δ CE values lower than −14‰ (Cerling and Harris, 1999; 13 Cerling et al., 2004; Kohn et al., 2005). Cerling et al. (2004) report a similar range of δ CE values (−16.0‰ to −14.1‰) for extant duikers (Cephalophus sp.) and water chevrotains (Hyemoschus aquaticus) in the Ituri Forest, Democratic Republic of Congo. Both duikers and water chevrotains inhabit the forest floor and feed on fruits, seeds, and leaves fallen from the forest canopy (Cerling et al., 2004). Meso- and microwear data for M. flourensianus and D. naui from Atzelsdorf, a slightly earlier Late Miocene locality in Austria, suggest selective fruit browsing by both taxa (Merceron, 2009). Merceron et al. (2007) analyzed the microwear pattern

39 of M. flourensianus from R. II and also suggest year-round fruit browsing by the moschid. Isotopic data for M. flourensianus from the Steinheim Basin and from Gratkorn, a late Middle 13 18 Miocene locality in Austria, show comparable but somewhat higher δ CE and δ OE values 18 (Tütken et al., 2006; Aiglstorfer et al., 2014). The δ OE values reported for D. naui from Gratkorn are also similar, but slightly higher, than those measured at R. II. Interestingly, the 13 δ CE values of D. naui from Gratkorn (x̅ : −9.9‰) are markedly higher than those from R. II (x̅ : −16.0‰) and are unexpected given the habitat preference of modern Tragulidae (Aiglstorfer et al., 2014). Paleoenvironmental reconstructions of Gratkorn indicate an open canopy woodland environment, with a semi-arid, subtropical climate (MAP: 486± 252 mm/yr; MAT: ~15°C), and distinct seasonality (Gross et al., 2011b; Aiglstorfer et al. 2014). In this type of environment, year-round access to fruit would be unlikely and low MAP would preclude the development of a closed canopy forest. The lower isotopic values of D. naui at R. II likely reflect a more humid, wet, and closed canopy forest environment as well as a diet that may have included leaves and shoots growing the dense subcanopy in addition to fruits and seeds.

5.2 The Paleoenvironment of Rudapithecus hungaricus

The R. II fauna provide evidence of a diverse wetland-forest environment, with a range of habitat types from closed to open canopy. These findings are consistent with previous palaeoecological reconstructions (Kordos and Begun, 2002; Bernor et al., 2003; Scott et al., 13 2005; Merceron et al., 2007). The higher δ CE values displayed by the rhinoceros, cervid, suids, and equid are indicative of more open canopy habitats. However, the complete lack of strict grazers and limited presence of mixed or intermediate feeders suggests that forested settings were substantial enough to support a diverse population of browsers. Approximately 43% of the 13 sampled taxa yield δ CE values ≤−13‰, suggesting a relatively dense forest canopy. The mean modern δ13C value of temperate deciduous flora ranges between approximately −26‰, in relatively open canopy forests, and –30‰, in forests with relatively dense canopies (Garten and Taylor, 1992; Tu et al., 2004). After accounting for dietary (14.1±0.5‰) and atmospheric enrichment (1.5‰), the mean δ13C value of plants eaten by the R. II fauna is −28.3‰. This value is almost identical to that measured for modern deciduous subtropical vegetation (−28.4‰) in the Okefenokee Swamp-Forest, southern Georgia, USA (DeLucia and Schlesinger, 1995), and is also comparable with that of mixed mesophytic forests in east-central North America (−29.4‰; Walker Branch Watershed, Tennessee; Garten and Taylor, 1992; Garten et al., 2000). Within the

40 gradient of open to closed canopy forest at R. II Rudapithecus would have likely occupied more humid, and densely closed canopy habitats. The postcranial morphology of Rudapithecus is consistent with adaptations related to derived suspensory arboreality suggestive of the presence of densely closed canopy forest at or near R. II, including strongly curved phalanges (Begun, 1988; Deane and Begun, 2008), and features of the elbow, wrist and femur (Begun 1992; 2007; Kordos and Begun, 2002; Kivell and Begun 2009).

Our isotopic data are congruent with the results of previous meso and microwear studies suggesting the consumption of fruit by several taxa including the small ruminants, bovid, and cervid (Merceron et al., 2007; 2009). These findings are supported by the abundance of fruit endocarps recovered from R. II (Kordos and Begun, 2002; Hably and Erdei, 2013). The presence of taxa exploiting fruit resources has important implications for Rudapithecus, which has been identified as a dedicated soft fruit frugivore on the basis of dental microwear, shearing crest development, and molar cusp proportions (Ungar, 1996; 2005; Teaford and Ungar, 2000). More recent interpretations of incisor shape and curvature suggest elevated compressive loads in the incisor region that are consistent with the removal of tough protective fruit pericarps (Deane et al., 2013). An affinity for hard fruit feeding was also reported by DeMiguel et al. (2014), who examined the microwear of Late Miocene Western Eurasian hominoids in correlation with a sample of modern primates. The combination of a soft and hard fruit feeding signal could indicate a fall back feeding strategy that allowed Rudapithecus to exploit harder fruiting resources during short-term (seasonal) periods of ripe fruit shortage

While the current study did not evaluate seasonal variation in climate, the relatively low 18 mean δ OE values in all of the sampled fauna suggest that Rudapithecus experienced generally humid and wet climatic conditions. This interpretation is consistent with those derived from other proxies (Damuth et al., 2003; van Dam, 2006; Böhme et al., 2008, 2011; Hably and Erdei, 2013; Utescher et al., 2017), however, it must be viewed with caution as the enamel sampling strategy undertaken in the current study provides average isotope values for the span of tooth formation, which may have been concentrated during more biologically productive periods of the year (spring/summer). Modern mammals inhabiting humid and wet environments generally 18 18 yield lower δ OE values due to decreased leaf water O-enrichment via evapotranspiration (Cerling et al., 2004). Humid and wet conditions are further supported by the relatively low 13 13 δ CE values found in the majority of the sampled fauna. In C3-dominated ecosystems the δ C

41 values of mammalian bone and enamel are correlated with the amount of precipitation and plant productivity as well as the ratio between potential evapotranspiration and MAP (Kohn and Law, 2006; Kohn, 2010).

The palaeoenvironmental interpretations presented here are consistent with proxy data for the early Late Miocene, which indicate warmer, wetter, and more humid conditions in Central Europe than today (e.g. Mosbrugger et al., 2005; van Dam, 2006; Harzhauser et al., 2007; 2008; Böhme et al., 2008, 2011; Utescher et al., 2009, 2011; 2016; Pound et al., 2011; Kern et al., 2012). Two episodes of anomalously high precipitation (≥ 1200mm/yr) have been proposed on the basis of herpetological data, occurring between 10.2 – 9.8 Ma and 9 – 8.5 Ma (Böhme et al., 2008). Geochemical and paleontological studies of Lake Pannon confirm a peak in precipitation and humidity between 10.5 and 10 Ma, during a phase of maximum lake extension (Harzhauser and Mandic, 2004; Harzhauser, 2007; Harzhauser et al., 2008; Gross et al., 2011a). It is likely that the faunal assemblage at R. II accumulated during this period when coastal environments were characterized by extensive marshes grading into forested-wetlands, and mixed evergreen and deciduous forest (Harzhauser et al., 2007; Hably and Erdei, 2013). Hably and Erdei (2013) document the presence of fossil mastixioid flora at R. II, and suggest that the Pannonian Basin acted as a refugium for thermophilic plant taxa during the Late Miocene. Modern Mastixia is geographically restricted to areas with a MAT above 19 °C and a MAP of approximately 2000 mm (Mai, 1997). Following its maximum extension (~10 Ma), Lake Pannon began to shrink in several phases beginning in the late Vallesian. By the middle Turolian, the northeastern margin of the lake had contracted significantly from its former extent and progradation almost completely filled the western portion of Hungary (Magyar et al., 1999). As lake the regressed more open deciduous woodlands replaced humid wetland-forests (Lueger, 1978; Bernor et al., 1996; Daxner-Höck, 2004; Harzhauser et al., 2004; 2007; Merceron et al., 2010). These environmental changes are reflected by the occurrence of more open country fauna such as hyenas, porcupines, and antelopes (Bernor et al., 1996; Harzhauser et al., 2004). While adaptations for efficient suspensory arboreality and hard fruit feeding would have allowed Rudapithecus to endure some degree of environmental fluctuation, the loss of humid forest habitats would have greatly impacted the continuing survival of this fossil ape.

5.3 Comparative Paleoecology of Late Miocene Hominoids in Western Eurasia

Considerable variation has been shown in the paleoecology of Late Miocene hominoids in Western Eurasia. The paleoenvironment of Rudapithecus is comparable with that reconstructed for Hispanopithecus laietanus and H. crusafonti, early Vallesian hominoids from the Vallès-Penedès Basin in Spain. These fossil apes were also large-bodied, suspensory frugivores found in association with wetland or humid subtropical forest habitats (Begun, 1992; Ungar and Kay, 1995; Ungar, 1996; Moyà-Solà and Köhler, 1996; Almécija et al., 2007; Alba et al., 2010ab; Marmi et al., 2012; DeMiguel et al., 2014). The decline of Hispanopithecus during the late Vallesian has been related to increasingly seasonal climatic conditions and the replacement of evergreen by deciduous forest (Agustí et al., 2003; Marmi et al., 2012; DeMiguel et al., 2014). Linear enamel hypoplasia, a dental developmental defect observed in Hispanopithecus (Skinner et al., 1995), suggests repeated episodes of malnutrition due to seasonal fluctuations in fruit resources (Eastham et al., 2009). Like Rudapithecus, Hispanopithecus shows locomotor and dietary adaptations that might have allowed for temporary survival during periods of environmental change (Begun, 1992; Moyà-Solà and Köhler, 1995; Almécija et al., 2007; Alba et al., 2010ab; Alba, 2012; DeMiguel et al., 2014). Ultimately, however, it is hypothesized that these adaptations could not prevent its extinction as humid forest habitats became progressively discontinuous and dominated by deciduous tree species during late Vallesian (Agustí et al., 2003; Marmi et al., 2012; DeMiguel et al., 2014).

The paleoenvironment of Ankarapithecus meteai from early Vallesian Turkey and Ouranopithecus macedoniensis from late Vallesian Greece differs greatly from that of hominoids in Central and Western Europe. These fossil apes are associated with more open and dry environments characterized by abundant C3 grasses and a developed herbaceous layer (Bonis et al., 1992; 1999; Fortelius et al., 1996; Merceron et al., 2005; 2010; 2013; Koufos, 2006; Koufos and Konidaris, 2011). Serial isotope analysis of fossil bovid enamel revealed that Ouranopithecus endured relatively cold winters, with temperatures dropping below 10 °C (Merceron et al., 2013). Cranial and post-cranial characteristics suggest that the Eastern Mediterranean hominoids were hard object feeders with adaptations for terrestrial locomotion (Bonis and Koufos 1993; 1997; Begun and Güleç, 1998; Merceron et al., 2005; Begun 2007; DeMiguel et al., 2014). Previous studies suggest that the extinction of hominoids in this region

43 was not related to a decrease in tree cover, but instead occurred in correlation with an increase in bushy sclerophyllous vegetation (Merceron et al., 2010; 2013). The more recent discovery of Ouranopithecus-like apes in association with early Turolian mammals in Turkey (Guleç et al., 2007), Bulgaria (Spassov et al., 2011), and Iran (Suwa et al., 2016) implies a less abrupt extinction for hominoids in the Eastern Mediterranean. It is interesting to note that slightly further east in Georgia, Udabnopithecus garedziensis, known only from an isolated maxillary fragment, is associated with fauna indicating a humid closed forest environment during latest Vallesian, roughly contemporaneous with Ouranopithecus (Vekua and Lordkipanidze, 2008; Casanovas-Vilar et al., 2011a).

Oreopithecus bambolii, the latest surviving Western Eurasian hominoid, inhabited a subtropical to warm-temperate mosaic environment within the Tusco-Sardinia paleobioprovince (Harrison and Harrison, 1989; Carnieri and Mallegni, 2003; Matson et al., 2012; Nelson and Rook, 2016). Evolving in conditions of insularity between approximately 8.5/8 Ma and 7/6.7 Ma (Casanovas-Vilar et al., 2011a), this hominoid shows a peculiar mixture of primitive and derived characters making the interpretation of its phylogeny as well as diet and locomotion a source of continued debate (Delson, 1986; Moyà-Sola et al., 1999, 2005; Alba et al., 2001; Sussman, 2004, 2005; Begun, 2007). Locomotor behaviours ranging from suspensory arboreality to arboreal bipedality have been suggested on the basis of postcranial features (Köhler and Moyà-Solà, 1997; Moyà-Solà et al., 1999; 2005; Rook et al., 1999; Susman, 2004; Begun, 2007). A folivorous diet requiring high bite forces but relatively little extractive foraging has traditionally been assumed for Oreopithecus (Ungar, 1995; 1996; Kay and Ungar, 1997; Begun, 2007). More recent microwear studies suggest that soft fruit feeding (DeMiguel et al., 2014) and possibly hard object feeding (Williams, 2013) characterized at least a portion of its diet. Isotopic analysis of 13 18 Oreopithecus enamel from sites in Tuscany revealed higher δ C and lower δ O values indicative of a diet that included aquatic plants or underground storage organs (Nelson and Rook, 2016). Unlike other Western Eurasian hominoids, the extinction of Oreopithecus was likely unrelated to environmental change, and instead has been attributed to interactions with species arriving from continental Europe following the tectonic collision of the Tusco-Sardinia province with mainland Italy at ca. 7 Ma (Rook et al., 2006; Agustí, 2007; Abbazzi et al., 2008; Casanovas-Vailar et al., 2011b; Matson et al., 2012). An isotopic study of organic matter in paleosols from the Baccinello Basin in Tuscany, Italy, found very low spatial and temporal

44 variability, indicating that Oreopithecus experienced relatively stable environmental conditions (Matson et al., 2012). However, a recent isotopic study of fossil mammalian enamel indicates that environmental change was a factor in the extinction of Oreopithecus (Nelson and Rook, 2016). Nelson and Rook (2016) found that the decline of this hominoid occurred in correlation with an increase in forest canopy density and a shift from warm humid conditions to an inconsistent climatic regime.

6 Conclusions

Stable isotope analysis of 10 coexisting ungulate species from R. II revealed significant differences in dietary and habitat use. Our results support the niche partitioning hypothesis and suggest that coexistence was maintained through resource specialization within the local environment. Similar isotopic values found in several of the sampled taxa suggest some level of interspecific competition. However, the interpretation of interspecific competition must be viewed with caution given the degree of resolution associated stable isotope analysis (Kartzinel et al., 2015). The results of this study are concordant with the meso- and microwear data for the equid, cervid, bovid, and moschid indicating some degree of dietary niche overlap (Merceron et al., 2007). A year-round abundance of plant resources would have allowed for a moderate degree of niche overlap. The range of isotope values displayed by the R. II fauna indicates a variable forest environment, which included both open and closed canopy habitats. Higher carbon isotope values found in the rhinoceros, cervid, equid, gomphothere, and suids suggest foraging under a relatively open forest canopy, while lower carbon values found in bovid and small ruminants suggest a preference for more humid and densely forested habitats. Relatively low oxygen and carbon isotope values found in all sampled taxa indicate humid and wet climatic conditions.

Within this mixed open and closed canopy forest, we suspect Rudapithecus would have occupied more humid, densely closed canopy habitats where access to fruit was relatively continuous. The palaeoenvironment of Rudapithecus is comparable with that reconstructed for other suspensory and frugivorous hominoids in Western Europe. Adaptations for efficient suspensory foraging and hard fruit feeding would have allowed these hominoids to endure short- term periods of environmental variability; however, the progressive fragmentation and loss of humid forests during the late Vallesian would have ultimately led to their extinction. While this

45 environmental scenario accounts for the decline of hominoids in Central and Western Europe, a contrasting environmental shift (increasing bushy vegetation) may have caused the decline of the more terrestrial and hard object feeding hominoids in the Eastern Mediterranean. Within the Tusco-Sardinian archipelago the extinction of Oreopithecus was likely related to both environmental change and interactions with non-indigenous species. No single ecological factor can account for the decline of Western Eurasian hominoids during the Late Miocene. The continued analysis of regional palaeoecology will allow for a better understanding the evolution and extinction of this highly diverse group.

Acknowledgements

We thank the Geological and Geophysical Institute of Hungary (MAFI) and the New York State Museum. We thank László Kordos for his contributions to this research. We also thank Jochen Halfar, Dave Bovee, and David Boutilier for their contributions to this research. Finally, we thank two anonymous reviewers for their helpful critiques that greatly strengthened the manuscript. This research was funded by the Natural Sciences and Engineering Research Council (NSERC) of Canada, the National Geographic Society, Ontario Graduate Scholarship, Geological Society of America Graduate Research Award, and General Motors Women in Science and Mathematics Award.

References

Agustí, J., Moyà-Solà, S., 1990. Mammal extinctions in the Vallesian (Upper Miocene). In: Kauffman, E.G., Walliser, O.H. (Eds.), Extinction Events in Earth History, Proceedings of the Project 216, Global Biological Events in Earth. Lecture Notes in Earth Sciences 30, pp. 425–432.

Agustí, J., Siria, A. S. d., Garcés, M., 2003. Explaining the end of the hominoid experiment in Europe. J. Hum. Evol. 45, pp. 145-153.

Agustí, J., 2007. The biotic environments of the Late Miocene hominids. In: Henke, W., Tattersall, I. (Eds.), Handbook of Paleoanthropology. Springer, Berlin, pp. 979-1010.

Agustí, J., Cabrera, L., Garcés, M., 2013. The Vallesian mammal turnover: A Late Miocene record of decoupled land-ocean evolution. Geobios 46, pp. 151-157.

Aiglstorfer, M., Bocherens, H., Böhme, M., 2014. Large Mammal Ecology in the late Middle Miocene locality Gratkorn (Austria). Palaeobiodivers. Palaeoenviron. 94, pp. 189–213.

Alba, D.M., Moyà-Solà, S., Kӧhler, M., 2001. Canine reduction in the Miocene hominoid Oreopithecus bambolii: behavioural and evolutionary implications. J. Hum. Evol. 40, pp. 1-16.

Alba, D.M., Almécija, S., Moyà-Solà, S., 2010a. Locomotor inferences in Pierolapithecus and Hispanopithecus: reply to Deane and Begun. J. Hum. Evol. 59, pp. 143-149.

Alba, D.M., Fortuny, J., Moyà-Solà, S., 2010b. Enamel thickness in middle Miocene great apes Anoiapithecus, Pierolapithecus and Dryopithecus. Proc. R. Soc. Biol. 277, pp. 2237-2245.

Alba, D.M., 2012. Fossil apes from the Vallès-Penedès Basin. Evol. Anth. 21, pp. 254–269.

Ambrose, S. H., DeNiro, M. J., 1986. The isotopic ecology of East African mammals. Oecologia 69, pp. 395-406.

Andrews, P., Cameron, D., 2010. Rudabànya: Taphonomic analysis of a fossil hominid site from Hungary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 297, pp. 311-329

Armour-Chelu, M., Andrews, P., Bernor, R. L., 2005. Further observations on the primate community at Rudabánya II (Late Miocene, early Vallesian age), Hungary. J. Hum. Evol. 49, pp. 88-98.

Begun, D. R., 1988. Catarrhine phalanges from the Late Miocene (Vallesian) of Rudabánya, Hungary. J. Hum. Evol. 17, pp. 413-438.

Begun, D. R., 1992. Phyletic diversity and locomotion in primitive European hominids. American Journal of Physical Anthropology 87, pp. 311-340.

Begun, D. R., Güleç, E., 1998. Restoration of the Type and Palate of Ankarapithecus meteai: Taxonomic, Phylogenetic, and Functional Implications. Am. J. Phys. Anth. 105, pp. 279– 314.

Begun, D.R., 2007. Fossil record of Miocene hominoids. In: Henke, W., Tattersall, I. (Eds.), Handbook of Paleoanthropology, Springer, Heidelberg, pp. 921–977.

Begun, D.R., 2009. Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade. Geodiversitas 31, pp. 789–816.

Bernor, R.L., Fahlbusch, V., Andrews, P., de Bruijn, H., Fortelius, M., Rögl, F., Steininger, F.F., Werdelin, L., 1996. The evolution of European and West Asian later Neogene faunas: a biogeographic and paleoenvironmental synthesis. In: Bernor, R., Fahlbusch, V., Mittmann, W. (Eds.), The Evolution of Western Eurasian Neogene Mammal Faunas. Columbia University Press, pp. 449–470.

Bernor, R. L., Armour-Chelu, M., Kaiser, T. M., Scott, R. S., 2003. An evaluation of the late MN 9 (Late Miocene, Vallesian age), hipparion assemblage from Rudabánya (Hungary): Systematic background, functional anatomy and paleoecology. Coloquios De Paleontología, Volumen Extraordinario 1, pp. 35-45.

Bernor, R.L., Kordos, L., Rook, L., Agustí, J., Andrews, P., Armour-Chelu, M., Begun, D.R., de Bonis, L., Cameron, D.W., Damuth, J., Daxner-Höck, G., Fessaha, N., Fortelius, M.,

Franzen, J.L., Gasparik, M., Gentry, A., Heissig, K., Hernyak, G., Kaiser, T.M., Koufos, G.D. Krolopp, E., Jánossy, D., Llenas, M., Meszáros, L., Müller, P., Renne, P.R., Rocek, Z., Sen, S., Scott, R.S., Szindlar, Z., Topál, G.Y., Ungar, P.S., Untescher, T., van Dam, J.A., Werdelin, L. & Ziegler, R., 2004. Recent advances on multidisciplinary research at Rudabanya, Late Miocene (MN9), Hungary: a compendium. Paleontographica Italia 89, pp. 3–36.

Benton, M., 1990. Vertebrate Paleontology. Unwin Hyman, London.

Bocherens, H., Fizet, M., Mariotti, A. 1994a. Diet, physiology and ecology of fossil mammals as inferred by stable carbon and nitrogen isotopes biogeochemistry: implications for Pleistocene bears. Palaeogeogr. Palaeoclimatol. Palaeoecol. 107, pp. 213-225.

Bocherens, H., Fizet, M., Mariotti, A., Bellon, G., Borel, J.-P. 1994b. Les gisements de mammifères du Miocène supérieur de Kemiklitepe, Turquie: 10. Biogéochimie isotopique. Bulletin du Museum d'Histoire Naturelle, Paris, 4e sér. 16, C(1), pp. 211-223.

Bocherens, H., Fogel, M.L., Tuross, N., Zeder, M. 1995. Trophic structure and climatic information from isotopic signatures in a Pleistocene cave fauna of Southern England. J. Arch. Sci. 22, pp. 327-340.

Bocherens, H., Koch, P. L., Mariotti, A., Geraads, D., Jaeger, J., 1996. Isotopic biogeochemistry (13C, 18O) of mammalian enamel from African Pleistocene hominid sites. Palaios 11, pp. 306-318.

Bocherens, H., 2000. Preservation of isotopic signals (13C, 15N) in Pleistocene mammals. In: Katzenberg, A.M., Ambrose, S.H. (Eds), Biogeochemical approaches to Paleodietary Analyses. Plenum Publishers, pp. 65-88.

Bocherens, H., 2003. Isotopic biogeochemistry and the palaeoecology of the mammoth steppe fauna. Deinsea 9, pp. 57–76.

Böhme, M., Ilg, A., Winklhofer, M., 2008. Late Miocene “washhouse” climate in Europe. Earth Planet. Sci. Lett. 275, pp. 393-401.

Böhme, M., Winklhofer, M., Ilg, A., 2011. Miocene precipitation in Europe: Temporal trends and spatial gradients. Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, pp. 212-218.

Bonis, L.de, Bouvrain, G., Geraads, D., Koufos, G.D., 1992. Diversity and palaeoecology of Greek Late Miocene mammalian faunas. Palaeogeogr. Palaeoclimatol. Palaeoecol. 91, pp. 99–121.

Bonis, L., Koufos, G., 1993. The face and mandible of Ouranopithecus macedoniensis: description of new specimens and comparisons. J. Hum. Evol. 24, pp. 469-491.

Bruch, A. A., Utescher, T., Mosbrugger, V., Gabrielyan, I., Ivanov, D. A., 2006. Late Miocene climate in the circum-alpine realm-a quantitative analysis of terrestrial palaeofloras. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, pp. 270-280

Bruch, A. A., Uhl, D., Mosbrugger, V., 2007. Miocene climate in Europe - patterns and evolution. A first synthesis of NECLIME. Palaeogeogr. Palaeoclimatol. Palaeoecol. 253, pp. 1-7.

Bryant, J.D., Froelich, P.N., 1995. A model of oxygen isotope fractionation in body water of large mammals. Geochim. Cosmochim. Acta. 39, pp. 4523-4537.

Calandra, I., Göhlich, U., Merceron, G., 2008. How could sympatric megaherbivores coexist? Example of niche partitioning within a proboscidean community from the Miocene of Europe. Naturwissenschaften 95, pp. 831 – 838.

Carnieri, E., Mallegni, F., 2003. A new specimen and dental microwear in Oreopithecus bambolii. Homo 54, pp. 29-35.

Casanovas-Vilar, I., Alba, D.M., Garcés, M., Robles, J.M., Moyá-Solá, S., 2011a. Updated chronology for the Miocene hominoid radiation in western Eurasia. PNAS 108, pp. 5554- 5559.

Casanovas-Vilar, I., van den Hoek Ostende, L., Furió, M., Madern, A., 2014. The range and extent of the Vallesian Crisis (Late Miocene): new prospects based on the micromammal record from the Vallès-Penedès Basin (Catalonia, Spain). J. Iberian Geol. 40, pp. 29 – 48.

Cerling, T. E., Harris, J. M., MacFadden, B. J., Leakey, M. G., Quade, J., Eisenmann, V., 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature 389, pp. 153-158.

Cerling, T. E., Harris, J. M., Leakey, M. G., 1999. Browsing and grazing in elephants: The isotope record of modern and fossil proboscideans. Oecologia, 120, pp. 364-374.

Cerling, T. E., Harris, J. M., 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, pp. 347-363.

Cerling, T. E., Hart, J. A., Hart, T. B., 2004. Stable isotope ecology in the Ituri forest. Oecologia 138, pp. 5-12.

Cody, M.L., 1974. Competition and the structure of bird communities. Princeton University Press. Princeton, NJ.

Collins, R.P., Jones, M.B., 1986. The influence of climatic factors on the distribution of C4 species in Europe. Plant Ecol. 64, pp. 121-129.

Crawford, R.M., 1984. Activity, group structure and lambing of blue duikers Cephalophus monticola in the Tsitsikamma National Parks, South Africa. South African Journal of Wildlife Research 14, pp. 65-68.

Daxner-Höck, G., 2004. Biber und ein zwerghamster aus Mataschen (unter-pannonium, steirisches becken). Joannea Geologie Und Paläontologie 5, pp. 19-33.

Daxner-Höck, G., Harzhauser, M., Göhlich, U., 2016. Fossil record and dynamics of the Late Miocene small mammal faunas of the Vienna Basin and adjacent basins, Austria. Comptes Rendus Palevol, 15, pp. 855-862.

Deane, A.S., Nargolwalla, M.C., Kordos, L., Begun, D.R., 2013. New evidence for diet and niche partitioning in Rudapithecus and Anapithecus from Rudabánya, Hungary. J. Hum. Evol. 65, pp. 704-714.

Delson, E., 1986. An anthropoid enigma: historical introduction to the study of Oreopithecus bambolii. J. Hum. Evol. 15, pp. 523-531.

DeLucia, E.H., Schlesinger, W.H., 1995. Photosynthetic rates and nutrient-use efficiency among evergreen and deciduous shrubs in Okefenokee Swamp. Inter. J. Plant Sci. 156, pp. 19-28.

DeMiguel, D., Alba, D., Moyà-Solà, S., 2014. Dietary specializations during the evolution of Western Eurasian hominoids and the extinction of great apes. PLoS ONE 9(5): e97442.

DeSantis, L. R. G., Wallace, S. C., 2008. Neogene forests from the Appalachians of Tennessee, USA: Geochemical evidence from fossil mammal teeth. Palaeogeogr. Palaeoclimatol. Palaeoecol. 266, pp. 59-68.

Diefendorf, A.F., Mueller, K.E., Wing, S.L., Koch, P.L., Freeman, K.H., 2010. Global patterns in leaf 13C discrimination and implications for studies of past and future climate. PNAS. 107, pp. 5738–5743.

Djagoun, C., Kassa, B., Mensah, G., Sinsin, B. 2013. Seasonal habitat and diet partitioning between two sympatric bovid species in Pendjari Biosphere Reserve (northern Benin): waterbuck and western kob. African Zoology 48, pp. 279 – 289.

Domingo, L., Cuevas-González, J., Grimes, S.T., Hernández Fernández, M., López-Martínez, N., 2009 Multiproxy reconstruction of the palaeoclimate and palaeoenvironment of the Middle Miocene Somosaguas site (Madrid, Spain) using herbivore dental enamel. Palaeogeogr. Palaeoclimatol. Palaeoecol. 272, pp. 53–68.

Domingo, L., Koch, P.L., Grimes, S.T., Morales, J., López-Martínez, N., 2012. Isotopic paleoecology of mammals and the Middle Miocene Cooling event in the Madrid Basin

(Spain). Palaeogeogr. Palaeoclimatol. Palaeoecol. 339-341, pp. 98-113.

Drucker, D., Bocherens, H., Bridault, A., Billiou, D., 2003. Carbon and nitrogen isotopic composition of red deer (Cervus elaphus) collagen as a tool for tracking palaeoenvironmental change during the Late Glacial and Early Holocene in the northern Jura (France). Palaeogeogr. Palaeoclimatol. Palaeoecol. 195, pp. 375–388.

Eastham, L., Feranec, R.S., Begun, D.R., Kordos, L., 2011. Resource partitioning in Late Miocene Central European Mammals: Isotopic evidence from the Rudabánya fauna. J. Vert. Paleo. 31 (Suppl. 2), 103.

Ecker, M., Bocherens, H., Julien, M.-A., Rivals, F., Raynal, J.-P., Moncel, M.-H., 2013. Middle Pleistocene ecology and Neanderthal subsistence: Insights from stable isotope analyses in Payre (Ardèche, France). J. Hum. Evol. 65, pp. 363-373.

Ehleringer, J. R., Field, C. B., Lin, Z., Kuo, C., 1986. Leaf carbon isotope and mineral composition in subtropical plants along an irradiance cline. Oecologia 70, pp. 520-526.

Ehleringer, J. R., Lin, Z. F., Field, C. B., Sun, G. C., Kuo, C. Y., 1987. Leaf carbon isotope ratios of plants from a subtropical monsoon forest. Oecologia, 72, pp. 109-114.

Ehleringer, J. R., Sage, R. F., Flanagan, L. B., Pearcy, R. W., 1991. Climate change and the

evolution of C4 photosynthesis. Trends Ecol. Evol. 6, pp. 95-99.

Ehleringer, J. R., Monson, R. K., 1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Ann. Rev. Ecol. System. 24, pp. 411-439.

Ehleringer, J. R., Cerling, T. E., Helliker, B. R., 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, pp. 285-299.

Eisenmann, V., 1998. Folivores et tondeurs d’herbe: forme de la symphyse mandibulaire des Equide´s et des Tapiride´s (Perissodactyla, Mammalia). Geobios 31, pp. 113 - 123.

Epstein, S., Thompson, P., Yapp, C. J., 1977. Oxygen and hydrogen isotopic ratios in plant cellulose. Science 198, pp. 1209-1215.

Estes, R.D., 1991. Behavior Guide to African Mammals. The University of California Press, Los Angeles.

Farquhar, G. D., O'Leary, M. H., Berry, J. A., 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Austral. J. Plant Physiol. 9, pp. 121-137.

Feranec, R. S., MacFadden, B. J., 2000. Evolution of the grazing niche in Pleistocene mammals from Florida: Evidence from stable isotopes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 162, pp. 155-169.

Feranec, R. S., MacFadden, B. J., 2006. Isotopic discrimination of resource partitioning among

ungulates in C3-dominated communities from the Miocene of Florida and California. Paleobiology 32, pp. 191-205.

Feranec, R. S., 2007. Stable carbon isotope values reveal evidence of resource partitioning

among ungulates from modern C3-dominated ecosystems in North America. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252, pp. 575-585.

Feranec, R. S., Hadly, E. A., Paytan, A., 2009. Stable isotopes reveal seasonal competition for resources between Late Pleistocene bison (Bison) and horse (Equus) from Rancho La Brea, southern California. Palaeogeogr. Palaeoclimatol. Palaeoecol. 271, pp. 153-160.

Fortelius, M., Hokkanen, A., 2001. The trophic context of hominoid occurrence in the later Miocene of western Eurasia—a primate-free view. In: de Bonis, L., Koufos, G., Andrews, A., (Eds.), Phylogeny of the Neogene Hominoid Primates of Eurasia, pp. 19–47. Cambridge University Press, Cambridge.

Fortelius, M., Eronen, J., Jernvall, J., Liu, L., Pushkina, D., Rinne, J., 2002. Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evol. Ecol. Res. 4, pp. 1005-1016.

Franzen, J. L., Storch, G., 1999. Late Miocene mammals from central Europe. Hominoid Evolution and Climatic Change in Europe 1, pp. 165-190.

Franzen, J., L., Pickford, M., Costeur, L., 2013. Palaeobiodiversity, palaeoecology, palaeobiogeography and biochronology of Dorn-Dü rkheim 1—a summary. Palaeobiodivers. Palaeoenviron.93, pp. 277 – 284.

Friedli, H., Lötscher, H., Oeschger, H., Siegenthaler, U., Stauffer, B., 1986. Ice core record of 13 12 the C/ C ratio of atmospheric CO2 in the past two centuries. Nature 324, pp. 237-238.

Garten Jr., C. T., Taylor Jr., G. E., 1992. Foliar d13C within a temperate deciduous forest: Spatial, temporal, and species sources of variation. Oecologia 90, pp. 1-7.

Garten Jr., C.T., Cooper, L.W., Post III, W.M., Hanson, P.J., 2000. Climate controls on forest soil C isotope ratios in the southern Appalachian Mountains. Ecology 81, pp. 1108 -1119.

Gartlan J.S., Struhsaker T.T., 1972. Polyspecific associations and niche separation of rain forest anthropoids in Cameroon, W. Afr. J. Zoo. 168, pp. 221–266.

Gentry, A.W., 2005. Ruminants of Rudabánya. Palaeontographia Italica 90, pp. 283-302.

Green, M.B., 1986. The distribution, status and conservation of the Himalayan musk deer Moschus chrysogaster. Biol. Conserv. 35, pp. 347 - 375.

Gordon, I.J., Illius, A.W., 1989. Resource partitioning by ungulates on the Isle of Rhum. Oecologia 79, pp. 383-389.

Gross, M., Piller, W. E., Scholger, R., Gitter, F., 2011a. Biotic and abiotic response to palaeoenvironmental changes at Lake Pannons' western margin (central Europe, Late Miocene). Palaeogeogr. Palaeoclimatol. Palaeoecol. 312, pp. 181-193.

Gross, M., Böhme, M., Prieto, J., 2011b. Gratkorn: A benchmark locality for the continental Sarmatian of the Central Paratethys. Inter. J. Earth Sci. (Geol Rundsch) 100, pp.1895–1913.

Guleç, E.S., Sevim, A., Pehlevan, C., Kaya, F., 2007. A new great ape from the Late Miocene of Turkey. Anthropol. Sci. 115, pp. 153-158.

Hably, L., Erdei, B., 2013. A refugium of mastixia in the Late Miocene of eastern central Europe. Rev. Palaeobot. Palynol. 197, pp. 218-225.

Harris, J. M., Cerling, T. E., 2002. Dietary adaptations of extant and Neogene African suids. J. Zoo. 256, pp. 45-54.

Harrison, T.S., Harrison, T., 1989. Palynology of the late Miocene Oreopithecus bearing lignite from Baccinello, Italy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 76, pp. 45-65.

Harrison, T., 2002. Late Oligocene to middle Miocene catarrhines from Afro‐ Arabia. In: Hartwig, W. (Ed.), The primate fossil record, pp. 311–338. Cambridge University Press, Cambridge

Harzhauser, M., Mandic, O., 2004. The muddy bottom of Lake Pannon - A challenge for dreissenid settlement (Late Miocene; bivalvia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 204, pp. 331-352.

Harzhauser, M., Latal, C., Piller, W. E., 2007. The stable isotope archive of Lake Pannon as a mirror of Late Miocene climate change. Palaeogeogr. Palaeoclimatol. Palaeoecol. 249, pp. 335-350.

Harzhauser, M., Mandic, O., 2008. Neogene lake systems of Central and South-Eastern Europe: faunal diversity, gradients and interrelations. Palaeogeogr. Palaeoclimatol. Palaeoecol. 260, pp. 417–434.

Harzhauser, M., Kern, A., Soliman, A., Minati, K., Piller, W. E., Danielopol, D. L., 2008. Centennial- to decadal scale environmental shifts in and around Lake Pannon (Vienna Basin) related to a major Late Miocene lake level rise. Palaeogeogr. Palaeoclimatol. Palaeoecol. 270, pp. 102-115.

Hayek, C.L., Bernor, R.L., Solounias, N., Steigerwald, P., 1992. Preliminary studies of Hipparionine horses diet as measured by tooth microwear. Annales Zoologici Fennici 28, pp. 187 - 200.

13 12 Heaton, T. H. E., 1999. Spatial, species, and temporal variations in the C/ C ratios of C3 plants: Implications for palaeodiet studies. J. Arch. Sci. 26, pp. 637-649.

Hernández Fernández, M., Cárdaba, J. A., Cuevas-González, J., Fesharaki, O., Salesa, M. J., Corrales, B., 2006. The deposits of Middle Miocene vertebrates of Somosaguas (pozuelo de

Alarcon, Madrid): Paleoenvironment and paleoclimate implications. [Los yacimientos de vertebrados del Mioceno medio de Somosaguas (Pozuelo de Alarcón, Madrid): Implicaciones paleoambientales y paleoclimáticas] Estudios Geologicos 62, pp. 263-294.

Hillson, S., 2005. Teeth, Cambridge Manuals in Archaeology (2nd Ed.). Cambridge University Press, Cambridge.

Kartzinela, T., Chen, P., Coverdale, T., Erickson, D., Kress, J., Kuzmina, M., Rubenstein, D., Wang, W., Pringle, R. DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. PNAS. 112, pp. 8019 – 8024.

Kázmér, M., 1990. Birth, life and death of the Pannonian Lake. Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, pp. 171-188.

Kern, A. K., Harzhauser, M., Soliman, A., Piller, W. E., Gross, M., 2012. Precipitation driven decadal scale decline and recovery of wetlands of Lake Pannon during the Tortonian. Palaeogeogr. Palaeoclimatol. Palaeoecol. 317-318, pp. 1-12.

Kivell, T. L., Begun, D. R., 2009. New primate carpal bones from Rudabánya (Late Miocene, Hungary): Taxonomic and functional implications. J. Hum. Evol. 57, pp. 697-709.

Koch, P. L., Tuross, N., Fogel, M. L., 1997. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J. Arch. Sci. 24, pp. 417-429.

Koch, P.L., 1998. Isotopic reconstruction of past continental environments. Ann. Rev. Earth Planet. Sci. 26, pp. 573–613.

Kӧhler, M., Moyà-Sola, S., 1997. Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. PNAS. 94, pp. 11747-11750.

Kohn, M. J., 1996. Predicting animal δ18O: Accounting for diet and physiological adaptation. Geochim. Cosmochim. Acta. 60, pp. 4811-4829.

Kohn, M. J., Schoeninger, M. J., Valley, J. W., 1996. Herbivore tooth oxygen isotope compositions: Effects of diet and physiology. Geochim. Cosmochim. Acta. 60, pp. 3889- 3896.

Kohn, M.J., Cerling, T.E., 2002. Stable isotope compositions of biological apatite. Rev. Mineral. Geochem. 48, pp. 455–488.

Kohn, M. J., Welker, J. M., 2005. On the temperature correlation of δ18O in modern precipitation. Earth Planet. Sci. Lett. 231, pp. 87-96.

Kohn, M.J., Law, J.M., 2006. Stable isotope chemistry of fossil bone as a new paleoclimate indicator. Geochim. Cosmochim. Acta. 70, pp. 931–946.

Kohn, M.J., 2010. Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. PNAS. 46, pp. 19691-19695.

Kordos, L., 1991. Le Rudapithecus hungaricus de Rudabànya (Hongrie). L'Anthropologie 95, pp. 343–362.

Kordos, L., Begun, D. R., 2002. Rudabánya: A Late Miocene subtropical swamp deposit with evidence of the origin of the African apes and humans. Evol. Anth. 11, pp. 45-57.

Koufos, G.D., 2006. Palaeoecology and chronology of the Vallesian (Late Miocene) in the Eastern Mediterranean region. Palaeogeogr. Palaeoclimatol. Palaeoecol. 234, pp.127–145.

Koufos, G.D., Konidaris, G.E., 2011. Late Miocene carnivore of the Greco-Iranian Province: Composition, guild structure and paleoecology. Palaeogeogr. Palaeoclimatol. Palaeoecol. 305, pp. 215–226.

Krigbaum, J., Berger, M.H., Daegling, D.J., McGraw, W.S., 2013. Stable isotope canopy effects for sympatric monkeys at Taï Forest, Côte d’Ivoire. Proc. R. Soc. Biol. 9: 20130466

Landman, M., Schoeman, D., Kerley, G., 2013. Shift in Black Rhinoceros diet in the presence of Elephant: Evidence for competition? PLoSONE 8(7): e69771. doi:10.1371/journal.pone.0069771

Latorre, C., Quade, J., McIntosh, W. C., 1997. The expansion of C4 grasses and global change in the Late Miocene: Stable isotope evidence from the Americas. Earth Planet. Sci. Lett. 146, pp. 83-96.

Lee-Thorp J.A., van der Merwe N.J., 1987. Carbon isotope analysis of fossil bone apatite. S. Afr. J. Sci. 83, pp. 712–715.

Lee-Thorp, J. A., Sealy, J. C., van der Merwe, N. J., 1989. Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. J. Arch. Sci. 16, pp. 585-599.

Lee-Thorp, J.A., Sponheimer, M., 2003. Three case studies used to reassess the reliability of fossil bone and enamel isotope signals for paleodietary studies. J. Anth. Arch. 22, pp. 208– 216.

Levine, J.M., HilleRisLambers, J., 2009. The importance of niches for maintenance of species diversity. Nature 461, pp. 254 – 257.

Levin, N. E., Cerling, T. E., Passey, B. H., Harris, J. M., Ehleringer, J. R., 2006. A stable isotope aridity index for terrestrial environments. PNAS. 103, pp. 11201-11205.

Lumpkin, S., Kranz, K.R., 1984. Cephalophus sylvicultor. Mammalian Species 225, pp. 1 - 7.

Macarthur, R., Levins, R., 1967. The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101, pp. 377-385.

MacFadden, B. J., Cerling, T. E., 1996. Mammalian herbivore communities, ancient feeding ecology, and carbon isotopes: A 10 million-year sequence from the Neogene of Florida. J. Vert. Paleo. 16, pp. 103-115.

MacFadden, B. J., Solounias, N., Cerling, T. E., 1999. Ancient diets, ecology, and extinction of 5-million-year-old horses from Florida. Science 283, pp. 824-827.

MacFadden, B. J., Higgins, P., 2004. Ancient ecology of 15-million-year-old browsing mammals

within C3 plant communities from Panama. Oecologia 140, pp. 169-182.

MacFadden, B. J., DeSantis, L. R. G., Hochstein, J. L., Kamenov, G. D., 2010. Physical properties, geochemistry, and diagenesis of xenarthran teeth: Prospects for interpreting the paleoecology of extinct species. Palaeogeogr. Palaeoclimatol. Palaeoecol. 291, pp. 180-189.

Magyar, I., Geary, D. H., Müller, P., 1999. Paleogeographic evolution of the Late Miocene Lake Pannon in central Europe. Palaeogeogr. Palaeoclimatol. Palaeoecol. 147, pp. 151-167.

Marino, B.D., McElroy, M.B., 1991. Isotopic composition of atmospheric CO2 inferred from

carbon in C4 plant cellulose. Nature 349, 127–131.

Marino, B.D., McElroy, M.B., Salawitch, R.J., Spaulding, W.G., 1992. Glacial-to-interglacial

variations in the carbon isotopic composition of atmospheric CO2. Nature 357, 461–466.

Marion H. O'Leary., 1988. Carbon isotopes in photosynthesis. Bioscience 38, pp. 328-336.

Merceron, G., Zazzo, A., Spassov, N., Geraads, D., Kovachev, D., 2006. Bovid paleoecology and paleoenvironments from the Late Miocene of Bulgaria: Evidence from dental microwear and stable isotopes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 241, pp. 637-654.

Merceron, G., Schulz, E., Kordos, L., Kaiser, T. M., 2007. Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: Evidence from dental meso- and micro-wear analyses of large vegetarian mammals. J. Hum. Evol. 53, pp. 331-349. Merceron, G., 2009. The early Valleisan vertebrates of Atzelsdorf (Late Miocene, Austria). Annals of the Natural History Museum Vienna 111A, pp. 647 – 660.

Merceron, G., Kaiser, T.M., Kostopoulos, D.S., Schulz, E., 2010. Ruminant diets and the Miocene extinction of European great apes. Proc. R. Soc. Biol. 277, pp. 3105-3112.

Mosbrugger, V., Utescher, T., 1997. The coexistence approach — a method for quantitative reconstructions of tertiary terrestrial palaeoclimate data using plant fossils. Palaeogeogr. Palaeoclimatol. Palaeoecol. 134, pp. 61-86.

Mosbrugger, V., Utescher, T., Dilcher, D. L., 2005. Cenozoic continental climatic evolution of central Europe. PNAS. 102, pp. 14964-14969.

Moyà-Solà, S., Köhler, M., 1996. A Dryopithecus skeleton and the origins of great ape locomotion. Nature 379, pp. 156-159.

Moyà-Solà, S., Köhler, M., Rook, L., 1999. Evidence of hominid-like precision grip capabilities in the hand of the Miocene ape Oreopithecus PNAS. 96 pp. 313-317.

Moyà-Solà, S., Köhler, M., Rook, L., 2005. The Oreopithecus thumb: a strange case in hominoid evolution. J. Hum. Evol. 49, pp. 395-404.

Nelson, S.V., 2003. The Extinction of Sivapithecus. Brill Academic Publishers, Inc., Boston, USA.

Nelson, S. V., 2007. Isotopic reconstructions of habitat change surrounding the extinction of Sivapithecus, a Miocene hominoid, in the Siwalik group of Pakistan. Palaeogeogr. Palaeoclimatol. Palaeoecol. 243, pp. 204-222.

Nelson, S.V., Rook, L., 2016. Isotopic reconstruction of habitat change surrounding the extinction of Oreopithecus, the last European ape. Am. J. Phys. Anth. 160, 254–271. Nowak, R.M. 1991. Walker's Mammals of the World (Fifth Edition). Johns Hopkins University Press, Baltimore.

Nowak R.M., 1999. Walker’s Mammals of the world, (Sixth Edition). Johns Hopkins University Press, Baltimore.

Passey, B. H., Cerling, T. E., 2002. Tooth enamel mineralization in ungulates: Implications for recovering a primary isotopic time-series. Geochim. Cosmochim. Acta. 66, pp. 3225-3234

Passey, B. H., Robinson, T. F., Ayliffe, L. K., Cerling, T. E., Sphonheimer, M., Dearing, M. D.,

2005. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J. Arch. Sci. 32, pp. 1459-1470

Pianka, E. R., 1981. Competition and niche theory. In: May, R.M. (Ed.), Theoretical Ecology: Principles and Applications. Blackwell Scientific Publications, Oxford, United Kingdom, pp. 167–196.

Popov, S.V., Rögl, F., Rozanov, A.Y., Steininger, F.F., Shcherba, I.G., Kováè, M., 2004. Lithological–paleogeographic maps of Paratethys. 10 maps Late Eocene to Pliocene. Courier Forschungsinstitut Senckenberg 250, pp. 1–46.

Pound, M. J., Haywood, A. M., Salzmann, U., Riding, J. B., Lunt, D. J., Hunter, S. J., 2011. A Tortonian (Late Miocene, 11.61-7.25Ma) global vegetation reconstruction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 300, pp. 29-45.

Prins, H.T., de Boer, W., Oeveren, H., Correia, A., Mafuca, J., Olff, H. 2006. Co-existence and niche segregation of three small bovid species in southern Mozambique. Afr. J. Ecol. 44, pp. 186 –198.

Pyke G.H., Pulliam H.R., Charnov E.L., 1977. Optimal foraging: a selective review of theory and tests. Quarterly Rev. Bio. 52, pp. 137–157.

Quade, J., Cerling, T. E., Andrews, P., Alpagut, B., 1995. Paleodietary reconstruction of Miocene faunas from Paşalar, Turkey using stable carbon and oxygen isotopes of fossil tooth enamel. J. Hum. Evol. 28, pp. 373-384.

Rey, K., Amiot, R., Lécuyer, C., Koufos, G.D., Martineau, F., Fourel., F., Kostopoulos, D.S., Merceron, G., 2013. Late Miocene climatic and environmental varaitions in northern

Greece inferred from stable isotope compositions (δ18O, δ13C) of equid teeth apatite. Palaeogeogr. Palaeoclimatol. Palaeoecol. 388, pp. 48–57.

Rook, L., Bondioli, L., Kӧhler, M., Moyà-Sola, S., Machiarelli, R., 1999. Oreopithecus was a bipedal ape after all: evidence from the iliac cancellous architecture. PNAS. 96, pp. 8795- 8799.

Rook, L., Gallai, G., Torre, D., 2006. Lands and endemic mammals in the Late Miocene of Italy: constraints for paleogeographic outlines of Tyrrhenian area. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, pp. 263-269.

Rögl, V.F., 1998. Palaeogeographic considerations for Mediterranean and Paratethys seaways (Oligocene to Miocene). Annals of the Natural History Museum Vienna 99A, pp. 279–310.

Rössner, G. E., 2007. Family tragulidae. The Evolution of Artiodactyls, pp. 213-220.

Rozanski, K., Araguas-Araguas, L., Gonfiantini, R., 1993. Isotopic patterns in modern global precipitation. Geophysical Monograph 78, pp. 1–36.

Schoener, T. W., 1974. Resource partitioning in ecological communities. Science 185, pp. 27-39.

Scott, R. S., Amour-Chelu, M., Bernor, R. L., 2005. Hipparionine horses of the greater Pannonian Basin: Morphometric evidence from the postcranial skeleton. Paleontographica Italia 90, pp. 193-212.

Singh, M., Roy, K., Singh, M., 2011. Resource partitioning in sympatric langurs and macaques in tropical rainforests of the Central Western Ghats, South India. Am. J. Primatol. 73, pp. 355 – 346.

Skinner, M.F., Dupras, T.L., Moyà-Solà, S., 1995. Periodicity of linear enamel hipoplasia among Miocene Dryopithecus from Spain. J. Paleopath. 7, pp. 195–222.

Smith, T.M., Begun, D.R., Eastham, L., Hublin, J.J., Kordos, L., Olejniczak, A.J., Pouech, J., Reid, D.J., Tafforeau, P., Zermeno., 2010. Enamel thickness and tooth development in a subadult Dryopithecus brancoi (Rudapithecus hungaricus) individual. Am. J. Phys. Anth. 50, pp. 220.

Solounias, N., Dawson-Saunders, B., 1988. Dietary adaptations and palaeoecology of the Late Miocene ruminants from Pikermi and Samos in Greece. Palaeogeogr. Palaeoclimatol. Palaeoecol. 65, pp. 149 - 172.

Solounias, N., Semprebon, G., 2002. Advances in the reconstruction of ungulates ecomorphology with application to early fossil equids. American Museum Novitates 3366, pp. 1 – 49.

Spassov, N., Geraads, D., 2004. Tragoportax pilgrim, 1937 and Miotragocerus stromer, 1928 (Mammalia, Bovidae) from the Turolian of Hadjidimovo, Bulgaria, and a revision of the Late Miocene Mediterranean boselaphini. Geodiversitas 26, pp. 339-370.

Sponheimer, M., Lee-Thorp, J. A., 1999. Oxygen isotopes in enamel carbonate and their ecological significance. J. Arch. Sci. 26, pp. 723-728.

Sponheimer, M., Lee-Thorp, J.A., 2001. The oxygen isotope composition of mammalian enamel carbonate from Morea Estate, South Africa. Oecologia 126, pp. 153–157.

Sponheimer, M., Lee-Thorp, J., de Ruiter, D., Codron, D., Codron, J., Baugh, A. T., 2005. Hominins, sedges, and termites: New carbon isotope data from the Sterkfontein Valley and Kruger National Park. J. Hum. Evol. 48, pp. 301-312.

Sternberg, L.S.L., Mulkey, S.S., Wright, S.J., 1989. Oxygen isotope ratio stratification in a tropical moist forest. Oecologia 81, pp. 51–56.

Storms, D., Aubry, P., Hamann, J-L., Saïd, S., Fritz, H., Saint-Andrieux, C., Klein, F., 2008. Seasonal variation in diet composition and similarity of sympatric red deer Cervus elaphus and roe deer Capreolus capreolus. Wildlife Biology 14, pp. 237 – 250.

Sussman, R.L., 2004. Oreopithecus bambolii: an unlikely case of hominid like grip capability in a Miocene ape. J. Hum. Evol. 46, pp. 105-117.

Sussman R.L., 2005. Oreopithecus: still ape-like after all these years. J. Hum. Evol. 49, pp. 405- 411.

Tabara, D., Chirila, G., 2011. Palaeoclimatic and palaeoenvironmental interpretation on the Sarmatian deposits of Şupanu Formation from Comăneşti Basin (Bacău County). Acta Palaeontologica Romaniae 7, pp. 315-333.

Tipple, B.J., Meyers, S.R., Pagani, M., 2010. Carbon isotope ratio of Cenozoic CO2: a comparative evaluation of available geochemical proxies. Paleoceanography 25, PA3202.

Tu, T.T.N., Kü rschner, W.M., Schouten, S., Van Bergen, P.F., 2004. Leaf carbon isotope composition of fossil and extant oaks grown under differing atmospheric CO2 levels. Palaeogeogr. Palaeoclimatol. Palaeoecol. 212, pp. 199–213.

Tütken, T., Vennemann, T. W., Janz, H., Heizmann, E. P. J., 2006. Palaeoenvironment and palaeoclimate of the Middle Miocene lake in the Steinheim Basin, SW Germany: A reconstruction from C, O, and Sr isotopes of fossil remains. Palaeogeogr. Palaeoclimatol. Palaeoecol. 241, pp. 457-491.

Tütken, T., Vennemann, T., 2009. Stable isotope ecology of Miocene large mammals from Sandelzhausen, southern Germany. Palaontologische Zeitschrift 83, pp. 207-226.

Tütken, T., Kaiser, T.M., Vennemann, T., Merceron, G., 2013. Opportunistic feeding strategy for the earliest hypsodont equids: Evidence from stable isotopes and dental wear proxies. PLoS ONE 8(9), E74463.

Ungar, P.S., Kay, R.F., 1995. The dietary adaptations of European Miocene catarrhines. PNAS. 92, pp. 5479–81.

Ungar, P.S., 1996. Dental microwear of European Miocene catarrhines: evidence for diets and tooth use. J. Hum. Evol. 31, pp. 335–66.

Ungar, P.S., Scott, J.R., Curran, S.C., Dunsworth, H.M., Harcourt-Smith W.E.H., Lehmann, T., Manthi, F.K., McNulty, K.P., 2012. Early Neogene environments in East Africa: Evidence from dental microwear of tragulids. Palaeogeogr. Palaeoclimatol. Palaeoecol. 342–343, pp. 84–96.

Urton, E. J. M., Hobson, K. A., 2005. Intrapopulation variation in gray wolf isotope (δ15N and δ13C) profiles: Implications for the ecology of individuals. Oecologia 145, pp. 317-326.

Utescher, T., Bruch, A. A., Micheels, A., Mosbrugger, V., Popova, S., 2011. Cenozoic climate gradients in Eurasia - a palaeo-perspective on future climate change? Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, pp. 351-358.

Utescher, T., Erdei, B., Hably, L., Mosbrugger, V., 2017. Late Miocene vegetation of the Pannonian Basin. Palaeogeogr. Palaeoclimatol. Palaeoecol. 467, pp. 131-148. van Dam, J. A., 2006. Geographic and temporal patterns in the late Neogene (12-3 Ma) aridification of Europe: The use of small mammals as paleoprecipitation proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, pp. 190-218. van Dam, J.A., Reichart, G.J., 2009. Oxygen and carbon isotope signatures in late Neogene horse teeth from Spain and application as temperature and seasonality proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 274, pp. 64–81. van der Merwe, N. J., Medina, E., 1989. Photosynthesis and 13C:12C ratios in Amazonian rain forests. Geochim. Cosmochim. Acta. 53, pp. 1091-1094. van der Merwe, N. J., Medina, E., 1991. The canopy effect, carbon isotope ratios and foodwebs in Amazonia. J. Arch. Sci. 18, pp. 249-259.

Vevuka, A., Lordkipanidze, D., 2008. The history of vertebrate fauna in Eastern Georgia. Bulletin of the Georgian National Academy of Science 2, pp. 149-155.

Vogel, J.C., 1980. Fractionation of the Carbon Isotope during photosynthesis. Springer-Verlag, Berlin.

Williams, F., 2013. Enamel microwear texture properties of IGF 11778 (Oreopithecus bambolii) from the Late Miocene of Baccinello, Italy. J. Anthropol. Sci. 91, pp. 201-217.

Yakir, D., 1992. Variation in the natural abundances of oxygen-18 and deuterium in plant carbohydrates. Plant, Cell and Environment 15, pp. 1005–102.

Yalden, D.W., Largen, M.J., Kock D., 1984. Catalogue of the Mammals of Ethiopia. Monitore Zoologico Italiano 19, pp. 73 - 74.

Zanazzi, A., Kohn, M. J., 2008. Ecology and physiology of white river mammals based on stable isotope ratios of teeth. Palaeogeogr. Palaeoclimatol. Palaeoecol. 257, pp. 22-37.

Zin-Maung-Maung-Thein, Takai, M., Uno, H., Wynn, J. G., Egi, N., Tsubamoto, T., 2011. Stable isotope analysis of the tooth enamel of Chaingzauk mammalian fauna (late Neogene, Myanmar) and its implication to paleoenvironment and paleogeography. Palaeogeogr. Palaeoclimatol. Palaeoecol. 300, pp. 11-22.

Chapter 3

Trace Element Analysis Provides Insight into the Diets of early Late Miocene Ungulates from the Rudabánya II Locality (Hungary)

Accepted for publication in: Geologica Acta (May 19th, 2017).

The early Late Miocene vertebrate locality of Rudabánya II (R. II) in northeastern Hungary preserves an abundance of forest-adapted ungulate species. To better understand the ecological relationships within this ancient ecosystem, we used analysis of enamel strontium/calcium (Sr/Ca) trace element ratios to infer dietary preferences. The goals of the analysis were to (1) determine whether these ungulate species specialized in specific plants or plant parts; (2) discern whether the Sr/Ca ratios support what was previously suggested about the ecology of these species; and (3) evaluate the factors that may have acted to promote coexistence within this diverse community of predominantly browsing herbivores. Results show significant differences in the diets of the sampled species. The highest Sr/Ca ratios were displayed by the suids Parachleuastochoerus kretzoii and Propotamochoerus palaeochoerus implying a preference for Sr-rich underground plants parts. Elevated Sr/Ca ratios yielded by the cervid Lucentia aff. pierensis and equid Hippotherium intrans are indicative of intermediate feeding. The bovid Miotragocerus sp. showed higher Sr/Ca ratios than the gomphothere Tetralophodon longirostris, which is incongruent with morphological and stable isotope data, which suggested browsing by both taxa. This finding is likely the result of a difference in digestive physiology (ruminant vs.

69 monogastric) rather than a difference in dietary behaviour. The lowest Sr/Ca ratios were displayed by the traguild Dorcatherium naui and moschid Micromeryx flourensianus suggesting a preference for Sr-poor fruits. Resource specialization and partitioning within the local environment likely acted to decrease interspecific competition and promote coexistence within the diverse ungulate community at R. II.

1 Introduction

The relative concentration of strontium to calcium (Sr/Ca) in mammalian bioapatite has proven to be an effective indicator of trophic level and dietary behavior in both modern and ancient ecosystems (Elias et al., 1982; Sillen, 1986; Sealy and Sillen, 1988; Sillen et al., 1992; Gilbert et al., 1994; Burton et al., 1999; Blum et al., 2000; Balter et al., 2002; 2012; Palmqvist et al., 2003; Lee-Thorp et al., 2003; Balter, 2004; Sponheimer et al., 2005; Sponheimer and Lee- Thorp, 2006; Domingo et al., 2012; Peek and Clementz, 2012; Qu et al., 2013). Strontium is a non-essential trace element, which mammals discriminate against relative to Ca in their intestines, kidneys, sites of bioapatite formation, and across the placenta and mammary glands (Taylor et al., 1962; Lengemann, 1963; Walser and Robinson, 1963; Underwood, 1977; Sasaki and Garant, 1986; Avioli, 1988; Rossipal et al., 2000; Chattopadhyay et al., 2007). This results in herbivore tissues having lower Sr/Ca ratios than the plants they consume and carnivores having lower Sr/Ca ratios than their prey (Elias et al., 1982; Burton et al., 1999; Blum et al., 2000). Systematic variations in Sr/Ca ratios also occur within trophic levels and can be used to assess the relative dietary contribution of certain plants and plant parts (Rao, 1979; Ruina, 1987; Burton et al., 1999; Sponheimer et al., 2005; Sponheimer and Lee-Thorp, 2006; Domingo et al., 2012). Due to a decrease in Sr concentration that occurs during xylem transport (centripetal accumulation) plant roots and stems have higher Sr/Ca ratios than leaves and fruits (Bowen and Dymond, 1955; Runia, 1987; Sillen, 1992; Burton et al., 1999; Sponheimer et al., 2005; Drouet and Herbauts, 2008). Grasses have been shown to have higher concentrations of Sr than the leaves of dicotyledonous plants (Sponheimer and Lee-Thorp, 2006). By analyzing the Sr/Ca ratios of sympatric mammalian herbivores it is possible to evaluate differences in dietary resource use and gain a better understanding of the factors that act to promote species coexistence. Here we use Sr/Ca ratios of fossil tooth enamel to evaluate dietary resource use within the ungulate community at Rudabánya II (R. II), an early Late Miocene (early Vallesian) (~10 Ma) vertebrate locality in northeastern Hungary. The faunal assemblage at R. II preserves

70 an abundance of forest-adapted fauna and presents a unique opportunity to examine species coexistence during a dynamic period in the evolution of terrestrial ecosystems in Europe.

During the early Vallesian (11.2 – 9.7 Ma), mammalian communities in Central and Western Europe achieved exceptionally high levels of species diversity (Agustí et al., 1997; 2001; 2013; Franzen and Stroch, 1999; Daxner-Höck, 2004; Bernor et al., 2005; Casanovas-Vilar et al., 2014; 2016). The entry of new woodland-adapted immigrant taxa (hipparione horses, giraffids, and boselaphine bovids) during this time is not associated with the local extinction of forest-adapted faunas (Agustí et al., 1997; Franzen and Stroch, 1999), suggesting low levels of competition. This period of optimum diversity was followed by the decline of forest-dwelling browsers and rise of woodland-adapted mixed-feeders and grazers (Fortelius et al., 2002). It was traditionally hypothesized that the diversity of forest-adapted taxa decreased abruptly at the early/late Vallesian boundary (~9.7Ma) in a faunal turnover event termed the Vallesian Crisis (Agustí and Moyà-Solà, 1990; Agustí et al., 1997; 1999; 2003; 2013; Fortelius et al., 1996; Fortelius and Hokkanen, 2001). However, more recent analysis suggests that the demise of forest-dwelling communities occurred gradually through a series of extinction events that began in the late Vallesian/early Turolian (Franzen et al., 2013; Casanovas-Vilar et al., 2014; 2016; Daxner-Höck et al., 2016).

To better understand how early Vallesian ecosystem functioned it is necessary to examine the complex ecological relationships that occurred within each trophic level. In this study, we use Sr/Ca ratios to evaluate the diets of early Vallesian ungulates with the aim of determining: (1) whether the sampled ungulate species show specialization for specific plants or plant parts, (2) whether Sr/Ca ratios support what is known about the ecology of these particular ungulate species from other methods, and (3) what factors may have acted to maintain coexistence within this diverse community of predominantly browsing herbivores.

Figure 3.1 The Pannonian Basin with estimated maximum extension of Lake Pannon at ca. 10 Ma indicated by white shading. Black diamond marks position of Rudabánya. Black circles indicate position of Belgrade, Bucharest, Budapest, Vienna, and Zagreb for reference (modified from Rögl, 1998; Magyar et al., 1999; Popov et al., 2004).

Geological Setting

Rudabánya is an early Late Miocene (early Vallesian) vertebrate paleontological locality situated within the Pannonian Basin, on the western flank of the northern Carpathian Mountains, in northeastern Hungary (N48°22'48.13", E20°37'43.57") (Figure 3.1). There are several vertebrate localities within the Rudabánya complex; the current study analyzes fauna from the Rudabánya II (R. II) locality. The fossiliferous deposits at Rudabánya accumulated near the shoreline of Lake Pannon, which formed at approximately 11.6 Ma (Kázmér, 1990, Rögl, 1998; Magyar et al., 1999; Popov et al., 2004). Lake Pannon reached its maximum extent (c. 290,000km2) between 10.5 – 10Ma, during a period of high precipitation and humidity (Magyar et al., 1999; Harzhauser and Mandic, 2004; Harzhauser, 2007; Harzhauser et al., 2008; Utescher et al., 2017). During this period coastal environments were characterized by extensive marshes

72 grading into forested-wetlands, and mixed evergreen and deciduous forest (Kretzoi et al., 1976; Erdei et al., 2007; Harzhauser et al., 2008; Halby and Erdei, 2013; Utescher et al., 2017). Palaeobotanical remains from R. II reflect a swamp association dominated by deciduous taxa (Kretzoi et al., 1976; Halby and Erdei, 2013). Stable isotope analysis of 10 species of ungulates from R. II indicates a variable forest environment, which included both open and closed canopy habitats (Eastham et al., 2016).

The depositional sequence at R. II is comprised of cyclic layers of clay, mud, and lignite totaling 8-12 meters. While the sequence is too short to tie into the geomagnetic timescale, the evolutionary stage of the fauna suggests it belongs near the top of the MN9 land mammal zone (10 – 9.8Ma) (Kordos, 1991; Andrews et al., 1997; Bernor et al., 2003; Andrews and Cameron, 2010; Casanovas-Vilar et al., 2011). The current study analyzes fauna from the black mud and gray marl depositional layers as one community. A lack of faunistic difference has been observed between theses depositional layers suggesting that they sample overlapping communities (Kordos and Begun, 2002). Stable isotope analysis showed no significant difference in the values of fauna from the black mud and gray marl indicating little, if any, change in environmental conditions (Eastham et al., 2011).

With 112 vertebrate species, including 69 species of mammals, R. II represents one of the richest early Vallesian palaeontological sites in Europe. The majority of the ungulate taxa are morphologically inferred as browsers including Dorcatherium naui (Tragulidae), Micromeryx flourensianus (Moschidae), Miotragocerus sp. (Bovidae), Tapirus cf. priscus (Tapiridae), Chalicotherium aff. goldfussi (Chalioctheriidae), Hoploaceratherium belvederense, Aceratherium incisivum, and Lartetotherium aff. sansaniensis (Rhinocerotidae), and Tetralophodon longirostris (Gomphotheriidae; Bernor et al., 2004). Suid taxa include a suine, Propotamochoerus palaeochoerus, first known from the Middle Miocene, and a primitive tetraconodont, Parachleuastochoerus kretzoii (Bernor et al., 2004). The equid Hippotherium intrans, a derived member of the Hippotherium primigenium lineage, shows morphological adaptations suggestive of more cursorial behaviour (Bernor et al., 2003; Scott et al., 2005). Patterns of meso- and microwear, as well as and stable isotope values indicate that the equid was an intermediate feeder (engaged in both browsing and grazing; Merceron et al., 2007; Tütken et al., 2013; Eastham et al., 2016). Intermediate feeding has also been interpreted for the cervid Lucentia aff. pierensis on the basis of meso- and microwear and stable isotopes (Merceron et al.,

2007; Eastham et al., 2016). R. II is one of the very few Late Miocene sites in Eurasia that preserves extensive samples of both a hominoid and pliopithecoid (Andrews et al., 1997: Harrison et al., 2002; Kordos and Begun, 2002; Armour-Chelu et al., 2005). Rudapithecus hungaricus and Anapithecus hernyaki have been recovered from the same depositional layers supporting the assumption of sympatry in these fossil primates (Andrews et al., 1997; Kordos & Begun 2002; Armour-Chelu et al., 2005).

Taxon Family N Sr/Ca x 1000 Mean SD Range Dorcatherium naui Tragulidae 4 0.52 0.13 0.45 To 0.7 Hippotherium intrans Equidae 8 0.89 0.23 0.62 To 1.21 Lucentia aff. pierensis Cervidae 9 0.92 0.27 0.6 To 1.26 Micromeryx flourensianus Moschidae 6 0.57 0.16 0.31 To 0.73 Miotragocerus sp. Bovidae 8 0.82 0.22 0.58 To 1.2 Parachleuastochoerus kretzoii Suidae 4 1.54 0.38 1.25 To 2.08 Propotamochoerus palaeochoerus Suidae 4 1.22 0.19 0.98 To 1.42 Tetralophodon longirostris Gomphotheriidae 2 0.77 0.05 0.73 To 0.8

Table 3.1 Descriptive statistics for the R. II ungulate species analyzed in this study.

Materials and Methods

All of the fauna sampled in the current study were recovered from the R. II locality within the Rudabánya complex. A total of 45 enamel samples from eight genera of medium to large-bodied mammals were analyzed (Table 3.1). Bedrock geology controls groundwater and soil trace element concentrations, making the direct comparison of trace element ratios from plants and animals living in different regions quite difficult (Sillen and Kavanagh, 1982; Sealy and Sillen, 1988; Sponheimer and Lee-Thorp, 2006; Kohn et al., 2013). Enamel was chosen for analysis over bone or dentine because of its increased resistance to diagenetic alteration, due in part to its greater mineral content and lack of natural pores (Lee-Thorp and van der Merwe, 1987, 1991; Wang and Cerling, 1994; Sponheimer and Lee-Thorp, 1999; Kohn et al., 1999; Tutken et al., 2008). While the majority of previous trace element studies have focused on Plio- Pleistocene and Holocene fossil material, works by Domingo et al. (2009 and 2012) and Eberle et al. (2009) have shown the preservation of biogenic signals in Middle Miocene and Early

Oligocene mammalian tooth enamel. Because the goal of our analysis was to examine variation in the feeding behaviour of adult animals, we preferentially sampled teeth that are among the last to develop, mineralize, and erupt (Hillson, 2005). Enamel (~10mg) was removed using a low speed FOREDOMTM drill and carbide dental burs. 2-3mm wide samples were taken along the non-occlusal surface parallel to the growth axis across the entire length of the tooth, which provides average values of resource use during tooth development, typically representing many months to a few years.

Samples were chemically pretreated with hydrogen peroxide (30%, H2O2) to remove organics and weak acetic acid (0.1 M, CH3CO2H) to remove secondary carbonates (Koch et al., 1997). Samples were centrifuged at a high speed and rinsed in distilled water to neutral pH before proceeding with the next solution. The remaining sample (~5 mg) was then dissolved in 1 ml of HNO3 in closed teflon beakers. After complete dissolution the beakers were opened and the samples evaporated to dryness on a hotplate. The residue was then dissolved in 0.5 ml of 6M

HNO3 and evaporated to dryness, then dissolved again 0.5 ml of 2.5M HNO3 and evaporated to dryness. Prior to analysis the samples were dissolved in 1 ml of 2% HNO3 solution. Sr and Ca concentrations were analyzed by using an Element XRTM inductively coupled plasma-mass spectrometer (ICP-MS) at the University of California, Santa Cruz. The precision of the ICP- MS is better than +/- 2-4%. Sr and Ca data are presented here as ratios multiplied by 1000 (e.g. Sr/Ca x 1000) (Sillen 1992; Balter et al., 2002; Palmqvist et al., 2003; Lee-Thorp et al., 2003; Sponheimer et al., 2005; Spomheimer and Lee-Thorp, 2006; Domingo et al., 2009; 2012). Sr/Ca ratios were compared among taxa using both parametric (ANOVA, Fisher’s LSD) and non- parametric (Kruskal-Wallis) tests where appropriate. Statistical analyses were run on SPSS 22.0, with significance set at p = <0.05.

Figure 3.2 Mean value ± 1 standard deviation plots of Sr/Ca enamel ratios of the R. II ungulates. Mammal reconstructions are not to scale.

sp.

Taxon

pierensis

intrans

H. H.

P. kretzoii P.

aff.

T.longirostris

L. L.

M. flourensianus M.

P. palaeochoerus P. Miotragocerus P. palaeochoerus 0.06 L. aff. pierensis 0.00* 0.04* Miotragocerus sp. 0.00* 0.01* 0.32 H. intrans 0.00* 0.03* 0.81 0.46 T. longirostris 0.00* 0.03* 0.4 0.83 0.5 M. flourensianus 0.00* 0.00* 0.00* 0.03* 0.01* 0.21 D. naui 0.00* 0.00* 0.02* 0.11 0.03* 0.34 0.74

Table 3.2. Significant differences in Sr/Ca ratios among the sampled R. II ungulate species.

Values shown with asterisks indicate significance for α≤0.05 using Fisher’s least significant difference test.

4 Results

The Sr/Ca ratios of the R. II fauna (Table 3.1; Figure 3.2, Appendix B) are comparable with those reported for both modern (Elias et al., 1982; Gilbert et al., 1994; Burton et al., 1999; Peek and Clementz, 2012; Martin et al., 2015) and fossil mammals (Balter et al., 2002; 2012; Lee-Thorp et al., 2003; Palmqvist et al., 2003; Sponheimer et al., 2005; Sponheimer & Lee- Thorp, 2006; Domingo et al., 2012). We found statistically significant differences in Sr/Ca ratios among taxa (Table 3.2) suggesting that diagenesis has not obscured the original ecological signal. Sympatric suids, Parachleuastochoerus kretzoii (x̅ = 1.54 ±0.38, n = 4) and Propotamochoerus palaeochoerus (x̅ = 1.22 ±0.19, n = 4), displayed the highest Sr/Ca ratios of the sampled fauna. The Sr/Ca ratios of the smaller tetraconodont suid P. kretzoii were higher than those of the larger suine P. palaeochoerus, but not significantly different (p = 0.06, Fisher’s LSD). The cervid Lucentia aff. pierensis (x̅ = 0.92 ±0.27, n = 9), bovid Miotragocerus sp. (x̅ = 0.82 ±0.22, n = 8), equid Hippotherium intrans (x̅ = 0.89 ±0.23, n = 8), and gomphothere Tetralophodon longirostris (x̅ = 0.77±0.05, n = 2), showed intermediate Sr/Ca ratios. Large- bodied ruminants L. aff. pierensis and Miotragocerus sp. yielded higher, but not significantly different (p = 0.989, Fisher’s LSD), Sr/Ca ratios than monogastric H. intrans and T. longirostris.

The tragulid Dorcatherium naui (x̅ = 0.52±0.13, n = 4) and moschid Micromeryx flourensianus (x̅ = 0.57±0.16, n = 6) displayed the lowest Sr/Ca ratios of the sampled fauna. The Sr/Ca ratios of the small-bodied ruminant M. flourensianus were significantly lower than those of the large- bodied ruminant Miotragocerus sp. (p = 0.03, Fisher’s LSD).

5 Discussion

We found significant differences in the Sr/Ca ratios of the R. II fauna indicative of differential dietary resource use (Figure 3.2; Table 3.2). Plant roots, rhizomes, and stems preferentially accumulate heavier alkaline-earth elements resulting in higher Sr concentrations than leaves, flowers, and fruits (Runia, 1987; Sillen et al., 1995; Burton et al., 1999). Several authors have linked elevated Sr/Ca ratios in modern and fossil mammals with the consumption of Sr-rich underground plant parts (Sealy and Sillen, 1988; Sillen et al., 1995; Burton et al., 1999; Lee-Thorp et al., 2003; Sponheimer et al., 2005; Sponheimer and Lee-Thorp, 2006). The suids showed the highest Sr/Ca ratios of the sampled fauna (Figure 3.2) suggesting diets rich in roots and rhizomes, which would have been abundant in the soft substrates along the margin of Lake Pannon. This interpretation is concordant with the higher carbon and lower oxygen isotope values reported for the R. II suids (Eastham et al., 2016). However, an omnivorous diet similar to that of the modern bush pig (Potamochoerus porcus) could also account for elevated Sr/Ca ratios (Balter et al., 2002; Sponheimer et al., 2005; Domingo et al., 2012). Patterns of molar emergence and wear indicate that the R. II suids had similar diets, with some degree of niche separation (Bernor et al., 2003). Bernor et al. (2003) suggest that the R. II locality was situated within the core habitat of the larger suine Propotamochoerus palaeochoerus and marginal to the preferred habitat of the smaller tetraconodont suid Parachleuastochoerus kretzoii. Stable isotope analysis also indicates differential dietary resource use, with P. palaeochoerus displaying significantly higher carbon isotope values than Parachleuastochoerus kretzoii (Eastham et al., 2016). Sr/Ca ratios support the interpretation of niche separation with P. kretzoii (x̅ = 1.54±0.38) showing comparatively higher Sr/Ca ratios than P. palaeochoerus (x̅ = 1.22±0.19). While it is likely that both of the R. II suids engaged in rooting the lower Sr/Ca ratios of P. palaeochoerus could indicate an increased dependence on Sr-poor resources, such as fruit. The higher and more varied Sr/Ca ratios of P. kretzoii could suggest a more omnivorous diet and/or an increased dependence on underground plant parts. An omnivorous diet has been interpreted for the Middle

Miocene tetraconodont suid Conohyus simorrensis on the basis of heterogeneous Sr/Ca ratios (Domingo et al., 2012).

The cervid Lucentia aff. pierensis (x̅ = 0.92±0.27) and equid Hippotherium intrans (x̅ = 0.89±0.23) share relatively higher Sr/Ca ratios, which could indicate intermediate feeding including some intake of C3 graminoids. Grazing herbivores have been shown to reflect higher Sr/Ca ratios than coexisting browsers (Sponheimer et al. 2005; Sponheimer and Lee-Thorp, 2006), as grasses are more enriched in Sr than dicotyledonous plants (Runia, 1987; Burton et al., 1999). A flexible feeding strategy that included the consumption of grasses, leaves, and possibly fruits has been interpreted for Late Miocene Hippotherium on the basis of stable isotope and meso- and microwear data (Merceron et al., 2007; Merceron, 2009; Tütken et al., 2013; Eastham et al., 2016). Meso- and microwear and stable isotope analysis of L. aff. pierensis also indicates intermediate feeding (Merceron et al., 2007; Eastham et al., 2016). Domingo et al. (2009 and 2012) analyzed the stable isotope, Sr/Ca, and barium/calcium (Ba/Ca) ratios of the Middle Miocene equid Anchitherium cf. A. cursor from the Somosaguas site in Spain, and interpreted intermediate feeding. The Sr/Ca ratios of Anchitherium were higher than those of the coexisting gomphothere, but slightly lower than those of the large-bodied ruminants (Domingo et al., 2012). At R. II, the Sr/Ca ratios of H. intrans are higher than those of the gomphothere Tetralophodon longirostris (x̅ = 0.77±0.05), and fall between those of the two large-bodied ruminants (L. aff. pierensis and Miotragocerus sp.).

Unlike the cervid and equid, the elevated Sr/Ca ratios of the bovid Miotragocerus sp. are incongruent with morphological and stable isotope data, which suggests a diet dominated by leaves with a small fruit component (Solounias and Dawson-Saunders, 1988; Spassov and Geraads, 2004; Merceron et al. 2007; Merceron, 2009; Eastham et al., 2016). This type of diet would typically be associated with relatively low Sr/Ca ratios (Burton et al., 1999; Lee-Thorp et al., 2003; Sponheimer et al., 2005; Drouet and Herbauts, 2008). The discrepancy between morphological and trace element data could be accounted for by differences in the gastrointestinal tract of ruminant vs. mongastric ungulates. Balter et al. (2002) found that ruminants were enriched in Ba compared to contemporaneous mongastric mammoths, rhinoceroses, and equids. These authors suggest that the prolonged retention of digesta in ruminant bodies, in addition to more efficient cellulose digestion, results in a greater concentration of non-essential trace elements in the bones and teeth. Deer and antelope have

79 been shown to yield significantly higher Ba/Ca ratios than other non-ruminant herbivores (Gilbert et al., 1994; Burton et al., 1999). Domingo et al. (2009 and 2012) found the highest Sr/Ca and Ba/Ca ratios in the large-bodied ruminants at the Somosaguas site. At R. II, the Sr/Ca ratios of Miotragocerus sp. are higher than those of the gomphothere T. longirostris (x̅ = 0.77±0.05) and comparable with those of the cervid and equid. While limited by sample size (n = 2), the Sr/Ca ratios of T. longirostris are congruent with morphological and stable isotope data indicating a browsing diet (Agustí and Antón, 2002; Domingo et al., 2013; Eastham et al., 2016). It is likely that the comparatively higher Sr/Ca ratios of the bovid reflect a different digestive physiology (ruminant vs. monogastric) rather than a significant difference in diet.

Dorcatherium naui (x̅ = 0.52±0.13; Tragulidae) and Micromeryx flourensianus (x̅ = 0.57±0.16; Moschidae) displayed the lowest Sr/Ca ratios of the sampled fauna (Table 3.2; Figure 3.2) indicating a preference for Sr-poor plants or plant parts. Trace element concentrations are unevenly distributed in plants, with the highest concentrations in the roots and lowest concentrations in the fruits (Rao, 1979; Ruina, 1987; Burton et al., 1999; Drouet and Herbauts, 2008). For example, an early study of chicku (Achras sapota) and mango (Mangifera indica) trees revealed lower Sr concentrations in fruits as compared to leaves (Rao, 1979). The low Sr/Ca ratios of D. naui and M. flourensianus are in accordance with morphological and stable isotope data indicating a dietary preference for fruit (Tütken et al., 2006; Merceron et al., 2007; Merceron, 2009; Aiglstorfer et al., 2014; Eastham et al., 2016). The presence of species dependent on fruit is consistent with the abundance of endocarps recovered from R. II (Kordos and Begun, 2002; Hably and Erdei, 2013). D. naui and M. flourensianus are suggested to have occupied a similar niche to extant duikers (Cephalophus sp.) and water chevrotains (Hyemoschus aquaticus), which inhabit the forest floors of tropical Africa and selectively feed on fruits and seeds fallen from the canopy (Köhler, 1993; Nowak, 1999; Cerling et al., 2004; Merceron et al., 2007; 2009; Rössner, 2007; Alba et al., 2011).

Interestingly, the Sr/Ca ratios of M. flourensianus were significantly lower (p = 0.03, Fisher’s LSD) than those of the bovid Miotragocerus sp. (Figure 3.2; Table 3.2). The results are unexpected given that both species were ruminants thought to have browsed on leaves and fruits (Tütken et al., 2006; Merceron et al., 2007; Merceron, 2009; Aiglstorfer et al., 2014; Eastham et al., 2016), which are Sr-poor plant resources. As far as we know, the behavior of Sr in the gastrointestinal tracts of small vs. large-bodied ruminants has not yet been studied, so no

80 conclusive remarks can be made. However, it is possible that the unique digestive adaptations of extant small-bodied ruminant frugivores could help to clarify this finding. Rumination is a relatively inefficient way to obtain energy from low fiber foods, like most fruits (Cork, 1996). Despite this, many small-bodied ruminants living in tropical forests throughout the world depend on fruit for energy and nutrients. The success of small-bodied ruminant frugivores has been related to several adaptations in their digestive process. Their small rumen and fermentation capacity relative to energy requirements requires that they eat more readily fermentable carbohydrates and subsequently pass plant fiber more rapidly through the digestive tract (Demment and Van Soest, 1985). They also tend to have a larger reticulo-omasal orifice, which allows some digesta to escape rumen fermentation (Hofmann, 1973). If the prolonged retention of digeta by large-bodied ruminants is associated with an increase in the uptake of non-essential trace elements, it seems plausible that the rapid passage of digesta by small-bodied ruminant frugivores could result in a decrease in trace element uptake. Testing this hypothesis, however, requires further baseline work with modern ruminants examining the behaviour of Sr under different digestive strategies.

Determining ecological relationships within trophic levels is important for understanding how ecosystems function. The niche partitioning hypothesis predicts that ecologically similar species can coexist by partitioning their resources in one or more of the three primary niche dimensions (diet, habitat and time; Hardin, 1960; Schoener, 1974; DiBitetti et al., 2009), with diet being the most commonly segregated axis among herbivores (Stewart et al., 2002). Trace element analysis shows significant differences in dietary resource use within the early Late Miocene ungulate community at R. II, implying that the different analyzed ungulate species did partition resources by selecting different plants and/or plant parts, which would diminish competition. However, the overlapping ranges of Sr/Ca values displayed by the two suids, the cervid and equid, and the tragulid and moschid indicate some degree of dietary niche overlap. Studies of modern herbivore communities have demonstrated increased dietary niche overlap during periods of resource abundance. The low levels of feeding competition that occur during these periods promote the coexistence of ecologically similar species (Pyke et al., 1977; Gordon and Illius, 1989; Stevenson et al., 2000; Levine and HilleRisLambers 2009; Singh et al., 2011; Djagoun et al., 2013; Landman et al., 2013; Kartzinel et al., 2015). A local abundance of plant

81 resources in addition to dietary resource partitioning likely acted as the primary factors promoting species coexistence within the ungulate community at R. II.

While the fossil record at R. II provides important information for understanding the factors that acted to promote the assembly and coexistence of early Vallesian mammalian communities, it lacks the depth of time required to evaluate changes in faunal diversity through time. Recent analysis of small mammal diversity in the Vallès-Penedès Basin in Spain indicates a slow decline in taxonomic richness occurring since the late Vallesian (Casanovas-Vilar et al. 2014; 2016). These findings are contrary to previous studies, which report an abrupt extinction event at the early/late Vallesian boundary (the Vallesian Crisis) (Agustí and Moyà-Solà, 1990; Agustí et al., 1997; 1999; 2003; 2013). Casanovas-Vilar et al. (2014 and 2016) suggest that the decline of forest-dwelling taxa occurred gradually through a series of extinction events beginning in the late Vallesain. These authors assert that the abrupt pattern of extinctions interpreted as the “Vallesian Crisis” results from uneven sampling. In Central Europe, studies by Franzen et al. (2013) and Daxner-Hö ck et al. (2015) have demonstrated the persistence of some forest-adapted fauna (chalicotheres, moschids, and certain rodents) well into the early Turolian. Environmental changes associated with the Late Miocene cooling are not well expressed in the Pannonian Basin (Ivanov et al., 2011; Hably, 2013; Utescher et al., 2017), due to the buffering effect of Lake Pannon. A recent palaeoclimatic study utilizing plant functional types (PFTs) indicates constantly humid conditions along the northern margin of lake throughout the early and middle Turolian (Utescher et al., 2017).

6 Conclusions

Examination of tooth enamel Sr/Ca ratios in early Late Miocene ungulates from R. II showed significant differences in dietary resource use. In general, the Sr/Ca ratios of the sampled species support previous ecological determinations made on the basis of morphological and stable isotope data. The suids Parachleuastochoerus kretzoii and Propotamochoerus palaeochoerus displayed the highest Sr/Ca ratios suggesting a preference for Sr-rich roots and rhizomes. Parachleuastochoerus kretzoii yielded higher and more heterogeneous Sr/Ca ratios than Propotamochoerus palaeochoerus, which could be indicative of a more omnivorous diet. Elevated Sr/Ca ratios exhibited by the cervid Lucentia aff. pierensis and equid Hippotherium intrans suggests intermediate feeding, which included the intake of C3 graminoids. The bovid

Miotragocerus sp. displayed higher Sr/Ca ratios, suggesting intermediate feeding, than the gomphothere Tetralophodon longirostris. The implication for Miotragocerus sp. as an intermediate feeder is incongruent with morphological and stable isotope data, which identifies it as a browser. This discrepancy likely reflects a difference in digestive physiology (ruminant vs. monogastric) as opposed to a difference in dietary behaviour. The traguild Dorcatherium naui and moschid Micromeryx flourensianus showed the lowest Sr/Ca ratios of the sampled R. II fauna suggesting a preference for Sr-poor fruit. A similar range of Sr/Ca values were found in several of the sampled species implying some degree of interspecific competition. To diminish potential competition it is likely that the different ungulate species partitioned plant resources within the local environment, which would have acted to promote coexistence within this diverse community of predominantly browsing herbivores. This study further highlights the utility of trace element ratios to discern the complex ecological relationships of species in ancient ecosystems.

Acknowledgements

Funding and/or logistical support was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) (RGPIN-2016-06761), the National Geographic Society (8801-10), Ontario Graduate Scholarship, Geological Society of America Research Award, General Motors Women in Science and Mathematics Award, University of Toronto Graduate Fellowship, and the New York State Museum. We thank the Geological and Geophysical Institute of Hungary (MAFI). We thank L. Kordos, J. Halfar, D. Bovee, and D. Boutilier for their contributions to this research.

References

Agustí, J., Cabrera, L., Garcés, M., 2013. The Vallesian mammal turnover: A Late Miocene record of decoupled land-ocean evolution. Geobios, 46, 151-157.

Agustí, J., 2007. The biotic environments of the Late Miocene hominids. In: Henke, W., Tattersall, I. (eds.). Handbook of Paleoanthropology, Berlin, Springer, 979 - 1010.

Agustí, J., Siria, A. S. d., Garcés, M., 2003. Explaining the end of the hominoid experiment in Europe. Journal of Human Evolution, 45, 145-153.

Agustí, J., and M. Antón., 2002. Mammoths, Sabertooths, and Hominids: 65 Million Years of Mammalian Evolution in Europe. New York, Columbia University Press, 313pp.

Agustí, J., Cabrera, L., Garcés, M., Llenas, M., 1999. Mammal turnover and Global climate change in the Late Miocene terrestrial record of the Vallès-Penedès Basin (NE Spain). In: Agustí, J., Rook, L., Andrews, P. (eds.). Hominoid Evolution and Climatic Change in Europe. Vol. 1: The Evolution of Neogene Terrestrial Ecosystems in Europe. Cambridge University Press, Cambridge, 390–397.

Agustí, J., Cabrera, L., Garcés, M., Parés, J.M., 1997. The Vallesian mammal succession in the Vallès-Penedès basin (Northeast Spain): paleomagnetic calibration and correlation with global events. Palaeogeography, Palaeoclimatology, Palaeoecology, 133, 149–180.

Agustí, J., Moyà-Solà, S., 1990. Mammal extinctions in the Vallesian (Upper Miocene). Lecture Notes in Earth Sciences, 30, 425–432.

Aiglstorfer, M., Bocherens, H., Böhme, M., 2014. Large Mammal Ecology in the late Middle Miocene locality Gratkorn (Austria). Palaeobiodiversity and Palaeoenvironments, 94, 189– 213.

Alba, D.M., Moyà-Solà, S., Robles, J.M., Casanovas-Vilar, I., Rotgers, C., Carmona, R., Galindo, J., 2011. Middle Miocene tragulid remains from Abocador de Can Mata: the earliest record of Dorcatherium naui fromWestern Europe. Geobios, 44, 135–150.

Andrews, P., Cameron, D., 2010. Rudabànya: Taphonomic analysis of a fossil hominid site from Hungary. Palaeogeography, Palaeoclimatology, Palaeoecology, 297, 311-329.

Andrews, P., Harrison, T., Martin, L., Delson, E., Bernor, R.L., 1996. Systematics and biochronology of European Neogene catarrhines. In: Bernor, R., Fahlbusch, V. (eds.). Evolution of Neogene Continental Biotopes in Europe and the Eastern Mediterranean, New York, Columbia University Press, 168-207.

Armour-Chelu, M., Andrews, P., Bernor, R. L., 2005. Further observations on the primate community at Rudabánya II (Late Miocene, early Vallesian age), Hungary. Journal of Human Evolution, 49, 88-98.

Avioli, L. V., 1988. Calcium and phosphorus. In: Shils, M.E., Young, V.R. (eds.). Modern Nutrition in Health and Disease, Philadelphia, Lea and Febiger, 142-148.

Balter, V., Braga, J., Telouk, P., Thackeray, F., 2012. Evidence for dietary change but not landscape use in South African early hominins. Nature, 489, 558–560.

Balter, V., 2004. Allometric constraints on Sr/Ca and Ba/Ca partitioning in terrestrial mammalian trophic chains. Oecologia, 139, 83–88.

Balter, V., Bocherens, H., Person, A., Labourdette, N., Renard, M., Vandermeersch, B., 2002. Ecological and physiological variability of Sr/Ca and Ba/Ca in mammals of West European mid-Wü rmian food webs. Palaeogeography, Palaeoclimatology, Palaeoecology, 186, 127-143.

Begun, D.R., 2007. Fossil record of Miocene hominoids. In: Henke, W., Tattersall, I. (eds.). Handbook of Paleoanthropology, Heidelberg, Springer, 921-977.

Bernor, R.L., Fahlbusch, V., Andrews, P., de Bruijn, H., Fortelius, M., Rögl, F., Steininger, F.F., Werdelin, L., 1996. The evolution of European and West Asian later Neogene faunas: a biogeographic and paleoenvironmental synthesis. In: Bernor, R., Fahlbusch, V., Mittmann,

W. (eds.), The Evolution of Western Eurasian Neogene Mammal Faunas. Columbia University Press, 449–470.

Blum, J.D., Taliaferro, H., Weisse, M.T., Holmes, R.T., 2000. Changes in Sr/Ca, Ba/Ca and 87Sr/86Sr ratios between trophic levels in two forest ecosystems in the northeastern USA. Biogeochemistry, 49, 87-101.

Bowen, H.J.M., Dymond, J.A., 1955. Strontium and barium in plants and soils. Proceedings of the Royal Society of London, 144(B), 355-368.

Burton, J.H., Price, T.D., Middleton, W.D., 1999. Correlation of bone Ba/Ca and Sr/Ca due to biological purification of calcium. Journal of Archaeological Science, 26, 609-616.

Casanovas-Vilar, I., Madern, A., Alba, D.M., Cabrera, L., García-Paredes, I., Van den Hoek Ostende, L.W., DeMiguel, D., Robles, J.M., Furió, M., van Dam, J., Garcés, M., Angelone, C., Moyà-Solà, S., 2016. The Miocene mammal record of the Vallès-Penedès Basin (Catalonia). Comptes Rendus Palevol 15, 791–812.

Casanovas-Vilar, I., Van den Hoek Ostende, L.W., Furió, M., Madern, P.A., 2014. The range and extent of the Vallesian Crisis (Late Miocene): new prospects based on the micromammal record from the Vallès-Penedès basin (Catalonia, Spain). Journal of Iberian Geololgy, 40, 29–48.

Casanovas-Vilar, I., Alba, D.M., Garcés, M., Robles, J.M., Moyá-Solá, S., 2011. Updated chronology for the Miocene hominoid radiation in western Eurasia. Proceedings of the National Academy of Sciences, 108, 5554-5559.

Cerling, T. E., Hart, J. A., Hart, T. B., 2004. Stable isotope ecology in the Ituri forest. Oecologia, 138, 5-12.

Chattopadhyay, N., Quinn, S. J., Kifor, O., Ye, C., Brown, E. M., 2007. The calcium-sensing receptor (CaR) is involved in strontium ranelate-induced osteoblast proliferation. Biochemical Pharmacology, 74, 438–447.

Cork, S., 1996. Optimal digestive strategies for arboreal herbivorous mammals in contrasting 354 forest types: why koalas and colobines are different. Australian Journal of Ecology, 21, 10-20.

Daxner-Höck, Harzhauser, M., Göhlich, U.B., 2016. Fossil record and dynamics of Late Miocene small mammal faunas of the Vienna basin and adjacent basins, Austria. Comptes Rendus Palevol, 15, 855-862.

Daxner-Höck, G., 2004. Biber und ein zwerghamster aus Mataschen (unter-pannonium, steirisches becken). Joannea Geologie Und Paläontologie, 5, 19-33.

Demment, M.W., Van Soest, P.J., 1985. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. American Naturalist, 125, 641-672.

DiBitetti, M. S., Di Blanco, Y. E., Pereira, J. A., Paviolo, A., Jiménez Pérez, I., 2009. Time partitioning favors the coexistence of sympatric crab-eating foxes (Cerdocyon thous) and pampas foxes (Lycalopex gymnocercus). Journal of Mammalogy, 90, 479–490.

Domingo, M.S., Domingo, L., Badgley, C., Sanisidro, O., Morales, J., 2013. Resource partitioning among top predators in a Miocene food web. Proceedings of the Royal Society of London B 280: 20122138.

Domingo, L., López-Martínez, N., Grimes, S.T., 2012. Trace element analyses indicative of paleodiets in Middle Miocene Mammals from the Somosaguas site (Madrid, Spain). Geologica Acta, 10, 1-12.

Domingo, L., Cuevas-Gonzalez, J., Grimes, S.T., Hernandez Fernandez, M., Lopez-Martinez, N., 2009. Multiproxy reconstruction of the palaeoclimate and palaeoenvironment of the Middle Miocene Somosaguas site (Madrid, Spain) using herbivore dental enamel. Palaeogeography, Palaeoclimatology, Palaeoecology, 272, 53-68.

Drouet, T., Herbauts, J., 2008. Evaluation of the mobility and discrimination of Ca, Sr and Ba in forest ecosystems: consequence on the use of alkaline-earth element ratios as tracers of Ca. Plant Soil, 302, 105–124.

Eastham, L., Feranec, R.S., Begun, D.R., 2016. Stable isotopes show resource partitioning among the early Late Miocene herbivore community at Rudabánya II: Palaeoenvironmental implications for the hominoid, Rudapithecus hungaricus. Palaeogeography, Palaeoclimatology, Palaeoecology, 454, 161–174.

Eastham, L., Feranec, R.S., Begun, D.R., Kordos, L., 2011. Resource partitioning in Late Miocene Central European Mammals: Isotopic evidence from the Rudabánya fauna. Journal of Vertebrate Paleontology, 31 (Suppl. 2), 103.

Eberle, J., Sponheimer, M., Marchitto, T., 2009. Biogenic patterning of Sr and Ba in Early Oligocene (Orellan) mammalian tooth enamel. Journal of Vertebrate Paleontology, 29, 91A.

Elias, R.W., Hirao, Y., Patterson, C.C., 1982. The circumvention of the natural biopurification of calcium along nutrient pathways by atmospheric inputs of industrial lead. Geochimica et Cosmochimica Acta, 46, 2561-2580.

Erdei, B., Hably, L., Kázmér, M., Utescher, T., Bruch, A., 2007. Neogene flora and vegetation development of the Pannonian domain in relation to palaeoclimate and palaeogeography. Palaeogeography, Palaeoclimatology, Palaeoecology, 253, 131–156.

Fortelius, M., Hokkanen, A., 2001. The trophic context of hominoid occurrence in the later Miocene of western Eurasia—a primate-free view. In: de Bonis, L., Koufos, G., Andrews, A., (eds.). Phylogeny of the Neogene Hominoid Primates of Eurasia, Cambridge, Cambridge University Press, 19-47.

Franzen, J.L., Pickford, M., Costeur, L., 2013. Palaeobiodiversity, palaeoecology, palaeobiogeography and biochronology of Dorn-Dü rkheim 1 – a summary. Palaeodiversity and Palaeoenvironments 93, 277–284.

Franzen, J. L., Storch, G., 1999. Late Miocene mammals from central Europe. Hominoid Evolution and Climatic Change in Europe. In: Agustí, J.L., Rook, L., Andrews, P. (eds). The evolution of Neogene terrestrial ecosystems in Europe, Cambridge, Cambridge University Press, 165-190.

Gilbert, C., Sealy, J., Sillen, A., 1994. An investigation of barium, calcium and strontium as palaeodietary indicators in the Southwestern Cape, South Africa. Journal of Archaeological Science 21, 173-184.

Hably, L., 2013. The Late Miocene flora of Hungary. Geol. Hung. Ser. Palaeontol. 59, 1–175.

Hably, L., Erdei, B., 2013. A refugium of mastixia in the Late Miocene of eastern central Europe. Review of Palaeobotany and Palynology, 197, 218-225.

Hardin, G., 1960. The competitive exclusion principle. Science 131, 1292–1297.

Harris, J. M., Cerling, T. E., 2002. Dietary adaptations of extant and Neogene African suids. Journal of Zoology, 256, 45-54.

Harzhauser, M., Latal, C., Piller, W. E., 2007. The stable isotope archive of Lake Pannon as a mirror of Late Miocene climate change. Palaeogeography, Palaeoclimatology, Palaeoecology, 249, 335-350.

Harzhauser, M., Mandic, O., 2004. The muddy bottom of Lake Pannon - A challenge for dreissenid settlement (Late Miocene; bivalvia). Palaeogeography, Palaeoclimatology, Palaeoecology, 204, 331-352.

Hillson, S., 2005. Teeth, Cambridge Manuals in Archaeology (2nd Ed.). Cambridge University Press, Cambridge.

Hofmann, R.R., 1973. The ruminant stomach. Nairobi, East African Literature Bureau.

Ivanov, D., Utescher, T., Mosbrugger, V., Syabryaj, S., Dordjevic-Milutinovic, D., Molchanoff, S., 2011. Miocene vegetation and climate dynamics in Eastern and Central Paratethys (Southeastern Europe). Palaeogeography, Palaeoclimatology, Palaeoecology, 304, 262–275.

Kázmér, M., 1990. Birth, life and death of the Pannonian Lake. Palaeogeography, Palaeoclimatology, Palaeoecology, 79, 171-188

Koch, P. L., Tuross, N., Fogel, M. L., 1997. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. Journal of Archaeological Science, 24, 417-429.

Kohn, M.J., Morris, J., Olin, P., 2013. Trace element concentrations in teeth – a modern Idaho baseline with implications for archeometry, forensics, and paleontology. Journal of Archaeological Science, 40, 1689-1699.

Kohn, M.J., Schoeninger, M.J., Barker, W.W., 1999. Altered states: effects of diagenesis on fossil tooth chemistry. Geochimica et Cosmochimica Acta, 63, 2737-2747.

Kordos, L., Begun, D. R., 2002. Rudabánya: A Late Miocene subtropical swamp deposit with evidence of the origin of the African apes and humans. Evolutionary Anthropology, 11, 45- 57.

Kordos, L., 1991. Le Rudapithecus hungaricus de Rudabànya (Hongrie). L'Anthropologie, 95, 343–362.

Kretzoi, M., Krolopp, E., Lörincz, H., Pálfalvy, I., 1976. A Rudabanyai also pannonai prehominidas lelohely floraja, faunaja es retegtani helyzete. Annual Report of the Hungarian Geological Institute, 365-394.

Lee-Thorp, J.A., Sponheimer, M., van der Merwe, N.J., 2003. What do stable isotopes tell us about hominid dietary and ecological niches in the Pliocene? International Journal of Osteoarchaeology, 13, 104-113.

Lee-Thorp, J.A., Van der Merwe, N.J., 1991. Aspects of the chemistry of modern and fossil biological apatites. Journal of Archaeological Science, 18, 343-354.

Lee-Thorp, J.A., Van der Merwe, N.J., 1987. Carbon isotope analysis of fossil bone apatite. South African Journal of Science, 83, 712-715.

Lengemann F. W., 1963. Over-all Aspects of Calcium and Strontium Absorption, the Transfer of Calcium and Strontium across Biological Membranes. New York, Academic Press, 85pp.

Levine, J.M., HilleRisLambers, J., 2009. The importance of niches for maintenance of species diversity. Nature 461, 254 – 257.

Magyar, I., Geary, D. H., Müller, P., 1999. Paleogeographic evolution of the Late Miocene Lake Pannon in central Europe. Palaeogeography, Palaeoclimatology, Palaeoecology, 147, 151- 167.

Martin, J.E., Vance, D., Balter, V., 2015. Magnesium stable isotope ecology using mammal tooth enamel. Proceedings of the National Academy of Sciences, 112, 430 – 435.

Merceron, G., Kaiser, T.M., Kostopoulos, D.S., Schulz, E., 2010. Ruminant diets and the Miocene extinction of European great apes. Proceedings of the Royal Society Biology, 277, 3105-3112. Merceron, G., 2009. The early Valleisan vertebrates of Atzelsdorf (Late Miocene, Austria). Annals of the Natural History Museum Vienna, 111A, 647 – 660.

Merceron, G., Schulz, E., Kordos, L., Kaiser, T. M., 2007. Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: Evidence from dental meso- and micro-wear analyses of large vegetarian mammals. Journal of Human Evolution, 53, 331-349 Nowak, R.M. 1991. Walker's Mammals of the World (Fifth Edition). Baltimore, Johns Hopkins University Press, 1936pp.

Palmqvist, P., Gröcke, D.R., Arribas, A., Fariña, R.A., 2003. Paleoecological reconstruction of a lower Pleistocene large mammal community using biogeochemical (δ13C, δ15N, δ18O, Sr:Zn) and ecomorphological approaches. Paleobiology, 29, 205-229.

Peek, S., Clementz, M.T., 2012. Sr/Ca and Ba/Ca variations in environmental and biological sources: A survey of marine and terrestrial systems. Geochimica et Cosmochimica Acta, 95, 36–52.

Qu, Y., Jin, C., Zhang, Y., Hu, Y., Shang, X., Wang, C., 2013. Distribution patterns of elements in dental enamel of G. blacki: a preliminary dietary investigation using SRXRF, Applied Physics A - Materials Science & Processing, 111, 75-82.

Rao, S.R., 1979. Elemental concentration in fruit and leaves of chicku and mango under natural environmental conditions. Proceedings of the Indian Academy of Science, 88, 175-182.

Rögl, V.F., 1998. Palaeogeographic considerations for Mediterranean and Paratethys seaways (Oligocene to Miocene). Annals of the Natural History Museum Vienna, 99A, 279–310.

Rössner, G. E., 2007. Family tragulidae. The Evolution of Artiodactyls, 213-220.

Rossipal, E., Krachler, M., Li, F., Turk Micetic, D., 2000. Investigation of the transport of trace elements across barriers in humans: studies of placental and mammary transfer. Acta Paediatr, 89, 1190–1195.

Runia, L.T., 1987. Strontium and calcium distribution in plants: Effect on palaeodietary studies. Journal of Archaeological Science, 14, 599-608.

Sasaki, T., Garant, P., 1986. Ultracytochemical demonstration of ATP-dependent calcium pump in ameloblasts of rat incisor enamel organ. Calcified Tissue International, 39, 86–96.

Schoener, T. W., 1974. Resource partitioning in ecological communities. Science, 185, 27-39.

Sealy, J. C., Sillen, A., 1988. Sr and Sr/Ca in marine and terrestrial foodwebs in the southwestern cape, South Africa. Journal of Archaeological Science, 15, 425–438.

Sillen, A., Hall, G., Armstrong, R., 1995. Strontium calcium ratios (Sr/Ca) and strontium isotopic ratios (87Sr/86Sr) of Australopithecus robustus and Homo sp. from Swartkrans. Journal of Human Evolution, 28, 277–285.

Sillen, A., 1992. Strontium-calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. Journal of Human Evolution, 23, 495-516.

Sillen, A., 1986. Biogenic and diagenetic Sr/Ca in Plio-Pleistocene fossils of the Omo Shungura Formation. Paleobiology, 12, 311-323.

Singh, M., Roy, K., Singh, M., 2011. Resource partitioning in sympatric langurs and macaques in tropical rainforests of the western Ghats, South India. American Journal of Primatology, 73, 355 – 346.

Sillen, A., Kavanagh, M., 1982. Strontium and paleodietary research: A review. Yearbook of Physical Anthropology, 25, 67-90.

Solounias, N., Dawson-Saunders, B., 1988. Dietary adaptations and palaeoecology of the Late Miocene ruminants from Pikermi and Samos in Greece. Palaeogeography, Palaeoclimatology, Palaeoecolology 65, 149 - 172.

Sponheimer, M., Lee-Thorp, J.A., 2006. Enamel diagenesis at South African Australopith sites: Implications for paleoecological reconstruction with trace elements. Geochimica et Cosmochimica Acta, 70, 1644-1654.

Sponheimer, M., de Ruiter, D., Lee-Thorp, J., Spath, A., 2005. Sr/Ca and early hominin diets revisited: new data from modern and fossil tooth enamel. Journal of Human Evolution, 48, 147-156.

Sponheimer, M., Lee-Thorp, J.A., 1999. Alteration of enamel carbonate environments during fossilization. Journal of Archaeological Science, 26, 143-150.

Stewart, K. M., R. T. Bowyer, J. G. Kie, N. J. Cimon, Johnson, B.K., 2002. Temporospatial distributions of elk, mule deer, and cattle: resource partitioning and competitive displacement. Journal of Mammalogy, 83, 229-244.

Taylor, D., Bligh, P., Duggan, M. H., 1962. The absorption of calcium, strontium, barium and radium from the gastrointestinal tract of the rat. Biochemical Journal, 83, 25–29.

Tü tken, T., Vennemann, T.W., Pfretzschner, H.U., 2008. Early diagenesis of bone and tooth apatite in fluvial and marine settings: Constraints from combined oxygen isotope, nitrogen and REE analysis. Palaeogeography, Palaeoclimatology, Palaeoecology, 266, 254-268.

Underwood, E. J., 1977. Trace Elements in Human and Animal Nutrition, Fourth Ed. New York, Academic Press Inc., 545pp.

Utescher, T., Erdei, B., Hably, L., Mosbrugger, V., 2017. Late Miocene vegetation of the Pannonian Basin. Palaeogeography, Palaeoclimatology, Palaeoecology, 467, pp. 131-148. van Dam, J. A., 2006. Geographic and temporal patterns in the late Neogene (12-3 Ma) aridification of Europe: The use of small mammals as paleoprecipitation proxies. Palaeogeography, Palaeoclimatology, Palaeoecology, 238, 190-218.

Walser, M., Robinson, B. H. B., 1963. Renal Excretion and Tubular Reabsorption of Calcium and Strontium, Transfer of Calcium and Strontium across Biological Membranes. New York, Academic Press, 326pp.

Wang, Y., Cerling, T.E., 1994. A model of fossil tooth and bone diagenesis: implications for paleodiet reconstruction from stable isotopes. Palaeogeography, Palaeoclimatology, Palaeoecology, 107, 281-289.

Chapter 4

Paleoclimate of the early Late Miocene Rudabánya II (R. II) Primate Locality Inferred from the Stable Isotope Compositions of Equid Enamel Apatite

In revision with: Journal of Human Evolution

Hominoids and pliopithecoids underwent a dramatic radiation in Eurasia during the Middle and early Late Miocene. Despite their broad geographic and temporal range the co-occurrence of these primate groups is extremely rare in the fossil record. Humidity has been suggested as a key environmental factor influencing their distribution. The rich early Late Miocene vertebrate locality of Rudabánya II (R. II) in northeastern Hungary is unique in preserving extensive samples of the fossil great ape, Rudapithecus hungaricus, and pliopithecoid, Anapithecus hernyaki. Here we use the carbon and oxygen stable isotope compositions of tooth enamel 13 18 carbonate (δ CE and δ OE) from the equid Hippotherium intrans to evaluate the climatic regime under which the R. II primates lived. An estimated mean annual precipitation (MAP) ranging 13 between 1030 and 1333 mm/yr was calculated from the average δ CE value of H. intrans (- 12.7‰). A mean annual temperature (MAT) ranging between 11°C and 14°C was calculated 18 from the average δ OE value (-7.2‰). MAT estimates reported here are lower than those derived from small mammal and paleobotanical proxies (~14 -16°C). Two factors could account for the lower MAT estimates: (1) drinking from water sources originating at higher elevations, such as rivers and streams flowing from mountainous regions, and/or (2) the amount effect.

18 13 Serial isotope analysis revealed relatively low average amplitudes of δ OE (1.8‰) and δ CE (0.8‰) variation. The estimated annual range of variation in drinking water stable oxygen 18 18 isotope (δ OH2O) values is 4.5‰. This value is lower than the modern range of δ O measured in precipitation at nearby reference stations, indicating that seasonal changes in climate were considerably milder during the early Late Miocene. Our interpretations are concordant with those of previous studies suggesting that the R. II primates experienced a humid and wet subtropical climate with relatively mild seasonality during the early Late Miocene.

1 Introduction

A vast radiation of catarrhine primates took place in Eurasia during the Middle and early Late Miocene. The first anthropoids to disperse across the continent were the pliopithecoids, a diverse superfamily of stem catarrhines that predate the cercopithecoid-hominoid split (Harrison, 2002; Begun, 2002, 2007). Following the dispersal of pliopithecoids, hominoids migrated into Eurasia where they diversified into more than 10 genera ranging between Spain and southeastern Asia (Begun, 2002, 2007, 2009). Despite the broad and penecontemporaneous distribution of the two primate groups their co-occurrence in the fossil record is extremely rare (Andrews et al., 1996; Harrison et al., 2002; Alba et al., 2011; Almécija et al., 2012; Sukselainen et al., 2015). It has been suggested that differences in the habitat preference of hominoids and pliopithecoids allowed for only minimal overlap in their geographic distribution (Andrews et al., 1996; Harrison et al., 2002; Armour-Chelu et al., 2005). Ecometric and ecological diversity studies indicate that humidity was a key environmental factor influencing the distribution of these primate groups (Eronen and Rook, 2004; Sukselainen et al., 2015). It seems critical then to evaluate the climatic context of localities where hominoids and pliopithecoids co-occurr.

The early Late Miocene (early Vallesian ~ 10 Ma) vertebrate locality of Rudabánya II (R. II) in northeastern Hungary is unique in preserving extensive samples of the hominoid, Rudapithecus hungaricus, and pliopithecoid, Anapithecus hernyaki (Harrison et al., 2002; Kordos and Begun, 2002; Armour-Chelu et al., 2005; Sukselainen et al., 2015). Here, Rudapithecus and Anapithecus have been recovered from within centimeters of each other at the same elevation and within the same depositional layer, indicating their likely co-occurrence in space and time (Begun et al., 2010). In this study we use stable carbon and oxygen isotope ratios

(δ13C and δ18O) of fossil equid enamel to investigate the climatic regime under which the Rudabánya primates lived.

Over the past two decades stable isotope analysis of fossil tooth enamel has been extensively utilized in the reconstruction of Miocene paleoclimates and paleoecology (Bocherens et al., 1994; Quade et al., 1995; Cerling et al., 1997; MacFadden and Higgins, 2004; Nelson, 2005, 2007; Hernández-Fernández et al., 2006; Tütken et al., 2006; 2013; Tütken and Vennemann, 2009; Domingo et al., 2009, 2012, 2013; Bernor et al., 2011; Zin-Maung-Maung- Thein et al., 2011; Merceron et al., 2013; Rey et al., 2013; Aiglstorfer et al., 2014; Eastham et al., 2016; Nelson and Rook, 2016; Johnson and Geary, 2016). Our isotopic study concentrates on a single taxon, the equid, Hippotherium intrans, in order to avoid ecological or physiological differences that may exist among taxa, and that could influence variations in the stable isotope compositions of hard tissues. The three-toed equid Hippotherium became a common component of Eurasian faunas after dispersing from North America during the early Late Miocene (Bernor et al., 1996), and a high diversity of Hippotherium species has been recorded in the Pannonian region (Hungary, Austria, Slovakia) including H. primigenium, H. microdon, and H. intrans (Bernor et al., 1993, 2003; Scott et al., 2005). Equids offer several advantages for stable isotope studies of paleoclimate compared with other large-bodied ungulates. Because equids are obligate drinkers with lower metabolic rates their enamel δ18O values are most likely to accurately reflect drinking water δ18O values that are close to those of local environmental waters (Delgado Huertas, et al., 1995; Kohn, 1996; Hoppe et al., 2004b; Levin et al., 2006). The broad temporal and geographic distribution of equids allows for the analysis of regional climatic change over long time periods (Nelson, 2005; van Dam and Reichart, 2009; Rey et al., 2013; Zanazzi et al., 2015; Johnson and Geary, 2016). Finally, because equid enamel has been used frequently in stable isotope studies there is an abundant comparative dataset (e.g. Bryant et al., 1994; 1996; Wang et al., 1994; Delgado-Huertas et al., 1995; Kohn et al., 1998; Sharp and Cerling, 1998; Feranec and MacFadden, 2000; Kohn et al., 2002; Passey et al., 2002; Hoppe et al., 2004b; Nelson, 2005; van Dam and Reichart, 2009; Bernor et al., 2011; Tütken et al., 2013; Rey et al., 2013; Zanazzi et al., 2015; Johnson and Geary, 2016). Here we analyze the stable isotope compositions of tooth enamel carbonate from H. intrans at R. II in order to: (1) estimate mean annual precipitation (MAP) and mean annual temperature (MAT), (2) examine intra-

98 annual (seasonal) variation in climate, and (3) provide the paleoclimatic context in which Rudapithecus and Anapithecus co-occurred.

Figure 4.1 Geographic location of the study area. Insert A shows the position of the

Pannonian Basin within Western Eurasia. Insert B shows the Pannonian Basin with the estimated maximum extension of Lake Pannon at ca. 10 Ma indicated by white shading.

White diamond marks the position of Rudabánya on the paleoshoreline. White circles indicate the positions of Bucharest, Budapest, Vienna, and Zagreb for reference (modified from Rögl, 1998; Magyar et al., 1999; Popov et al., 2004).

2 Background 2.1 Geology and Paleontology

There are several early Late Miocene vertebrate localities within the Rudabánya complex; the current study analyzes equid enamel from the R. II locality, where the majority of primate material has been recovered. Rudabánya is situated within the Pannonian Basin, on the western flank of the northern Carpathian Mountains, in northeastern Hungary (N48°22'48.13", E20°37'43.57") (Figure 4.1). The depositional sequence at R. II is comprised of cyclic layers of clay, mud, and lignite totaling 8–12 meters. These fossiliferous deposits accumulated near the shoreline of Lake Pannon, a relict of the Paratethys Sea, which formed at approximately 11.6 Ma (Kázmér, 1990, Rögl, 1998; Magyar et al., 1999; Popov et al., 2004). The lake reached its maximum extent (c. 290,000 km2) between 10.5 – 10 Ma, during a period of by high precipitation and humidity (Magyar et al., 1999; Harzhauser and Mandic, 2004; Harzhauser et al., 2007, 2008; Kern et al., 2012; Utescher et al., 2017). At this time coastal environments were characterized by extensive marshes grading into forested-wetlands, and predominantly deciduous moist forests (Kretzoi et al., 1976; Harzhauser et al., 2007; Halby and Erdei, 2013; Utescher et al., 2017).

R. II represents one of the most diverse vertebrate paleontological localities from the Eurasian early Late Miocene, preserving an abundance of forest-adapted fauna including 69 species of mammals. The evolutionary stage of the fauna suggests a biochronological age near to the top of the MN9 land mammal zone (10 – 9.8 Ma; Kordos, 1991; Bernor et al., 2003, 2004; Andrews and Cameron, 2010; Casanovas-Vilar et al., 2011). Meso- and microwear analysis of the Rudabánya ungulates indicates a predominantly closed-canopy forest environment (Merceron et al., 2007). Stable isotope analysis of 10 genera of medium to large-bodied ungulates from R. II revealed a gradient of more open to closed canopy forest habitats without sharp ecotonal 13 boundaries (Eastham et al., 2016). For comparison, the mean δ CE value of plants consumed by the R. II ungulates (−28.3‰) is similar to that measured for modern deciduous humid subtropical vegetation (−28.4‰) in the Okefenokee Swamp Forest, southern Georgia, USA (DeLucia and Schlesinger, 1995; Eastham et al., 2016).

100

Depositionally, the equid teeth analyzed here originate from the black mud and gray marl layers at R. II. Kordos and Begun (2002) observed a lack of faunistic difference between theses depositional layers and suggest that they sample overlapping communities. Stable isotope analysis of fauna from the black mud and gray marl layers showed no significant difference in values indicating little, if any, change in environmental conditions (Eastham et al., 2011). Thus, despite sampling two distinct sedimentary horizons, we interpret the equid stable isotope values as being derived from one faunal community.

2.2 Carbon Isotope Values in Mammalian Enamel

Miocene ecosystems in Europe were dominated by vegetation utilizing the C3 photosynthetic pathway (Calvin cycle), with little to no influence from plants using other photosynthetic pathways, such as C4 or CAM (Bocherens et al., 1994b; Hernández-Fernández et al., 2006; Merceron et al., 2006, 2013; Tütken et al., 2006; 2013; Domingo et al., 2009; 2012; Tütken and Vennemann, 2009; van Dam and Reichart, 2009; Rey et al., 2013; Aiglstorfer et al., 2014; Eastham et al., 2016; Johnson and Geary, 2016; Nelson and Rook, 2016). Thus, we 13 assume that the primary influence on the enamel carbon isotope ratios (δ CE) of the R. II equids 13 was from C3 plants. Modern C3 plants have a global mean δ C value of −28.5‰ and range 13 between −22‰ and −36‰ (Kohn, 2010). The range of δ C values exhibited by C3 vegetation is the result of variation in environmental factors such as solar radiation, water and nutrient availability, and temperature (Farquhar et al., 1982; Ehleringer et al., 1987; O’Leary, 1988; van der Merwe and Medina, 1991; Ehleringer and Monson, 1993; Koch, 1998; Heaton, 1999;

Diefendorf et al., 2010; Kohn, 2010). Under water stress conditions C3 plants close their stomata and show less discrimination against δ13C. Typically, higher δ13C values are associated with more open and arid environments (Farquhar et al., 1989). In contrast, lower δ13C values are 13 found in humid closed canopy forests due to the recycling of C-depleted CO2 and low solar irradiance (van der Merwe and Medina 1991; Cerling et al., 1999; Heaton, 1999; Cerling et al., 2004).

The carbon isotope values of herbivorous mammalian enamel reflect the composition of ingested plants, with a consistent enrichment factor due to metabolic processes and equilibrium constraints. The enrichment factor for ungulate enamel ranges from 12‰ to 14‰ due to differences in digestive physiology and the amount of methane produced (ruminant vs. non-

101 ruminant; Lee-Thorp and van der Merwe, 1987; Lee-Thorp et al., 1989; Cerling and Harris, 1999; Passey et al., 2005). Here we correct for the enrichment between diet and enamel using a value of 14.1 ± 0.5‰, which is the average value calculated for medium to large-bodied 13 ungulates (Cerling and Harris, 1999). Both the CO2 concentration and the δ CCO2 value of the atmosphere have fluctuated through time, affecting the δ13C value of plants and ultimately mammalian bioapatite (Friedli et al., 1986; Marino et al., 1992). Tipple et al. (2010) 13 reconstructed variation in δ CCO2 values for the Cenozoic using isotopic data from benthic 13 foraminifera. Following these measurements, a δ CCO2 value of –6‰ can be estimated for the Miocene (2‰ higher than the modern atmosphere) (Tipple et al., 2010). This means that 13 Miocene mammals feeding on C3 plant resources are expected to have δ CE values ranging between −22‰ and −6‰, with –22‰ to –13‰ for those feeding under a relatively closed canopy, −13‰ to −8‰ in mesic woodland environments, and <–8‰ for more open/arid C3 vegetation (Cerling and Harris 1999; Bocherens, 2003).

2.3 Oxygen Isotope Values in Mammalian Enamel

The oxygen isotope compositions of mammalian enamel depend on the δ18O composition 18 of drinking water (δ OH2O), the fractionation of isotopes between enamel and body water, and the metabolic rate of the animal (Longinelli, 1984; Luz et al., 1984); Luz and Kolodny, 1985; Koch et al., 1989; Bryant and Froelich, 1995; Kohn, 1996; Kohn et al., 1996, 1998). Herbivorous mammals obtain water either through drinking or the plants they consume. The isotopic composition of precipitation primarily depends on the air temperature where the evapo- condensation processes occur (Dansgaard, 1964; Rozanski et al., 1993; Kohn and Welker, 2005). At mid and high latitudes, where precipitation and humidity are relatively low, MAT has the greatest effect on the δ18O values (Dansgaard, 1964). However, this is not the case at lower latitudes and regions under monsoon effects, where the amount or rain-out effect dominates (Dansgaard, 1964; Rozanski et al., 1993). The amount effect may also influence δ18O values at

102 higher latitudes during heavy rainfall events (Celle-Jeanton et al., 2001). However, while mammal drinking water may derive from precipitation, drinking water is not necessarily the same as precipitation.

Interpreting δ18O values of mammalian enamel is complicated by the complex nature of oxygen flux in within the body. Taxa that drink frequently generally reflect lower enamel 18 18 oxygen isotope ratios (δ OE), whereas drought-tolerant animals usually have higher δ OE ratios because they obtain proportionally more water from 18O-enriched food sources such as leaves, fruits, or seeds (Kohn, 1996; Levin et al., 2006). In terrestrial settings, obligate drinking mammals obtain their water from different reservoirs including lakes, ponds, streams, and rivers. Each of these reservoirs can have different δ18O values relative to precipitation, due to variation in evaporative effects and variable mixing of temporally different precipitation (Montanari et al., 2013). In long-term lakes, such as Lake Pannon, these processes can lead to 18O enrichment (Talbot, 1990). Conversely, rivers and streams originating at higher elevations may have lower δ18O values than local precipitation (Dutton et al., 2005). Large obligate-drinking mammals with low metabolisms are suggested as the most likely to accurately reflect ingested δ18O values that are closer to those of local environmental waters (Longinelli, 1984; Luz et al., 1984; Bryant and Froelich, 1995; Hoppe, 2004b). The fossil equid H. intrans was large-bodied (242 kg; Bernor et al., 2003) and based on modern analogues is predicted to have a lower metabolism and be an obligate drinker. Equids employ hindgut fermentation, which is a relatively primitive adaptation that confers a strong water dependence (Kohn and Fremd, 2007).

2.4 Intra-tooth Isotopic Variation and Seasonality

Despite methodological issues associated with the complexity of enamel deposition and mineralization (Balasse, 2002, 2003; Passey and Cerling, 2002; Hoppe et al., 2004a; Passey et al., 2005; Zazzo et al., 2005, 2010, 2012; Bendrey et al., 2015) serial isotope analysis of fossil tooth enamel has been extensively used in the investigation of paleoclimate (MacFadden and Cerling, 1994; Fricke and O’Neil, 1996; Fricke et al., 1998; Zazzo et al., 2002; Balasse et al., 2003; MacFadden and Higgins, 2004; Nelson, 2005; Feranec et al., 2009; van Dam and Reichart, 2009; Zin-Maung-Thein et al, 2011; Merceron et al., 2013; Zanazzi et al., 2015). Because enamel forms by accretion and does not remodel once fully mineralized, the sequence of isotopic variation preserved along the length of the tooth crown provides a record of individual history

103 during tooth growth. Molars and premolars of the modern horse Equus caballus form during the first 4.5 years of life, with individual teeth taking between approximately 1.5 and 2.8 years to mineralize (Hoppe et al., 2004a). By collecting serial enamel samples perpendicular to the tooth’s growth axis it is possible to examine chronological variation in oxygen and carbon stable isotope values, which provides insight into seasonal variations in climate and diet. A detailed understanding of the duration and rate of tooth growth is essential for interpreting serially sampled isotope data (Balasse, 2002; Hoppe et al., 2004a; Zazzo et al., 2010, 2012; Balasse et al., 2012; Bendrey et al., 2015). The majority of isotopic studies utilizing equid enamel have assumed a constant rate of growth; however, the results of recent study by Bendrey et al. (2015) suggest that enamel apposition and maturation advances at an exponentially decreasing rate. These findings have significant implications for the interpretation of seasonal events, as the spacing of maxima and minima would appear closer together at the roots of the teeth (Bendrey et al., 2014).

Mammals drinking environmental water from the same general area and whose teeth 18 grow over the course of a year will typically display a sinusoidal curve in δ OE values where a complete cycle represents one year (Fricke and O’Neil, 1996; Passey and Cerling, 2002; Balasse et al., 2003; Nelson, 2005; Zazzo et al., 2005; Feranec, 2008; Feranec et al., 2009). Although 18 18 variation in δ OE values can be used to infer seasonal variability in the δ O of environmental water, the signal is both dampened and delayed (Kohn and Cerling, 2002; Kohn, 2004). Damping (referred to here as d) is defined as the difference in amplitude of the environmental signal and recorded signal, divided by the amplitude of the environmental signal, and ranges between 0 and 100% (Kohn, 2004). Several factors influence damping including internal time- averaging related oxygen fixation within the body of the animal (Kohn and Cerling, 2002), the residence time of oxygen in the body (Kohn et al., 1998, 2002, Kohn and Cerling 2002), the complexity and timing of enamel mineralization (Passey and Cerling, 2002; Kohn, 2004), and time-averaging associated with the method of sample collection (Hoppe et al., 2004b). In order 18 to estimate seasonal variation in drinking water δ OH2O the observed range must be divided by (1-d). Kohn (2004) estimated a damping factor of 40-50% for equids during amelogenesis, with an additional 10% damping related to the residence time of δ18O in the body of the animal. To 18 examine seasonal variation in δ OH2O we apply a conservative damping factor of 50% (0.5)

104

following Kohn (2004). For comparison, we also apply a damping factor of 0.6, which was modeled for Late Neogene equids from the Iberian Peninsula (van Dam and Reichart, 2009).

18 18 18 18 13 18 δ OCO3 δ OPO4 18 δ OH2O δ OH2O δ C δ OCO3 δ OPO4 MAT MAT Specimen Tooth (V- (V- (V- (V- (V- (V- Corr. h (°C) Eq (°C) No. type SMOW) SMOW) SMOW) SMOW) PDB) PDB) (+1.4‰) 6. Eq 6. Eq 2. Eq 3. Eq 4. Eq 5. RUD782 M3 –12.9 –7.2 23.4 14.4 15.8 –8.8 11 –7.6 14 RUD729 M2 –13.2 –7 23.6 14.6 16 –8.5 12 –7.3 15 RUD1082 m3 –11 –4.2 26.5 17.5 18.9 –4.8 22 –3.6 25 RUD1014 m3 –12.9 –8 22.6 13.6 15 –9.8 8 –8.6 11 RUD804 M2 –12.7 –8 22.6 13.6 15 –9.8 8 –8.6 11 RUD794 m2 –12.9 –8.3 22.3 13.4 14.8 –10.2 7 –9 10 RUD139 M3 –12.9 –8 22.6 13.6 15 –9.8 8 –8.6 11 RUD429 m3 –13 –7.4 23.2 14.2 15.6 –9 10 –7.8 13 RUD628 m2 –13 –7.2 23.4 14.4 15.8 –8.8 11 –7.6 14 RUD721 M3 –13 –7.5 23.1 14.1 15.5 –9.2 10 –8 13 RUD728 M3 –13 –8.2 22.4 13.5 14.9 –10.1 7 –8.9 11 RUD762 M2 –12 –5.5 25.2 16.2 17.6 –6.5 17 –5.3 21 Mean –12.7 –7.2 23.4 14.4 15.8 –8.8 11 –7.6 14

Table 4.1. Bulk oxygen and carbon compositions of Hippotherium intrans enamel carbonate using V-PDB standard scale. Oxygen isotope values converted to V-SMOW scale using equation 2 (Friedman and O’Neil, 1977). Carbonate oxygen isotope values converted to phosphate equivalent values using equation 3 (Iacumin et al., 1996). Correction for the difference in relative humidity (h) between the early Late Miocene and present following Tü tken et al. (2014). Estimated drinking water oxygen isotope composition calculated using equation 4 – the equid specific equation from Tü tken et al. (2006). Estimated drinking water oxygen isotope composition calculated using equation 5 – the general herbivore equation from Kohn (1996). Estimated mean annual temperature (MAT) calculated using equation 6 from Domingo et al. (2013).

3 Materials and Methods

All of the equid teeth sampled in the current study were recovered from the R. II locality within the Rudabánya complex. A total of 12 bulk and 28 serial enamel samples were collected (Table 4.1). We preferentially sampled third molars (M3) and second molars (M2), which have

105 the longest mineralization time (~34 months for M3; ~30 months for M2) and continue mineralizing after the weaning period (Hoppe et al., 2004a). Tooth surfaces were cleaned mechanically prior to sampling. Powdered enamel samples (~ 5–10 mg) were removed using a low-speed FOREDOMTM drill and carbide dental burs. 2-3 mm wide bulk samples were taken along the non-occlusal surface parallel to the growth axis across the entire length of the tooth. Powdered enamel samples were chemically pretreated prior to isotopic analysis using hydrogen peroxide (30%, H2O2) to remove organics and weak acetic acid (0.1 N, CH3CO2H) to remove secondary carbonates. Samples were centrifuged at a high speed and rinsed in distilled water to neutral pH before proceeding with the next solution. This sampling procedure generally follows the methods of MacFadden and Cerling (1996) and Koch et al. (1997). Approximately 1-2 mg of treated bulk enamel samples were used for carbon and oxygen analyses. This was performed using a Thermo-Finnigan MAT 253 gas source isotope ratio mass spectrometer via a Finnigan Gas Bench at the Stable Isotope Laboratory of the University of Toronto (Canada). Three equid teeth were serially sampled to examine intra-tooth variation in carbon and oxygen isotope values. Sub-samples were collected perpendicularly to the lateral side of the crown, with an average height of ~1 mm, a maximal depth of ~ 1 mm, and a length of ~5-8 mm. The number of sub- samples per tooth varied between 8 and 11. Since the isotopic amplitude is strongly time- averaged, no effort was taken to standardize the number of sub-samples per tooth. Approximately 1 mg of treated serial enamel samples were used for carbon and oxygen analyses. This was performed using a Thermo-Fisher DeltaVPlus 1 gas source isotope ratio mass spectrometer via a Finnigan Gas Bench at the Stable Isotope Laboratory of Memorial University (Canada). The measured carbon and oxygen isotope compositions were calibrated using the NBS-19 standard then to V-PDB (PeeDee Belemnite) following the Vienna (V-) convention. Two replicate samples were analyzed in duplicate, with a precision of ±0.2‰.

4 Results 4.1 Bulk Carbon Isotope Values and Mean Annual Precipitation (MAP)

13 Bulk δ CE values range between −13.2‰ and −11.0‰, and have a mean value of −12.7‰ (Table 4.1). After accounting for dietary (14.1±0.5‰) and atmospheric enrichment

106

(1.5‰), the δ13C values of plants eaten by H. intrans range between −28.8‰ and −26.6‰, a 13 range typical of C3 plants. In C3 ecosystems, the δ C values of mammalian bone and enamel are correlated with the amount of precipitation and plant productivity, as well as the ratio between potential evapotranspiration and MAP (Kohn and Law, 2006). Kohn (2010) showed that MAP 13 correlated to plant δ C values in modern C3 ecosystems, and that by correcting for isotopic discrimination, δ13C values from ungulate collagen or enamel could be used to back calculate the average plant values. Kohn and McKay (2012) and Zanazzi et al. (2015) provide an equation to calculate MAP from tooth enamel:

13 MAP=10^[δ Cmeq+10.29−0.000194×elev+0.0124×Abs(lat)/−5.61] −300 [1]

13 Where, elev, is the elevation of the site, Abs(lat), is the absolute latitude for the site, and δ Cmeq is the stable carbon isotope value from tooth enamel corrected to modern equivalent values, which includes correcting for the diet to enamel enrichment, as well as the difference in the δ13C of the atmosphere at the time of isotope incorporation relative to modern (–8.0‰). Rudabánya lies at 237 m altitude and is located at 48.3833 N latitude. For the MAP calculation we utilize 13 the average δ CE value (−12.7‰) of the equid as other researchers have done (e.g. Rey et al., 2013; Zanazzi et al., 2015). To analyze the range of MAP due to the error associated with diet to enamel enrichment, we also calculate and report MAP using an enrichment value of 13.6‰ and 14.6‰. Using a diet to enamel enrichment of 14.1‰ we calculate a MAP of 1333 mm/yr. When we calculate MAP using the error associated with diet to enamel enrichment, the values range between 1030 – 1705 mm/yr.

4.2 Bulk Oxygen Isotope Values and Mean Annual Temperature (MAT)

18 Bulk δ OE values range between −8.3‰ and −4.2‰, and have a mean value of −7.2‰ 18 (Table 4.1). Because δ OE values are directly related to the oxygen isotope composition of body 18 18 water, it is possible to calculate the value of drinking water δ O (δ OH2O) at the time of tooth 18 18 formation. In order to calculate δ OH2O, carbonate oxygen isotope values (δ OCO3) were first converted from V-PDB to the V-SMOW standard scale (Friedman and O’Neil, 1977):

107

18 18 δ OCO3(V-SMOW) = 1.03086* δ OCO3(V-PDB) + 30.86 [2]

18 and then to phosphate oxygen isotope (δ OPO4) – equivalent values (Iacumin et al., 1996):

18 18 δ OPO4(V-SMOW) = δ OCO3(V-SMOW)*0.98 – 8.5 [3]

18 We use the equid specific equation from Tü tken et al. (2006) to calculate δ OH2O from enamel 18 δ OPO4 values. This equation uses the isotopic scale for recent horses compiled by Delgado 18 Huertas et al. (1995), which relates δ OPO4 from bone and tooth enamel to local environmental waters from different locations around the world. Following Tü tken et al. (2014) we corrected for the difference in relative humidity between the early Late Miocene and today. H. intrans lived in a humid subtropical forest environment at Rudabánya (Kretzoi, 1976; Kordos and Begun, 2002; Erdei et al., 2007; Andrews and Cameron, 2010; Hably and Erdei, 2013; Utescher et al., 2017) where leaf water may not have been strongly 18O-enriched due to lower levels of evapotranspiration (Yakir, 1997). Kohn and Fremd (2007) found that humidity was only of minor importance in modern equids and can be assumed with 0.1‰ per percent relative humidity, as a minimum assumption. The modern horse specimens used in the equid-specific scale (Delgado Huertas et al., 1995) were collected from localities that cluster around 60% relative humidity, whereas the relative humidity of early Late Miocene Rudabánya ranged between 70 and 78% (pers. comm. T. Utescher, 2016). We use an average value of 74%, which was calculated from paleobotanicals using the Coexistence Approach (Mosbrugger and Utescher, 1997; Utescher et al., 2014) to adjust for the difference in relative humidity. To correct for the 18 14% difference an adjustment of 1.4‰ was added to the δ OPO4 values of H. intrans (Table 4.1).

18 18 δ OH2O(V-SMOW) = (δ OPO4(V-SMOW) – 22.6)/0.77 [4]

We also use the general herbivore equation (Kohn et al., 1996) for comparison:

18 18 δ OH2O(V-SMOW) = (δ OPO4(V-SMOW) – 26.8 + 8.9h)/0.76 [5] where h is relative humidity from 0 to 1. Here we also apply a value of 74% (0.74) relative humidity as estimated from paleobotanicals (pers. comm. T. Utescher, 2016).

Finally, we use a regression equation from Domingo et al. (2013) to estimate MAT from 18 δ OH2O (Table 4.1). This regression uses the meteorological data of Rozanski et al. (1993),

108 which was collected from meteorological stations worldwide. This equation was selected because it represents a global average climate for mid-latitudes, rather than polar extremes where 18 MAT is more sensitive to changes in δ OH2O:

18 2 MAT (°C) = (δ OH2O(V-SMOW) + 12.68) / 0.36) (R = 0.72) [6]

18 A range of MAT estimates were calculated using the δ OH2O values derived from equations [4] and [5] (Table 4.1). A MAT ranging between 8 and 22°C, with a mean of 11°C, 18 was calculated using δ OH2O values derived from the equid specific equation [4] (Tü tken et al., 18 2006). Using δ OH2O values derived from the general herbivore equation [5] (Kohn et al., 1996) we calculate a MAT ranging between 10 and 25°C, with a mean of 14°C.

109

13 18 Sample δ CCO3 δ OCO3 Specimen No. position (mm) (V-PDB) (V-PDB) RUD728 2 –13.5 –7.9 RUD728 6 –13 –7.2 RUD728 10 –13.6 –7.6 RUD728 14 –13.7 –8.5 RUD728 20 –13.9 –8.8

RUD728 26 –14 –8.6 RUD728 30 –13.4 –8.3 RUD728 34 –13 –8.2 RUD782 2 –12.7 –8 RUD782 8 –12.9 –8.3 RUD782 12 –12.9 –8

RUD782 18 –13.1 –8.1 RUD782 24 –13 –7.4 RUD782 28 –13 –7.2 RUD782 32 –13 –6.5 RUD782 36 –13.1 –7 RUD782 40 –13.2 –6.9 RUD1014 2 –12.3 –7.7 RUD1014 6 –13.1 –8 RUD1014 10 –12.6 –8.4

RUD1014 14 –12.9 –7.9 RUD1014 18 –12.9 –8.7 RUD1014 22 –13.1 –9.2 RUD1014 26 –13.1 –9.3 RUD1014 30 –12.5 –8.6 RUD1014 34 –12.8 –7.4 RUD1014 38 –12.8 –8 RUD1014 40 –12.3 –8

Table 4.2. Oxygen and carbon isotopic compositions of third molar serial enamel samples from Hippotherium intrans. Sample position measures distance from cervix.

110

-5.0 RUD728 (A) -7.0

-9.0 18 = δ OEnamel (‰, V-PDB) -11.0 13 = δ CEnamel (‰, V-PDB) -13.0

-15.0 0 4 8 12 16 20 24 28 32 36 40

-5.0 RUD782 (B) -7.0

-9.0

-11.0

-13.0

-15.0 0 4 8 12 16 20 24 28 32 36 40 44

-5.0 RUD1014 (C ) -7.0

-9.0

-11.0

-13.0

-15.0 0 4 8 12 16 20 24 28 32 36 40 44

Figure 4.2. Intra-tooth variation in enamel oxygen and carbon stable isotope compositions 18 along the third molars of Hippotherium intrans. White circles, δ OE values; black circles, 13 δ CE values. X-axis showing sample distance from cervix (mm).

111

4.3 Intra-tooth Variation in Isotope Values and Seasonality

The three teeth that were sampled serially showed quasi-sinusoidal isotopic variation in 18 δ OE values, C which are indicative of seasonality in temperature, with the lowest values occurring in winter (Figure 4.2). In all three teeth both a summer and winter extreme can be 18 established. Intra-tooth variation in δ OE ranged between 1.6 and 1.9‰ (V-PDB, Table 4.2), 13 with an average of 1.8‰. The largest amplitude (1.9‰) was found in RUD1014. δ CE values 18 generally followed the curves of δ OE values, but showed a much lower degree of variation. 13 Seasonal ranges of δ CE vary between 1 and 0.5‰ (V-PDB, Table 4.2), with an average of 0.8‰. The largest amplitude (1‰) was found in RUD728. In order to estimate seasonal 18 18 variation in drinking water δ OH2O, the observed δ OE (V-PDB) values were first converted to the V-SMOW scale using equation [1], then to phosphate equivalent values using equation [2], 1.4‰ 18 was added to the δ OPO4 values to correct for the difference in relative humidity between the 18 18 early Late Miocene and present, δ OPO4 values were then converted to δ OH2O values using 18 equation [4]. The average range of δ OH2O was then divided by 1-d, with d being the damping factor. As discussed previously, the estimation of this range is greatly impacted by the uncertainties in d. We applied a conservative damping factor of 0.5 following Kohn (2004), and a damping factor of 0.6 following van Dam and Reichart (2009). When we apply a damping 18 factor of 0.5 the average annual range of δ OH2O is 4.5‰. Using a damping factor of 0.6 the 18 average annual range of δ OH2O is 5.5‰.

Mean annual temperature (MAT) Mean annual precipitation (MAP) °C Ref. mm/yr Ref. This study 11 to 14 This study 1030 to 1333 Rodent species richness 14.1 j Small mammal community structure 1200+ b, c Paleobotanicals 15 to 16+ b, d, k Large mammal hypsodonty 1190 to 1400+ f, g, h Recent 10 to 11 a Herpetofaunal community structure 1200+ i Paleobotanicals 897 to 1600+ b, d, c, k Recent 500 to 800 a

Table 4.3 Mean annual temperature (MAT) and mean annual precipitation (MAP) estimates obtained from previous paleoclimatic studies and the results of the current study. a = Spinoni et al., 2015; b = Damuth et al., 2003; c = van Dam 2006; d = Mosbrugger et al., 2005; e = Bruch et al., 2011; f = Fortelius et al., 2002; g = Eronen and Rook, 2004; h = Eronen et al., 2010; i = Böhme et al., 2008; j = Montuire et al., 2006; k = Utescher et al., 2017.

112

5 Discussion 5.1 Climatic Interpretations: Mean Annual Precipitation (MAP)

An estimated mean annual precipitation of 1333 mm/yr was calculated from the average 13 δ CE value of the R. II equids using a diet-enamel enrichment factor of 14.1‰. This value is higher than the current range of MAP in the Pannonian Basin (500 - 800 mm/yr; Spinoni et al., 2015), and falls within the range calculated using other proxies (Table 4.3). Paleobotanical data indicates that rainfall was relatively high and constant in Central Europe from the Eocene up until the Late Miocene (Mosbrugger et al., 2005). Analysis of herpetofauna from this region revealed two episodes of anomalously high precipitation (>1200 mm/yr), occurring between 10.2 – 9.8 Ma and 9 – 8.5 Ma (Böhme et al., 2008). van Dam (2006) reconstructed MAP for Late Miocene Europe using small mammal community structure, with estimates ranging between 600 and 1200 mm/yr. This author found a peak in precipitation (> 1200 mm/yr) in Central Europe at approximately 10 Ma (van Dam, 2006).

When calculating MAP using the error associated with diet-enamel enrichment (13.6‰ and 14.6‰), estimated values range between 1030 and 1705 mm/yr. An estimated MAP of 1030 mm/yr falls within the lower range of estimates derived from other proxies (Table 4.3), however, a MAP of 1705 mm/yr seems unrealistically high. This issue highlights the importance of determining species-specific enrichment values. Passey et al. (2005) showed that inter-species differences in digestive physiology, such as methane production, are a major determinate of diet to enamel enrichment. Equids are monogastric feeders and have been shown to produce less methane than many large-bodied ruminants (Crutzen et al., 1986). Cerling and Harris (1999) found an enrichment value of 13.8‰ for modern horses in Mongolia. It is likely that the enrichment value for H. intrans falls between 13.6‰ and 14.1‰, as opposed to the higher enrichment values that have been reported for domestic ruminants (14.6 ± 0.3‰, Passey et al., 2005). While the lower range of MAP calculated in this study (1030 – 1333 mm/yr) is concordant with other proxies, it should likely be viewed with discretion as the relationship between plant δ13C values and MAP has been shown to be less strong in Europe than on other continents (Diefendorf et al., 2010). Diefendorf et al. (2010) suggest that the lack of strong correlation in Europe may arise from heterogeneity in growing season water availability, or the presence of sites where soil water does not come from local precipitation.

113

5.2 Climatic Interpretations: Mean Annual Temperature (MAT)

Reconstructed mean annual temperature varies considerably based upon the drinking 18 18 water δ OH2O value applied in equation [6] (Domingo et al., 2013). Using the mean δ OH2O value (–8.8‰) derived from equation [4] (Tü tken et al., 2006) we calculate a MAT of 11°C. This value seems unrealistically low given the subtropical character of the Rudabánya fauna (Bernor et al., 2003, 2004) and is inconsistent with estimates derived from other proxies (Table 4.3). Current MAT within the Pannonian Basin is equivalent to this estimate, falling between approximately 10 and 11°C (Spinoni et al., 2015). However, paleobotanical data indicates that MAT was approximately 5°C higher in Central Europe during Late Miocene (Mosbrugger et al., 18 2005). Using the mean δ OH2O value (–7.6‰) derived from equation [5] (Kohn et al., 1996) we calculate a MAT of 14°C. While this estimate is concordant with small mammal data (e.g. Montuire et al., 2006), it falls slightly below the range calculated from paleobotanicals (e.g. Damuth et al., 2003; Mosbrugger et al., 2005; Utescher et al., 2017).

There are two factors that could explain the relatively low MAT estimates calculated in this study. First, drinking from water sources with low δ18O values distinct from local precipitation, such as rivers and streams flowing from higher elevations may effect MAT calculations. With increased elevation, heavier 18O isotopes are preferentially rained out; resulting in 18O depleted rainfall in mountainous regions (Dansgaard, 1964; Poage and Chamberlain, 2001). Given the geographic location of Rudabánya on the western flank of the northern Carpathian Mountains, it is plausible that the equid could have consumed water from rivers and streams originating in the mountains. The estimated composition of drinking water δ18O calculated from the enamel of H. intrans (–8.8‰) is similar to the composition of river water estimated from the shells of early Late Miocene fluvial bivalves (–9 to –11‰) found in the hinterland Lake Pannon (Harzhauser et al., 2007). Molluscs precipitate their aragonitic shells in isotopic equilibrium (Grossman and Ku, 1986) and therefore preserve a record of temperature and the isotopic composition of ambient water. Similarly, low drinking water δ18O values (–9 to –11‰) were recently estimated for Late Miocene Hippotherium from various other localities in the Pannonian region (Johnson and Geary, 2016). Johnson and Geary (2016) interpreted the lower δ18O enamel values of equids from the central Pannonian Basin as indicating a reliance on water originating from higher elevations rather than local precipitation. Higher MAT estimates

114 for Rudabánya would be expected if H. intrans drank from Lake Pannon, as long-term lakes are enriched in 18O (Kelts and Talbot, 1990; Talbot, 1990; Tü tken et al., 2006). The δ18O values of lacustrine molluscs from Lake Pannon reflect higher δ18O values (–3.9 and +0.9‰) during middle Pannonian (Harzhauser et al., 2007), when the R. II deposits likely accumulated. Interestingly, strongly alkaline conditions, with an elevated pH value of 9-10 have been inferred from the δ13C values of the lacustrine molluscs within Lake Pannon (Harzhauser et al., 2007). This suggests that the carbon regime of the Lake Pannon was similar to that of modern long-term alkaline lakes in East Africa, such as Lake Turkana (pH ~ 10) and Lake Tanganyika (pH ~ 9) (Harzhauser et al., 2007). It is known that large-bodied mammals modify their drinking behavior based upon water quality, including alkalinity (Kutliek, 1979; Wolanski et al., 1999). Modern ungulates in Kenya’s Lake Nakuru National Park have been observed drinking from rivers and perennial springs and avoiding drinking out of the alkaline lake (Kutliek, 1979). Thus, the low 18 δ OE values of H. intrans appears to indicate that the equid avoided drinking from Lake Pannon and instead utilized water sources originating in the Carpathian Mountains.

The second factor that could have affected the low MAT estimates is the amount effect. 18 At mid-latitudes with low elevations temperature has the greatest control over the δ O value of 18 precipitation (Dansgaard, 1964). However, the distinct relationship between the δ O value of precipitation and temperature is absent at lower latitudes, due to the relatively minimal differences in latitudinal temperatures, and because of strong convective rains. In monsoonal 18 and tropical regions where relative humidity is high, the δ O value of precipitation primarily correlates with the amount of precipitation (Dansgaard, 1964; Rozanski et al., 1993). The amount effect leads to a higher percentage of 16O in rainwater than would be expected from the 18 global temperature-δ Oprecipitation scale (Rozanski et al., 1993; Fricke and O’Neil, 1999). Celle- Jeanton et al. (2001) showed that the amount effect also impacts higher latitude regions during periods of heavy rainfall. Rudabánya is situated at a latitude of approximately 48°N and was characterized by a constantly humid subtropical climate during the early Late Miocene (Kretzoi, 1976; Erdei et al., 2007; Hably and Erdei, 2013; Quan et al., 2014; Utescher et al., 2017). The amount effect, particularly during peak periods of precipitation (Damuth et al., 2003; Harzhauser 18 et al., 2007; Kern et al., 2012; Utescher et al., 2017), may have also influenced the low δ OE values of H. intrans from R. II.

115

5.3 Climatic Interpretations: Seasonality

18 13 Serially sampled δ OE and δ CE values are plotted in Figure 4.2, versus the position the sample was collected from along the tooth crown. All three of the serially-sampled teeth show 18 quasi-sinusoidal curves in δ OE values indicative of enamel growth during different seasons. While limited by sample size, the results show seasonal variation in temperature. However, 18 13 mean amplitudes of 1.8‰ for δ OE and 0.8‰ for δ CE indicate that seasonal changes in climate were not strongly pronounced. This interpretation is concordant with those based on other proxies (e.g. Damuth et al., 2003; Hably and Erdei, 2013; Utescher et al., 2017), which characterize the climatic regime at Rudabánya as constantly humid with warmer and wetter summers and relatively mild winters. Tü tken and Vennemann (2009) found an equivalent amplitude of δ18O variation (1.8‰) in the serially sampled tusk of a Middle Miocene gomphothere from Sandelzhausen, Germany. Based on their isotopic analysis of the Sandelzhausen fauna, these authors interpreted a warm and humid subtropical climate (MAT = 13 19°C) with relatively mild seasonality. The low mean amplitude of δ CE measured in the R. II equids is not unexpected, as the δ13C values of plants using a particular photosynthetic pathway at a given locality do not show large total variation (O’Leary, 1988; Garten and Tayler, 1992; Heaton, 1999; Codron et al., 2005). Intra-population variation in the δ13C values of plants due to seasonal changes is usually less than 1‰ (O’Leary, 1988; Garten and Tayler, 1992; Heaton, 18 1999; Codron et al., 2005). The mean estimated annual drinking water δ OH2O range on the basis of the observed tooth profiles is 4.5‰ using d = 0.5, and 5.5‰ using d = 0.6. Both of these values are significantly lower than the present day ranges of 7.5‰ and 7.2‰ recorded at nearby modern reference stations in Mochovce, Slovakia and Vienna, Austria, respectively (IAEA). At these modern reference stations the associated annual temperatures fluctuate by approximately 20°C, from 0°C in January to 20+°C in July (IAEA). Given the complex issues associated with estimating d, the potential influence of drinking water source (lake vs. rivers and streams flowing from the mountains), and the amount effect, we do not directly estimate seasonal variation in air 18 temperature at R. II. However, we do compare the amplitude of δ OE variation and the 18 estimated annual range of drinking water δ OH2O calculated from the R. II equids with those reported for other Late Miocene primate localities in Western Eurasia.

116

18 The mean δ OE amplitude of the R. II equids (1.8‰) is slightly lower than that (2.1‰) reported for early Late Miocene equids in Spain (van Dam and Reichart, 2009). van Dam and 18 Reichart (2009) estimated a 5.6‰ annual range of δ OH2O from serially sampled equid enamel from the Calatayud-Teruel Basin. This estimated range is very close to the modern range (5.4‰) of δ18O recorded in precipitation from Valencia, Spain, where the corresponding annual air temperature varies by 14°C, from 26°C in the summer to 12°C in the winter (IAEA). It is important to note, however, that van Dam and Reichart did not sample equids from the Vallès- Penedès Basin in northeastern Spain, where the majority of the hominoid and pliopithecoid material has been recovered. Paleoenvironmental data indicate that the Vallès-Penedès Basin was wetter, more humid, and more densely forested than the Calatayud-Teruel Basin during the early Vallesian (Moyà-Solà et al., 1990; Agustí et al., 2003; Casanova-Villar and Agusti, 2007; Marmi et al., 2012). Like Rudapithecus, the Spanish hominoids Hispanopithecus laietanus and H. crusafonti, were large-bodied, suspensory frugivores, which would have been dependent on continuous access to fruit resources (Begun, 1992; Ungar and Kay, 1995; Ungar, 1996; Moyà- Solà and Köhler, 1996; Almécija et al., 2007; Alba et al., 2010ab; Marmi et al., 2012; DeMiguel et al., 2014). The occlusal morphology and microwear of the pliopithecoids Pliopithecus canmatensis and Barberapithecus huerzeleri indicate a frugivorous diet with some component of sclerocarpic feeding (DeMiguel et al., 2013). The extinction of hominoids and pliopithecoids in Western Europe has been attributed the progressive loss of humid forest habitats and increase in deciduous tree species during the late Vallesian (Agustí et al., 2003; Alba, 2012; Marmi et al., 2012; DeMiguel et al., 2013, 2014).

In the Eastern Mediterranean, a more strongly seasonal climatic regime has been 18 interpreted from the serial δ OE values of fossil bovids (Merceron et al., 2013). Merceron et al. 18 (2013) report δ OE amplitudes ranging between 6–10‰ in bovids from the Axios Valley in northern Greece. An estimated annual range of temperature between 5 and 20+°C was 18 calculated from serial δ OE values, which is similar to the modern range of temperature (7– 27°C) recorded in Thessaloniki, northern Greece (IAEA). These results indicate that the terrestrial, hard-object feeding hominoid Ouranopithecus (Bonis and Koufos 1993; 1997; Begun and Güleç, 1998; Merceron et al., 2005; Begun 2007; DeMiguel et al., 2014) endured colder winters than any modern great ape, with the exception of mountain gorillas (Rowe, 1996; Merceron et al., 2013). The extinction of Ouranopithecus and spread of colobine cercopithecoids

117 around Vallesian/Turolian boundary (~8.7 Ma) was likely unrelated to climate change, but instead occurred in correlation with an increase in bushy sclerophyllous vegetation (Merceron et al., 2010; 2013; Rey et al., 2013). However, the more recent discovery of Ouranopithecus-like apes in association with early Turolian mammals in Turkey (Guleç et al., 2007), Bulgaria (Spassov et al., 2012), and Iran (Suwa et al., 2016) suggest a less abrupt extinction for hominoids in this region.

18 Farther east, in the Siwaliks of northern Pakistan, δ OE amplitudes of 2–3‰ have been measured in Late Miocene equids (Nelson, 2005). Nelson (2005) interpreted a monsoonal climate for the Siwaliks during this period comparable to that of present-day southern China. Under this type of climatic regime precipitation instead of temperature controls δ18O variation and the dry season can last between five and six months (Nelson, 2005). These findings indicate that the hominoid Sivapithecus, a large-bodied, arboreal frugivore, lived under a seasonal climatic regime with dry periods lasting longer than the maximum of 4 months that most extant great apes experience (McGrew et al., 1981; Goodall, 1986; Wrangham et al., 1993; Knott, 1998; Nelson, 2005). Increasing forest fragmentation and a decrease in mean annual precipitation are suggested to have influenced the extinction of Sivapithecus during the Late Miocene (Nelson, 2005; 2007).

5.4 Paleoecological Implications for the Rudabánya Primates

The results of this isotopic investigation are concordant with those of earlier studies indicating that the Rudabánya primates experienced an equable humid and wet subtropical climate during the early Late Miocene (Kretzoi, 1976; Kordos and Begun, 2002; Bernor et al., 2003; Damuth et al., 2003; Andrews and Cameron, 2010; Hably and Erdei, 2013; Utescher et al., 2017). A modern environmental analogue for early Late Miocene Rudabánya exists in the humid wetland-forests of the southeastern United States, including the Okefenokee Swamp in southern Georgia. The Okefenokee Swamp has a MAP of 1370 mm/yr and a MAT of 20°C. Seasonality is relatively mild in this environment ranging from warmer (27°C) and wetter (185 mm) summers, to cooler (13°C) and dryer (56 mm) winters (Chen and Gerber, 1990; Henry et al., 1994). Within the Pannonian region, the effects of global Late Miocene cooling (Zachos et al., 2001; Mosbrugger et al., 2005; Bruch et al., 2007; Darby, 2008; Utescher et al., 2009) may have been buffered by the presence of Lake Pannon (Ivanov et al., 2011; Hably and Erdei, 2013;

118

Utescher et al., 2017). This large water body (c. 290,000 km2) would have acted as a source in the regional hydrological cycle and thereby influenced local microclimates and habitats (Utescher et al., 2017). Quan et al. (2014) evaluated seasonal temperature and precipitation data derived from the European paleobotanical record and report humid to subhumid conditions in the Pannonian region throughout the Tortonian (11.6 – 7.2 Ma). A recent paleobotanical study by Utescher et al. (2017) utilizing plant functional types (PFTs) revealed warm and humid conditions within the Pannonian Basin throughout the Late Miocene, with a gradual decrease in MAT (ca. >16°C to ca. >14°C) occurring between 9 and 6.5 Ma. These authors found evidence for particularly humid and wet conditions (MAP > 1200 mm/yr) along the northern margin of the lake between 10.8 and 9.5 Ma (Utescher et al., 2017). The existence of a humid refugium in the northern Pannonian Basin is further evidenced by the presence of a fossil mastixioid flora at R. II (Hably and Erdei, 2013). Modern Mastixia is geographically restricted to the tropical forests of Southeast Asia and some Pacific Islands, where MAT is above 19°C and MAP is approximately 2000 mm/yr (Mai, 1997).

The presence of a humid refugium in the northern Pannonian Basin has important implications for hominoids and pliopithecoids during the early Late Miocene. Eronen and Rook (2004) examined the distribution of European primates throughout the Neogene and found that pliopithecoids and hominoids were only associated with humid habitats, whereas cercopithecoids had more complex patterns of habitat selection. With the progressive shift towards more open and seasonal environments during the Late Miocene, hominoids and cercopithecoids retreated to areas where humid conditions remained, while pliopithecoids became extinct (Eronen and Rook, 2004). A recent study by Sukselainen et al. (2015) evaluated the environmental context of Eurasian localities where pliopithecoids and hominoids co-occur. These authors found that co- occurring localities were restricted to even more humid areas than localities with only one of the two primate groups. Sukselainen et al. (2015) suggest that co-occurrence may have been restricted by the conservative nature of pliopithecoid adaptations to the progressively diminishing range of humid habitats. Our climatic estimates are concordant with those derived from other proxies (e.g. Damuth et al., 2003; Harzhauser et al., 2007; Kern et al., 2012; Hably and Erdei, 2013; Utescher et al., 2017) indicating high-levels of precipitation and humidity in the northern Pannonian region during the early Late Miocene. These findings support the interpretations of both Eronen and Rook (2004) and Sukselainen et al. (2015) identifying

119 humidity as a key environmental factor influencing the distribution of hominoids and pliopithecoids during the Middle and early Late Miocene.

While our results indicate that seasonal changes in climate were not strongly pronounced at Rudabánya, this does not necessarily mean that the primates experienced year-round access to ripe fruit resources. Paleobotanicals reflect the presence of a predominantly deciduous wetland- forest, which included several fruiting taxa such as Celtis and Mastixia (Kretzoi, 1976; Kordos and Begun, 2002; Hably and Erdei, 2013; Hably, 2013; Utescher et al., 2017). In modern humid and moist forests, where soil moisture is not seasonally limiting, seasonal variations in solar irradiance, temperature, and day length influence fruiting and flowering cycles (Morellato et al., 2000; Marques et al., 2004; Zimmerman et al., 2007; Chang-Yang et al., 2013). Chang-Yang et al. (2013) demonstrated that even under relatively aseasonal climatic conditions the Fushan humid subtropical forest in northern Taiwan still exhibited highly predictable seasonal patterns of fruiting and flowering. Rudapithecus has been identified as a dedicated soft fruit frugivore on the basis of dental microwear, shearing crest development, and molar cusp proportions (Ungar, 1996; 2005; Teaford and Ungar, 2000). However, more recent interpretations of incisor shape and curvature by Deane et al. (2013) suggest elevated compressive loads in the incisor region that are consistent with the removal of tough fruit pericarps. A microwear study by DeMiguel et al. (2014) further indicates an affinity for hard fruit feeding in this fossil hominoid. Modern great apes show a general preference for ripe fruit, but are able to cope with fluctuations in ripe fruit abundance by utilizing fallback resources, as demonstrated by the sclerocarpic feeding of orangutans (Vogel et al., 2008; Constantino et al., 2009). The combination of a soft and hard fruit feeding signal could indicate a fallback feeding strategy that allowed Rudapithecus to exploit harder fruiting resources during seasonal periods of ripe fruit shortage.

A more folivorous diet has been suggested for Anapithecus on the basis of molar occlusal morphology and incisor crown curvature (Ginsburg and Mein, 1980; Begun, 1989; Andrews et al., 1996; Köhler et al., 1999; Deane et al., 2013). In contrast, occlusal microwear and intermediate sheering quotients indicate a more frugivorous diet for the pliopithecoid (Ungar and Kay, 1995; Ungar, 1996; Kay and Ungar, 1997; Ungar, 1998; 2005; DeMiguel et al., 2013). Deane et al. (2013) suggest that while the diets of Anapithecus and Rudapithecus may have overlapped considerably, the two primates likely differed in their use of fallback food resources. During seasonal periods of ripe fruit shortage Anapithecus may have consumed a greater

120 proportion of leaves, while Rudapithecus consumed harder fruits. By engaging in different fallback feeding strategies the two primates could have avoided direct competition (Deane et al., 2013).

Adaptations for fallback food use and efficient suspensory arboreality would have allowed Rudapithecus and Anapithecus to endure some degree of seasonal fluctuation in resource availability. However, the progressive loss of humid closed canopy forest habitats during the late Vallesian would have greatly impacted their continuing survival. Following its maximum extension at approximately 10 Ma, Lake Pannon regressed in several phases. By the middle Turolian, the northeastern margin of the lake had contracted significantly from its former extent and progradation almost completely filled the western portion of Hungary (Magyar et al., 1999). As the lake retreated more open and seasonal woodlands gradually replaced humid wetland- forests (Lueger, 1978; Bernor et al., 1996; Daxner-Höck, 2004; Harzhauser et al., 2004; 2007; Merceron et al., 2010; Daxner-Höck et al., 2016). The faunal record reflects the increasing occurrence of open country fauna during the late Vallesian and early Turolian, including the suid Microstonyx, carnivores Indarctos, Adcrocuta, and Paramachaerodus, the bovid, Tragoportax, and the rodents Progonomys and Cricetulodon (Bernor et al., 1996; Harzhauser et al., 2004; Nargolwalla et al., 2006; Vislobokova, 2006, 2007). Nargolwalla et al. (2006) found that the distribution of large mammals, including Hippotherium, tracked the regression of the lake, moving from the northwest to southeast. A recent study by Daxner-Höck et al. (2016) examined small mammal assemblages from 16 Late Miocene localities in the Pannonian region, and found that the majority of early Vallesian taxa inhabited wetland-forest environments. The diversity of small mammals slowly decreased from the late Vallesian (9.7 – 8.7 Ma) towards the early Turolian (8.7 – 7.5 Ma), however, many forest-dwelling species persisted in low individual numbers. Daxner-Höck et al. interpreted these findings as indicating the beginning of an environmental shift towards more open and less humid conditions. The results of a comparative meso- and microwear study sampling European ruminants also indicate the onset of more open environments in Hungary during the early Turolian (Merceron et al., 2010). Johnson and Geary 13 (2016) found higher δ CE values for Hippotherium from the central Pannonian Basin during the late Vallesian and throughout the Turolian, suggesting open to water-stressed conditions. It is 13 interesting to note, however, that these authors report lower δ CE values for early Turolian equids from several localities in the northern Pannonian region, which suggests some persistence

121 of restricted forest habitats. Like other forest-adapted fauna Rudapithecus and Anapithecus would have likely tracked the humid habitats that fringed Lake Pannon as it progressively contracted.

6 Conclusions

Isotopic analysis of fossil equid enamel from the R. II primate locality indicates a humid and wet subtropical climate with relatively mild seasonality during the early Late Miocene. An estimated mean annual precipitation ranging between 1030 and 1333 mm/yr was calculated from 13 the average δ CE value of H. intrans (–12.7‰). A mean annual air temperature of 14°C was 18 calculated using the average drinking water δ OH2O value derived from the general herbivore 18 equation (Kohn, 1996). Using the drinking water δ OH2O value derived from the equid specific equation (Tütken et al., 2006) a MAT of 11°C was calculated. While a MAT of 14°C is slightly lower than estimates derived from paleobotanicals (~16°C), a MAT of 11°C is unrealistically low. Two factors could account for the lower MAT estimates reported in this study: (1) drinking from water sources originating at higher elevations, such as rivers and streams flowing from the Carpathian Mountains, and (2) the amount effect during periods of heavy rainfall. Serial isotope 18 13 analysis revealed an average δ OE amplitude of 1.8‰ and average δ CE amplitude of 0.8‰. These amplitudes are lower than those reported for Late Miocene primate localities in Greece (Merceron et al., 2013) and Pakistan (Nelson, 2005), suggesting that the R. II primates experienced milder seasonal variation in climate than Ouranopithecus or Sivapithecus. The 18 average annual range of drinking water δ OH2O based on the observed intra-tooth profiles is 4.5‰. This value is lower than the modern range of δ18O measured in precipitation at nearby reference stations in Slovakia (7.5‰) and Vienna (7.2‰) (IAEA), indicating that seasonal changes in climate were considerably milder during the early Late Miocene. The climatic regime under which the R. II primates lived was likely most similar to that experienced by early Vallesian hominoids and pliopithecoids in Spain (Agustí et al., 2003; Casanova-Villar and Agusti, 2007; van Dam and Reichart, 2009; Marmi et al., 2012; Alba, 2012).

Our climatic interpretations are concordant with the hypothesis that humidity was a key environmental factor influencing the distribution of hominoids and pliopithecoids during the Middle and Late Miocene (Eronen and Rook, 2004; Sukselainen et al., 2015). The extinction of both primate groups in the Pannonian Basin coincides with the regression of Lake Pannon during

122 the late Vallesian (Magyar, 1999). As the lake contracted the humid wetland-forests that fringed its margins became increasing restricted and fragmented. While adaptations to fallback feeding and efficient suspensory arboreality would have allowed Rudapithecus and Anapithecus to endure some degree of environmental fluctuation, the progressive loss of humid wetland-forest habitats would ultimately lead to their extinction.

Acknowledgements

We thank the Geological and Geophysical Institute of Hungary (MAFI) and the New York State Museum. We greatly thank Dr. László Kordos for his contributions to this research. We thank Dr. Torsten Utescher for his relative humidity calculations from the Rudabánya paleobotanicals. We also thank Jochen Halfar, Dave Bovee, and David Boutilier for their contributions to this research. This research was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) (RGPIN-2016-06761), the National Geographic Society (8801-10), Ontario Graduate Scholarship, Geological Society of America Graduate Research Award, and General Motors Women in Science and Mathematics Award.

References

Agustí, J., Siria, A.S.d., Garcés, M., 2003. Explaining the end of the hominoid experiment in Europe. J. Hum. Evol. 45, 145–153.

Aiglstorfer, M., Bocherens, H., Böhme, M., 2014. Large mammal ecology in the late Middle Miocene locality Gratkorn (Austria). Palaeobiodivers. Palaeoenviron. 94, 189–213.

Alba, D.M., 2012. Fossil apes from the Vallès–Penedès Basin. Evol. Anthropol. 21, 254–269.

Alba, D.M., Almécija, S., Moyà-Solà, S., 2010a. Locomotor inferences in Pierolapithecus and Hispanopithecus: reply to Deane and Begun. J. Hum. Evol. 59, 143–149.

Alba, D.M., Fortuny, J., Moyà-Solà, S., 2010b. Enamel thickness in middle Miocene great apes Anoiapithecus, Pierolapithecus and Dryopithecus. Proc. R. Soc. B. 277, 2237–2245

Alba, D.M., Fortuny, J., DeMiguel, D., 2011. Preliminary paleodietary inferences in two pliopithecid primates from the Vallès–Penedès Basin (NE Iberian Peninsula) based on

123

relative enamel thickness as compared to microwear analyses [Abstract]. Paleontol. Evol. I International Symposium on Paleohistology: 47.

Almécija, S., Alba, D.M., Moyà-Solà, S., 2012. The thumb of Miocene apes: new insights from Castell de Barberà (Catalonia, Spain). Am. J. Phys. Anthropol. 148, 436–450.

Andrews, P., Cameron, D., 2010. Rudabànya: taphonomic analysis of a fossil hominid site from Hungary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 297, 311–329.

Armour-Chelu, M., Andrews, P., Bernor, R.L., 2005. Further observations on the primate community at Rudabánya II (Late Miocene, early Vallesian age), Hungary. J. Hum. Evol. 49, 88–98

Balasse, M., 2002, Reconstructing dietary and environmental history from enamel isotopic analysis: time resolution of intra-tooth sequential sampling, Int. J. Osteoarchaeol. 12, 155– 65.

Balasse, M., 2003. Potential biases in sampling design and interpretation of intra-tooth isotope analysis. Int. J. Osteoarchaeol. 13, 3–10.

Balasse, M., Obein, G., Ughetto-Monfrin, J., Mainland, I., 2012. Investigating seasonality and season of birth in past herds: a reference set of sheep enamel stable oxygen isotope ratios, Archaeometry, 54, 349–68.

Begun, D.R., 1989. A large pliopithecine molar from Germany and some notes on the Pliopithecinae. Folia Primatol. 52, 156 - 166.

124

Begun, D.R., 1992. Phyletic diversity and locomotion in primitive European hominids. Am. J. Phys. Anthropol. 87, 311–340.

Begun, D.R., 2002. The Pliopithecoidea. In: Hartwig, W.C. (Ed.), The Primate Fossil Record. Cambridge University Press, New York, pp. 221–240.

Begun, D.R., 2007. Fossil record of Miocene hominoids. In: Henke, W., Tattersall, I. (Eds.), Handbook of Paleoanthropology. Springer, Heidelberg, pp. 921–977.

Begun, D.R., 2009. Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade. Geodiversitas, 31, 789–816.

Begun, D.R., Güleç, E., 1998. Restoration of the type and palate of Ankarapithecus meteai: taxonomic, phylogenetic, and functional implications. Am. J. Phys. Anthropol. 105, 279– 314.

Begun, D.R., Nargolwalla, M., Kordos, L., 2010. New catarrhine fossils from Rudabánya (Hungary): evidence for sympatric primates in a late Miocene swamp forest. Am. J. Phys. Anthropol 141 (S50), 64.

Bendrey, R., Lepetz, S., Zazzo, A., Balasse, M., Turbat, T., Giscard, P.-H., Vella, D., Zaitseva, G. I., Chugunov, K. V., Ughetto, J., Debue, K., and Vigne, J.-D., 2014. Nomads, horses and mobility: an assessment of geographic origins of Iron Age horses found at Tsengel Khairkhan and Baga Turgen Gol (Mongolian Altai) based on oxygen isotope compositions of tooth enamel. In: Mashkour, M., Beech, M. (Eds.), Proceedings of the 9th ASWA Conference, Al Ain, 2008, Oxbow Books, Oxford.

Bendrey, R. L., Vella, D., Zazzo, A., Balasse, M., Lepetz, S., 2015. Exponentially decreasing tooth growth rate in horse teeth: Implications for isotopic analyses. Archaeometry, 57, 1104-1124.

125

Faunas.Columbia University Press, pp. 449–470.

Bernor R.L., Mittmann H.-W., Kretzoi M., Tobien H., 1993. A preliminary systematic assessment of the Rudabánya hipparions. Mitteilungen der Bayerischen Staatssammlung fur Paläontologie und historische Geologie 33, 1–20.

Bernor, R.L., Armour-Chelu,M., Kaiser, T.M., Scott, R.S., 2003. An evaluation of the late MN9 (Late Miocene, Vallesian age), hipparion assemblage from Rudabánya (Hungary): systematic background, functional anatomy and paleoecology. Coloquios De Paleontología, Volumen Extraordinario, Vol. 1, 35–45.

Bernor, R.L., Kordos, L., Rook, L., Agustí, J., Andrews, P., Armour-Chelu, M., Begun, D.R., de Bonis, L., Cameron, D.W., Damuth, J., Daxner-Höck, G., Fessaha, N., Fortelius, M., Franzen, J.L., Gasparik, M., Gentry, A., Heissig, K., Hernyak, G., Kaiser, T.M., Koufos, G.D., Krolopp, E., Jánossy, D., Llenas, M., Meszáros, L., Mü ller, P., Renne, P.R., Rocek, Z., Sen, S., Scott, R.S., Szindlar, Z., Topál, G.Y., Ungar, P.S., Untescher, T., van Dam, J.A., Werdelin, L., Ziegler, R., 2004. Recent advances on multidisciplinary research at Rudabánya, Late Miocene (MN9), Hungary: a compendium. Paleontogr. Ital. 89, 3–36.

Bocherens, H., 2003. Isotopic biogeochemistry and the palaeoecology of the mammoth steppe fauna. Deinsea, 9, 57–76.

Bocherens, H., Fizet, M., Mariotti, A., 1994a. Diet, physiology and ecology of fossil mammals as inferred by stable carbon and nitrogen isotopes biogeochemistry: implications for Pleistocene bears. Palaeogeogr. Palaeoclimatol. Palaeoecol. 107, 213–225.

Bocherens, H., Fizet, M., Mariotti, A., Bellon, G., Borel, J.-P., 1994b. Les gisements de mammifères du Miocène supérieur de Kemiklitepe, Turquie: 10. Biogéochimie isotopique. Bulletin du Museum d'Histoire Naturelle, Paris, 4e sér. Vol. 16, (C)(1), pp. 211–223

Böhme, M., Ilg, A., Winklhofer, M., 2008. Late Miocene “washhouse” climate in Europe. Earth

126

Planet. Sci. Lett. 275, 393–401 de Bonis, L., Koufos, G., 1993. The face and mandible of Ouranopithecus macedoniensis: description of new specimens and comparisons. J. Hum. Evol. 24, 469–491. de Bonis, L., Koufos, G., 1997. The phylogenetic and functional implications of Ouranopithecus macedoniensis. In: Begun, D.R., Ward, C.V., Rose, M.D. (Eds.), Function, Phylogeny and Fossils: Miocene Hominoid Origins and Adaptations. Plenum Press, New York, pp. 317– 326

Bruch, A.A., Uhl, D., Mosbrugger, V., 2007. Miocene climate in Europe — patterns and evolution. A first synthesis of NECLIME. Palaeogeogr. Palaeoclimatol. Palaeoecol. 253, 1–7.

Bruch, A.A., Utescher, T., Mosbrugger, V., NECLIME members, 2011. Precipitation patterns in the Miocene of Central Europe and the development of continentality. Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, 202–211.

Bryant, J., Luz, B., Froelich, P., 1994. Oxygen isotopic composition of fossil horse tooth phosphate as a record of continental paleoclimate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 107, 303–316.

Bryant, J.D., Froelich, P.N., 1995. A model of oxygen isotope fractionation in body water of large mammals. Geochim. Cosmochim. Acta 39, 4523–4537

Bryant, J.D., Koch, P.L., Froelich, P.N., Showers, W.J., Genna, B.J., 1996. Oxygen isotope partitioning between phosphate and carbonate in mammalian apatite. Geochim. Cosmochim. Acta 60, 5145–5148.

Casanovas-Vilar, I., Agustí, J., 2007. Ecogeographical stability and climate forcing in the late Miocene (Vallesian) rodent record of Spain. Palaeogeogr. Palaeoclimatol. Palaeoecol. 248, 169 - 189.

Casanovas-Vilar, I., Alba, D.M., Garcés, M., Robles, J.M., Moyá-Solá, S., 2011. Updated chronology for the Miocene hominoid radiation in western Eurasia. Proc. Natl. Acad. Sci. 108, 5554–5559.

127

Celle-Jeanton, H., Travi, Y., Blavoux, B., 2001. Isotopic typology of the precipitation in the Western Mediterranean region at three different time scales. Geophys. Res. Lett. 28, 1215– 1218.

Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347–363.

Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., Quade, J., Eisenmann, V., 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature 389, 153–158.

Cerling, T.E., Harris, J.M., Leakey, M.G., 1999. Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia 120, 364–374.

Cerling, T.E., Hart, J.A., Hart, T.B., 2004. Stable isotope ecology in the Ituri forest. Oecologia 138, 5–12.

Chang-Yang, C-H, Lu, C-L, Sun, I-F, Hseih, C-F., 2013. Flowering and fruiting patterns in a subtropical rain forest, Taiwan. Biotropica, 45, 165–174.

Chen, E., Gerber, J.F., 1990. Climate. In: Meyers, R.L., Ewel, J.L. (Eds.), Ecosystems of Florida. University of Central Florida Press, Orlando, Florida, pp. 11–35.

Codron, J., Codron, D., Lee-Thorp, J.A., Sponheimer, M., Bond,W.J., de Ruiter, D., Grant, R., 2005. Taxonomic, anatomical, and spatio-temporal variations in the stable carbon and nitrogen isotopic compositions of plants from an African savanna. J. Arch. Sci. 32, 1757– 1772.

Constantino, P.J., Lucas, P.W., Lee, J.J.-W., Lawn, B.R., 2009. The influence of fallback foods on great ape tooth enamel. Am. J. Phys. Anthropol. 140, 653–660.

Crutzen, P., Aselmann, Seiler, W., 1986. Methane production by domestic animals, wild ruminants, other herbivorous fauna, and humans. Tellus, 388, 271-284

Damuth, J., J.A., v.D., Utescher, T., 2003. Palaeoclimate proxies from biotic proxies. In: Bernor, R.L., Kordos, L., Rook, L. (Eds.), Recent Advances on Multidisciplinary Research at

128

Rudabánya, Late Miocene (MN9), Hungary: A Compendium. Palaeontographica Italica Vol. 89, pp. 1–34.

Dansgaard, W., 1964. Stable isotopes in precipitation. Tellus, 16, 436–468.

Darby, D.A., 2008. Arctic perennial ice cover over the last 14 million years. Paleoceanography 23, PA1S07.

Daxner-Höck, G., 2004. Biber und ein zwerghamster aus Mataschen (unter-pannonium, steirisches becken). Joannea Geol. Paläontol. 5, 19–33.

Daxner-Höck, G., Harzhauser, M., Göhlich, U., 2016. Fossil record and dynamics of the Late Miocene small mammal faunas of the Vienna Basin and adjacent basins. Austria. C.R. Palevol. 15, 855-862.

Deane, A.S., Nargolwalla, M.C., Kordos, L., Begun, D.R., 2013. New evidence for diet and niche partitioning in Rudapithecus and Anapithecus from Rudabánya, Hungary. J. Hum. Evol. 65, 704–714.

Delgado Huertas, A., Iacumin, P., Stenni, B., Sánchez Chillón, B., Longinelli, A., 1995. Oxygen isotope variations of phosphate in mammalian bone and tooth enamel. Geochim. Cosmochim. Acta. 59, 4299–4305.

DeLucia, E.H., Schlesinger, W.H., 1995. Photosynthetic rates and nutrient-use efficiency among evergreen and deciduous shrubs in Okefenokee Swamp. Int. J. Plant Sci. 156, 19–28.

DeMiguel, D., Alba, D., Moyà-Solà, S., 2013. European pliopithecid diets revised in the light of dental microwear in Pliopithecus canmatensis and Barberapithecus huerzeleri. Am. J. Phys. Anthropol. 151, 573–582.

DeMiguel, D., Alba, D., Moyà-Solà, S., 2014. Dietary specializations during the evolution of Western Eurasian hominoids and the extinction of great apes. PLoS One 9 (5), 97442.

Diefendorf, A.F., Mueller, K.E.,Wing, S.L., Koch, P.L., Freeman, K.H., 2010. Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proc. Natl. Acad. Sci. 107, 5738–5743.

129

Domingo, L., Cuevas-González, J., Grimes, S.T., Hernández Fernández, M., López-Martínez, N., 2009. Multiproxy reconstruction of the palaeoclimate and palaeoenvironment of theMiddleMiocene Somosaguas site (Madrid, Spain) using herbivore dental enamel. Palaeogeogr. Palaeoclimatol. Palaeoecol. 272, 53–68.

Domingo, L., Koch, P.L., Grimes, S.T., Morales, J., López-Martínez, N., 2012. Isotopic paleoecology of mammals and the Middle Miocene Cooling event in the Madrid Basin (Spain). Palaeogeogr. Palaeoclimatol. Palaeoecol. 341, 98–113.

Domingo, L., Koch, P.L., Hernández Fernández, M., Fox, D.L., Domingo, M.S., Alberdi, M.T., 2013. Late Neogene and early quaternary paleoenvironmental and paleoclimatic conditions in southwestern Europe: isotopic analyses on mammalian taxa. PLoS One 8(5), E63739.

Dutton, A., Wilkinson, B.H., Welker, J.M., Bowen, G.J., Lohmann, K.C., 2005. Spatial distribution and seasonal variation in 18O/ 16O of modern precipitation and river water across the conterminous USA. Hydrol. Process. 19, 4121–4146.

Eastham, L., Feranec, R.S., Begun, D.R., Kordos, L., 2011. Resource partitioning in Late Miocene Central European mammals: isotopic evidence from the Rudabánya fauna. J. Vertebr. Paleontol. 31 (Suppl. 2), 103.

Ehleringer, J.R., Monson, R.K., 1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Annu. Rev. Ecol. Syst. 24, 411–439.

Ehleringer, J.R., Lin, Z.F., Field, C.B., Sun, G.C., Kuo, C.Y., 1987. Leaf carbon isotope ratios of plants from a subtropical monsoon forest. Oecologia, 72, 109–114.

Erdei, B., Hably, L., Kázmér,M., Utescher, T., Bruch, A., 2007. Neogene flora and vegetation development of the Pannonian domain in relation to palaeoclimate and palaeogeography. Palaeogeogr. Palaeoclimatol. Palaeoecol. 253, 131–156.

130

Eronen, J., Rook, L., 2004. The Mio-Pliocene European primate fossil record: dynamics and habitat tracking. J. Hum. Evol. 47, 323–341.

Eronen, J.T., Puolamäki, K., Liu, L., Lintulaakso, K., Damuth, J., Janis, C., Fortelius, M., 2010. Precipitation and large herbivorous mammal II: application to fossil data. Evol. Ecol. Res. 12, 235–248.

Farquhar, G.D., O'Leary, M.H., Berry, J.A., 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9, 121–137.

Feranec, R.S. 2008. Growth differences in the saber-tooth of three felid species. Palaios 23, 566– 569.

Feranec, R.S., MacFadden, B.J., 2000. Evolution of the grazing niche in Pleistocene mammals from Florida: evidence from stable isotopes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 162, 155–169.

Feranec, R.S., Hadly, E.A., Paytan, A., 2009. Stable isotopes reveal seasonal competition for resources between Late Pleistocene bison (Bison) and horse (Equus) from Rancho La Brea, southern California. Palaeogeogr. Palaeoclimatol. Palaeoecol. 271, 153–160.

Friedman, I., O'Neil, J.R., 1977. Compilation of stable isotope fractionation factors of geochemical interest. U.S. Geological Survey, Reston.

Fricke, H.C., O'Neil, J.R., 1996. Inter- and intra-tooth variation in the oxygen isotope composition of mammalian tooth enamel phosphate: implications for palaeoclimatological and palaeobiological research. Palaeogeogr. Palaeoclimatol. Palaeoecol. 126, 91–99.

18 Fricke, H. C., Clyde, W. C., and O’Neil, J. R., 1998, Intra-tooth variations in δ O(PO4) of mammalian tooth enamel as a record of seasonal variations in continental climate variables, Geochim. Cosmochim. Acta. 62, 1839–50.

Fricke, H.C., O’Neil, J.R., 1999. The correlation between 18O/16O ratios of meteoric water and surface temperature: its use in investigating terrestrial climate change over. Earth Planet. Sci. Lett. 170, 181–196.

131

Friedli, H., Lötscher, H., Oeschger, H., Siegenthaler, U., Stauffer, B., 1986. Ice core record of 13 12 the C/ C ratio of atmospheric CO2 in the past two centuries. Nature, 324, 237–238.

Garten Jr., C.T., Taylor Jr., G.E., 1992. Foliar δ 13C within a temperate deciduous forest: spatial, temporal, and species sources of variation. Oecologia, 90, 1–7.

Ginsburg, L., Mein, P., 1980. Crouzelia rhodanica, nouvelle espèce de Primate catarhinien, et essai sur la position systématique de Pliopithécidae. Bull. Mus. Hist. Nat. Paris. 4, 57–85.

Goodall, J., 1986. The Chimpanzees of Gombe. Belknap Press, Cambridge.

Grossman, E.L., Ku, T.-L., 1986. Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects. Chemical Geology, 59, 59–74.

Guleç, E.S., Sevim, A., Pehlevan, C., Kaya, F., 2007. A new great ape from the Late Miocene of Turkey. Anthropol. Sci. 115, 153–158.

Hably, L., Erdei, B., 2013. A refugium of mastixia in the Late Miocene of eastern central Europe. Rev. Palaeobot. Palynol. 197, 218–225.

Harrison, T., 2002. Late Oligocene to middle Miocene catarrhines from Afro−Arabia. In: Hartwig, W. (Ed.), The Primate Fossil Record. Cambridge University Press, Cambridge, pp. 311–338

Harzhauser, M., Mandic, O., 2004. The muddy bottom of Lake Pannon — a challenge for dreissenid settlement (Late Miocene; bivalvia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 204, 331–352.

Harzhauser, M., Daxner-Höck, G., Piller, W.E., 2004. An integrated stratigraphy of the Pannonian (Late Miocene) in the Vienna Basin. Austrian Journal of Earth Sciences, 95/96, 6–19.

Harzhauser, M., Latal, C., Piller, W.E., 2007. The stable isotope archive of Lake Pannon as a mirror of Late Miocene climate change. Palaeogeogr. Palaeoclimatol. Palaeoecol. 249, 335–350.

132

Harzhauser, M., Kern, A., Soliman, A., Minati, K., Piller, W.E., Danielopol, D.L., 2008. Centennial- to decadal scale environmental shifts in and around Lake Pannon (Vienna Basin) related to a major Late Miocene lake level rise. Palaeogeogr. Palaeoclimatol. Palaeoecol. 270, 102–115

13 12 Heaton, T.H.E., 1999. Spatial, species, and temporal variations in the C/ C ratios of C3 plants: implications for palaeodiet studies. J. Arch. Sci. 26, 637–649.

Henry, J. A., Portier, K.M., Coyne, J., 1994. The climate and weather of Florida. Pineapple Press, Sarasota, Florida, USA.

Hernández Fernández, M., Cárdaba, J.A., Cuevas-González, J., Fesharaki, O., Salesa, M.J., Corrales, B., 2006. The deposits of Middle Miocene vertebrates of Somosaguas (pozuelo de Alarcon, Madrid): paleoenvironment and paleoclimate implications (Los yacimientos de vertebrados del Mioceno medio de Somosaguas (Pozuelo de Alarcón, Madrid): Implicaciones paleoambientales y paleoclimáticas). Estud. Geol. 62, 263–294.

Hoppe, K. A., Stover, S. M., Pascoe, J. R., and Amundson, R., 2004a, Tooth enamel biomineralization in extant horses: implications for isotopic microsampling, Palaeogeogr. Palaeoclimatol. Palaeoecol. 206, 355–65.

Hoppe, K.A., Amundson, R., Vavra, M., McClaran, M.P., Anderson, D.L., 2004b. Isotopic analysis of tooth enamel carbonate from modern North American feral horses: implications for paleoenvironmental reconstructions. Palaeogeogr. Palaeoclimatol. Palaeoecol. 203, 299– 311

IAEA, 2016. Global network of isotopes in precipitation, the GNIP Database; available at http://www-naweb.iaea.org/napc/ih/IHS_resources_isohis.html

Iacumin, P., Bocherens, H., Mariotti, A., Longinelli, A., 1996. Oxygen isotope analyses of coexisting carbonate and phosphate in biogenic apatite; a way to monitor diagenetic alteration of bone phosphate? Earth Planet. Sci. Lett. 142, 1–6.

Ivanov, D., Utescher, T., Mosbrugger, V., Syabryaj, S., Djordjević-Milutinović, D., Molchanoff, S., 2011. Miocene vegetation and climate dynamics in Eastern and Central Paratethys

133

(Southeastern Europe). Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, 262–275.

Johnson, M., Geary, D., 2016. Stable isotope ecology of Hippotherium from the Late Miocene Pannonian Basin system. Palaeogeogr. Palaeoclimatol. Palaeoecol. 459, 44–52.

Kázmér, M., 1990. Birth, life and death of the Pannonian Lake. Palaeogeogr. Palaeoclimatol. Palaeoecol. 79, 171–188.

Kelts, K., Talbot, M., 1990. Lacustrine carbonates as geochemical archives of environmental change and biotic/abiotic interactions. In: Tilzer, M.M., Serruya, C. (Eds.), Large Lakes: Ecological Structure and Function. Springer, Berlin, pp. 288–315.

Kern, A.K., Harzhauser, M., Soliman, A., Piller, W.E., Gross, M., 2012. Precipitation driven decadal scale decline and recovery of wetlands of Lake Pannon during the Tortonian. Palaeogeogr. Palaeoclimatol. Palaeoecol. 317, 1–12.

Knott, C., 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int. J. Primatol. 19, 1061–1079.

Koch, P., Fisher, D., Dettman, D., 1989. Oxygen isotope variation in the tusks of extinct proboscideans: a measure of season of death and seasonality. Geology, 17, 515–519.

Koch, P.L., 1998. Isotopic reconstruction of past continental environments. Annu. Rev. Earth Planet. Sci. 26, 573–613.

Koch, P.L., Tuross, N., Fogel, M.L., 1997. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J. Arch. Sci. 24, 417–429

Kӧhler, M., Moyà-Sola, S., 1997. Ape-like or hominid-like? The positional behavior of Oreopithecus bambolii reconsidered. Proc. Natl. Acad. Sci. 94, 11747–11750.

134

Kohn, M.J., 1996. Predicting animal δ18O: accounting for diet and physiological adaptation. Geochim. Cosmochim. Acta. 60, 4811–4829.

Kohn, M.J., 2004. Reviewed comment: tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series, by Passey, B. H. and Cerling, T. E. (2002). Geochim. Cosmochim. Acta. 68, 403–405.

Kohn, M.J., 2010. Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. Proc. Natl. Acad. Sci. 46, 19691–19695.

Kohn, M.J., Schoeninger, M.J., Valley, J.W., 1996. Herbivore tooth oxygen isotope compositions: effects of diet and physiology. Geochim. Cosmochim. Acta. 60, 3889–3896.

Kohn, M.J., Schoeninger, M.J., Valley, J.W., 1998. Variability in herbivore tooth oxygen isotope compositions: reflections of seasonality or developmental physiology? Chem. Geol. 152, 97–112.

Kohn, M.J., Cerling, T.E., 2002. Stable isotope compositions of biological apatite. Rev. Mineral. Geochem. 48, 455–488.

Kohn, M.J., Welker, J.M., 2005. On the temperature correlation of δ18O in modern precipitation. Earth Planet. Sci. Lett. 231, 87–96

Kohn, M.J., Fremdt, T.J., 2007. Tectonic controls on isotope compositions and species diversification, John Day Basin, central Oregon. Paleobios, 27, 48-61.

Kohn, M.J., McKay, M.P., 2012. Paleoecology of late Pleistocene–Holocene faunas of eastern and central Wyoming, USA, with implications for LGM climate models. Palaeogeogr. Palaeoclimatol. Palaeoecol. 326, 42-53.

Kordos, L., 1991. Le Rudapithecus hungaricus de Rudabànya (Hongrie). l'Anthropologie, 95, 343–362

Kordos, L., Begun, D.R., 2002. Rudabánya: a Late Miocene subtropical swamp deposit with evidence of the origin of the African apes and humans. Evol. Anthropol. 11, 45–57.

135

Kretzoi, M., Krolopp, E., Lörincz, H., Pálfalvy, I., 1976. A Rudabanyai also pannonai prehominidas lelohely floraja, faunaja es retegtani helyzete. Annual Report of the Hungarian Geological Institute, pp. 365–394.

Kutilek, M. J., 1979. Forage-habitat relations of non-migratory African ungulates in response to seasonal rainfall. J. Wildl. Managen. 43, 899-908.

Lee-Thorp, J.A., der Merwe N.J., v., 1987. Carbon isotope analysis of fossil bone apatite. S. Afr. J. Sci. 83, 712–715.

Lee-Thorp, J.A., van der Merwe, N.J., Brain, C.K., 1989. Isotopic evidence for dietary differences between two extinct baboon species from Swartkrans. J. Hum. Evol. 18, 183– 189.

Levin, N.E., Cerling, T.E., Passey, B.H., Harris, J.M., Ehleringer, J.R., 2006. A stable isotope aridity index for terrestrial environments. Proc. Natl. Acad. Sci. 103, 11201–11205.

Longinelli, A., 1984, Oxygen isotopes in mammal bone phosphate: a new tool for paleohydrological and paleoclimatological research? Geochim. Cosmochim.

Acta. 48, 385–90.

Lueger, J.P., 1978. Klimaentwicklung im Pannon und Pont des Wiener Beckens aufgrund von Landschneckenfaunen. Anzeiger der math.-naturw. Klasse der Österreichischen Akademie der Wissenschaften, Vol. 6, pp. 137–149.

Luz, B., Kolodny, Y., Horowitz, M., 1984. Fractionation of oxygen isotopes between mammalian bone-phosphate and environmental drinking water. Geochim. Cosmochim. Acta. 48, 1689–1693.

Luz, B., Kolodny, Y., 1985. Oxygen isotope variations in phosphate of biogenic apatites, IV. Mammal teeth and bones. Earth Planet. Sci. Lett. 75, 29–36.

MacFadden, B., and Cerling, T. E., 1994, Fossil horses, carbon isotopes, and global change, Trends in Ecology and Evolution, 9, 481–5.

136

MacFadden, B.J., Cerling, T.E., 1996. Mammalian herbivore communities, ancient feeding ecology, and carbon isotopes: a 10 million-year sequence from the Neogene of Florida. J. Vertebr. Paleontol. 16, 103–115.

MacFadden, B.J., Higgins, P., 2004. Ancient ecology of 15-million-year-old browsing mammals

within C3 plant communities from Panama. Oecologia, 140, 169–182.

Magyar, I., Geary, D.H., Mü ller, P., 1999. Paleogeographic evolution of the Late Miocene Lake Pannon in central Europe. Palaeogeogr. Palaeoclimatol. Palaeoecol. 147, 151–167.

Mai, D.H., 1997. Die oberoligozänen Floren am Nordrand der Sächsischen Lausitz. Palaeontographica Abteilung B, 244, 1–124.

Marino, B.D., McElroy, M.B., Salawitch, R.J., Spaulding, W.G., 1992. Glacial-to-interglacial

variations in the carbon isotopic composition of atmospheric CO2. Nature, 357, 461–466

Marques, M. C. M., Roper, J.J., Salvalaggio, P.B., 2004. Phenological patterns among plant life- forms in a subtropical forest in southern Brazil. Plant Ecol. 173: 203–213.

McGrew, W., Baldwin, P., Tutin, C., 1981. Chimpanzees in a hot, dry open habitat: Mt. Asserik, Senegal, West Africa. J. Hum. Evol. 10, 227– 244.

Merceron, G., Blondel, C., de Bonis, L., Koufos, G.D., Viriot, L., 2005. A new dental microwear analysis: application to extant primates

Merceron, G., Zazzo, A., Spassov, N., Geraads, D., Kovachev, D., 2006. Bovid paleoecology and paleoenvironments from the Late Miocene of Bulgaria: evidence from dental microwear and stable isotopes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 241, 637–654.

Merceron, G., Schulz, E., Kordos, L., Kaiser, T.M., 2007. Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: evidence from dental meso- and micro-wear analyses of

137

large vegetarian mammals. J. Hum. Evol. 53, 331–349.

Merceron, G., Kaiser, T.M., Kostopoulos, D.S., Schulz, E., 2010. Ruminant diets and the Miocene extinction of European great apes. Proc. R. Soc. Biol. 277, 3105–3112.

Montanari, S., Louys, J., Price, G.J., 2013. Pliocene paleoenvironments of Southeastern Queensland, Australia inferred from stable isotopes of marsupial tooth enamel. PLoS One 8.

Montuire, S., Maridet, O., Legendre, S., 2006. Late Miocene–Early Pliocene temperature estimates in Europe using rodents. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, 247–262.

Morellato, L.P, Talora, D.C., Takahasi, A., Benecke, C.C., Romera, E.C., Zipparro, V.B., 2000. Phenology of Atlantic rain forest trees: A comparative study. Biotropica, 32, 811–823.

Mosbrugger, V., Utescher, T., 1997. The coexistence approach—a method for quantitative reconstructions of tertiary terrestrial palaeoclimate data using plant fossils. Palaeogeogr. Palaeoclimatol. Palaeoecol. 134, 61–86.

Mosbrugger, V., Utescher, T., Dilcher, D.L., 2005. Cenozoic continental climatic evolution of central Europe. Proc. Natl. Acad. Sci. 102, 14964–14969

Moyà-Solà, S., Pons Moyà, J., Kohler, M., 1990. Primates catarrinos (Mammalia) del Neogeno de la península Iberica. Paleontol. Evol. 23, 41–45.

Moyà-Solà, S., Köhler, M., 1996. A Dryopithecus skeleton and the origins of great ape locomotion. Nature 379, 156–159.

138

Nelson, S.V., 2003. The Extinction of Sivapithecus. Brill Academic Publishers, Inc., Boston, USA.

Nelson, S.V., 2007. Isotopic reconstructions of habitat change surrounding the extinction of Sivapithecus, a Miocene hominoid, in the Siwalik group of Pakistan. Palaeogeogr. Palaeoclimatol. Palaeoecol. 243, 204–222.

Nelson, S.V., Rook, L., 2016. Isotopic reconstruction of habitat change surrounding the extinction of Oreopithecus, the last European ape. Am. J. Phys. Anthropol. 160, 254–271.

O'Leary, M.H., 1988. Carbon isotopes in photosynthesis. Bioscience 38, 328–336.

Passey, B. H., and Cerling, T. E., 2002, Tooth enamel mineralization in ungulates: implications for recovering a primary isotopic time-series, Geochim. Cosmochim. Acta. 66, 3225–34.

Passey, B.H., Cerling, T.E., Perkins, M.E., Voorhies, M.R., Harris, J.M., Tucker, S.T., 2002. Environmental change in the great plains: an isotopic record from fossil horses. J. Geol. 110, 123–140.

Passey, B.H., Robinson, T.F., Ayliffe, L.K., Cerling, T.E., Sphonheimer, M., Dearing, M.D.,

2005. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J. Arch. Sci. 32, 1459–1470.

Poage, M.A., Chamberlain, C.P., 2001. Empirical relationships between elevation and the stable isotope composition of precipitation and surface waters: considerations for studies of paleoelevation change. Am. J. Sci. 301, 1–15.

Quade, J., Cerling, T.E., Andrews, P., Alpagut, B., 1995. Paleodietary reconstruction of Miocene faunas from Paşalar, Turkey using stable carbon and oxygen isotopes of fossil tooth enamel. J. Hum. Evol. 28, 373–384.

Quan, C., Liu, Y.-S.C., Tang, H., Utescher, T., 2014. Miocene shift of European atmospheric

139

circulation from trade wind to westerlies. Sci. Rep. 4, 5660.

Rey, K., Amiot, R., Lécuyer, C., Koufos, G.D., Martineau, F., Fourel, F., Kostopoulos, D.S., Merceron, G., 2013. Late Miocene climatic and environmental variations in northern Greece inferred from stable isotope compositions (δ18O, δ13C) of equid teeth apatite. Palaeogeogr. Palaeoclimatol. Palaeoecol. 388, 48–57.

Rögl, V.F., 1998. Palaeogeographic considerations for Mediterranean and Paratethys seaways (Oligocene to Miocene). Ann. Nat. Hist. Mus. Vienna 99A, 279–310.

Rowe, N., 1996. The Pictorial Guide to the Living Primates. Pogonias Press, East Hampton

Rozanski, K., Araguas-Araguas, L., Gonfiantini, R., 1993. Isotopic patterns in modern global precipitation. Geophys. Monogr. 78, 1–36.

Scott, R.S., Amour-Chelu, M., Bernor, R.L., 2005. Hipparionine horses of the greater Pannonian Basin: morphometric evidence from the postcranial skeleton. Paleontogr. Ital. 90, 193–212.

Sharp, Z. D., and Cerling, T. E., 1998, Fossil isotope records of seasonal climate and ecology: straight from the horse’s mouth. Geology, 26, 219–22.

Spassov, N., Geraads, D., Hristova, L., Markov, G.N.,Merceron, G., Tzankov, T., Stoyanov, K., Böhme, M., Dimitrova, A., 2012. A hominid tooth from Bulgaria: the last pre-human hominid of continental Europe. J. Hum. Evol. 62, 138–145.

Spinoni, J., Szalai, S., Szentimrey, T., Lakatos, M., Bihari, Z., Nagy, A., Németh, Á., Kovács, T., Mihic, D., Dacic, M., Petrovic, P., Kržič, A., Hiebl, J., Auer, I., Milkovic, J., Štepánek, P., Zahradnícek, P., Kilar, P., Limanowka, D., Pyrc, R., Cheval, S., Birsan, M.-V., Dumitrescu, A., Deak, G., Matei, M., Antolovic, I., Nejedlík, P., Štastný, P., Kajaba, P., Bochnícek, O., Galo, D., Mikulová, K., Nabyvanets, Y., Skrynyk, O., Krakovska, S., Gnatiuk, N., Tolasz, R., Antofie, T., Vogt, J., 2015. Climate of the Carpathian Region in the period 1961–2010: climatologies and trends of 10 variables. Int. J. Climatol. 35, 1322– 1341.

Sukselainen, L., Fortelius, M., Harrison, T., 2015. Co-occurrence of pliopithecoid and hominoid primates in the fossil record: An ecometric analysis. J. Hum. Evol. 84, 25–41.

140

Suwa, G., Kunimatsu, Y. Ataabadi, M., Orak, Z., Sasaki, T., Fortelius, M., 2016. The first hominoid from the Maragheh Formation, Iran. Palaeobiodivers. Palaeoenviron. 1–9.

Talbot, M.R., 1990. A review of the palaeohydrological interpretation of carbon and oxygen isotopic ratios in primary lacustrine carbonates. Chem. Geol. 80, 261–278.

Teaford, M.F., Ungar, P.S., 2000. Diet and the evolution of the earliest human ancestors. Proc. Natl. Acad. Sci. 97, 13506–13511.

Tipple, B.J., Meyers, S.R., Pagani, M., 2010. Carbon isotope ratio of Cenozoic CO2: a comparative evaluation of available geochemical proxies. Paleoceanography, 25, PA3202.

Tü tken, T., Vennemann, T., 2009. Stable isotope ecology of Miocene large mammals from Sandelzhausen, southern Germany. Paläontol. Z. 83, 207–226.

Tü tken, T., Vennemann, T.W., Janz, H., Heizmann, E.P.J., 2006. Palaeoenvironment and palaeoclimate of the Middle Miocene lake in the Steinheim Basin, SW Germany: a reconstruction from C, O, and Sr isotopes of fossil remains. Palaeogeogr. Palaeoclimatol. Palaeoecol. 241, 457–491.

Tü tken, T., Kaiser, T.M., Vennemann, T.,Merceron, G., 2013. Opportunistic feeding strategy for the earliest hypsodont equids: evidence from stable isotopes and dental wear proxies. PLoS One 8 (9), E74463

Tü tken, T., 2014. Isotope compositions (C, O, Sr, Nd) of vertebrate fossils from the Middle Eocene oil shale of Messel, Germany: Implications for their taphonomy and palaeoenvironment. Palaeogeogr. Palaeoclimatol. Palaeoecol. 416, 92–109.

Ungar, P.S., 1996. Dental microwear of European Miocene catarrhines: evidence for diets and tooth use. J. Hum. Evol. 31, 335–366.

Ungar, P.S., 1998. Dental allometry, morphology, and wear as evidence for diet in fossil primates. Evol. Anthropol. 6, 205–217.

Ungar, P.S., 2005. Dental evidence for the diets of fossil primates from Rudabánya, northeastern Hungary with comments on extant primate analogs and “noncompetitive” sympatry.

141

Palaeontogr. Ital. 90, 97–112.

Ungar, P.S., Kay, R.F., 1995. The dietary adaptations of European Miocene catarrhines. Proc. Natl. Acad. Sci. 92, 5479–5481

Utescher, T., Ivanov, D., Harzhauser, M., Bozukov, V., Ashraf, A.R., Rolf, C., 2009. Cyclic climate and vegetation change in the Late Miocene of western Bulgaria. Palaeogeogr. Palaeoclimatol. Palaeoecol. 272, 99–11

Utescher, T., Bruch, A.A., Erdei, B., François, L., Ivanov, D., Jacques, F.M.B., Kern, A.K., Liu, Y.-S.(.C.)., Mosbrugger, V., Spicer, R.A., 2014. The coexistence approach—theoretical background and practical considerations of using plant fossils for climate quantification. Palaeogeogr. Palaeoclimatol. Palaeoecol. 410, 58–73.

Utescher, T., Erdei, B., Hably, L., Mosbrugger, V., 2017. Late Miocene vegetation of the Pannonian Basin. Palaeogeogr. Palaeoclimatol. Palaeoecol. 467, pp. 131-148. van Dam, J.A., 2006. Geographic and temporal patterns in the late Neogene (12–3 Ma) aridification of Europe: the use of small mammals as paleoprecipitation proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, 190–218. van Dam, J.A., Reichart, G.J., 2009. Oxygen and carbon isotope signatures in late Neogene horse teeth from Spain and application as temperature and seasonality proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 274, 64–81 van der Merwe, N.J., Medina, E., 1991. The canopy effect, carbon isotope ratios and foodwebs in Amazonia. J. Arch. Sci. 18, 249–259.

Vislobokova, I. A., 2006. Associations of ruminants in Miocene ecosystems of Eastern Alpine Region. Paleontological Journal. 40, 438–447.

Vislobokova, I. A., 2007. New data on Late Miocene mammals of Kohfidisch, Austria. Paleontological Journal. 41, 451–460.

Vogel, E.R., van Woerden, J.T., Lucas, P.W., Utami Atmoko, S.S., van Schaik, C.P., Dominy, N.J., 2008. Functional ecology and evolution of hominoid molar enamel thickness: Pan

142

troglodytes schweinfurthii and Pongo pygmaeus wurmbii. J. Hum. Evol. 55, 60–74.

Wang, Y., Cerling, T. E., and MacFadden, B., 1994, Fossil horses and carbon isotopes: new evidence for Cenozoic dietary, habitat, and ecosystem changes in North America, Palaeogeogr. Palaeoclimatol. Palaeoecol, 107, 269–79.

Wolanski, E., Gereta, E., Borner, M., Mduma, S., 1999. Water, migration and the Serengeti ecosystem. Am. Sci. 87, 526–533.

Wrangham, R., Rogers, M., Basuta, G., 1993. Ape food density in the ground layer in Kibale Forest, Uganda. Afr. J. Ecol. 31, 49– 57.

Yakir, D., 1992. Variation in the natural abundances of oxygen-18 and deuterium in plant carbohydrates. Plant Cell Environ. 15, 1005–1102

Zachos, J., Pagani, M., Sloan, L., Thomas, E., Billups, K., 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292, 686-693.

Zanazzi, A., Judd, D., Fletcher, A., Bryant, H., Kohn, M., 2015. Eocene-Oligocene latitudinal climate gradients in North America inferred from stable isotope ratios in perissodactyl tooth enamel. Palaeogeogr. Palaeoclimatol. Palaeoecol. 417, 561-568.

Zazzo, A., Lécuyer, C., Heintz, E., and Mariotti, A., 2002, Intra-tooth isotopic variations in late Miocene bovid enamel from Afghanistan: paleobiological, taphonomical, and climatical implications, Palaeogeogr. Palaeoclimatol. Palaeoecol. 186, 145–61.

Zazzo, A., Balasse, M., and Patterson, W. P., 2005, High-resolution δ13C intra-tooth profiles in bovine enamel: implications for mineralization pattern and isotopic attenuation. Geochim. Cosmochim. Acta. 69, 3631–42.

Zazzo, A., Balasse, M., Passey, B. H., Moloney, A. P., Monahan, F. J., and Schmidt, O., 2010, The isotope record of short and long-term dietary changes in sheep tooth enamel: Implications for quantitative reconstruction of palaeodiets. Geochim. Cosmochim. Acta. 74, 3571–86.

Zazzo, A., Bendrey, R., Vella, D., Moloney, A. P., Monahan, F. J., and Schmidt, O., 2012, A

143

refined sampling strategy for intra-tooth stable isotope analysis of mammalian enamel. Geochim. Cosmochim. Acta. 84, 1–13.

Zin-Maung-Maung-Thein, Takai, M., Uno, H., Wynn, J.G., Egi, N., Tsubamoto, T., 2011. Stable isotope analysis of the tooth enamel of Chaingzauk mammalian fauna (late Neogene, Myanmar) and its implication to paleoenvironment and paleogeography. Palaeogeogr. Palaeoclimatol. Palaeoecol. 300, 11–22.

Zimmermann, J.K., Wright, S.J., Calderon, O., Pagan, M.A., Paton, S. 2007. Flowering and fruiting phenologies of seasonal and aseasonal neotropical forests: The role of annual changes in irradiance. J. Trop. Ecol. 23, 231–251.

144

Chapter 5

5 Conclusions and Directions for Future Research 5.1 Summary and Perspectives

The research presented in this dissertation provides new and significant information concerning the paleoenvironmental context for Miocene great ape evolution in Europe. This geochemical study had three primary aims: 1) evaluate the types of habitats present at Rudabánya II (R. II) in terms of forest canopy cover, 2) examine trophic niche dynamics among the diverse ungulate community in assessment of the niche partitioning hypothesis, and 3) estimate key climatic variables including mean annual temperature (MAT), mean annual precipitation (MAP), and degree of seasonality. The results of this research underscore the importance of evaluating Miocene hominoid paleoecology on a regional scale. This research also provides critical information for understanding the factors that acted to promote the assembly of high diversity browsing ungulate communities in Central and Western Europe during the early Late Miocene (Vallesian Optimum).

Several of the results reported here confirm existing ideas about the paleoecology and paleoclimate of R. II. For example, stable carbon (δ13C) and oxygen (δ18O) isotope ratios indicate the presence of a heterogeneous wetland-forest environment with a gradient of more open to closed canopy habitats. The mean δ13C value of plants consumed by the R. II ungulates (−28.3‰) is similar to that measured for modern deciduous humid subtropical vegetation (−28.4‰) in the Okefenokee Swamp Forest, southern Georgia, USA (DeLucia and Schlesinger, 1995). These results are concordant with those previously interpreted from paleobotanicals (Kretzoi et al., 1976; Kordos and Begun, 2002; Halby and Erdei, 2013; Utescher et al. 2017), ungulate meso- and microwear (Merceron et al., 2007), and small and large mammal ecometrics (Bernor et al., 2004; Scott et al., 2005; Sukselainen et al., 2015). Within the gradient of more open to closed canopy forest, it is likely that Rudapithecus would have occupied dense closed canopy habitats where access to fruit was relatively continuous. The trophic behaviours of the R. II ungulates inferred from stable isotope and strontium/calcium (Sr/Ca) trace element ratios were broadly consistent with those reconstructed using and meso- and microwear (Merceron et al.,

145

2007). Geochemical analysis revealed significant differences in dietary resource use within the ungulate community, implying that the different species did partition resources by selecting different plants and/or plant parts. However, several of the sampled species displayed overlapping ranges of isotopic and Sr/Ca values implying some degree of interspecific competition. A local abundance of plant resources in addition to dietary resource partitioning likely acted to diminish competition and promote species coexistence within the diverse community of predominantly browsing ungulates.

Both MAP and seasonality estimates derived from stable isotope values are congruent with those reconstructed from paleobotanicals (Damuth et al., 2003; van Dam, 2006; Böhme et al., 2008, 2011; Hably and Erdei, 2013; Utescher et al., 2017), large and small mammals (Damuth et al., 2003; Eronen and Rook, 2004; van Dam 2006; Eronen et al., 2010), and herpetofauna (Böhme et al., 2008). A MAP estimate ranging between 1030 and 1333 mm/yr was calculated from the average δ13C value of the equid Hippotherium intrans. Serial isotope analysis revealed low average amplitudes of variation in δ18O (1.8‰), suggesting relatively mild intra-annual variation in climate. The average annual range of drinking water δ18O values based on the serial profiles is 4.5‰, which is lower than the modern range measured in precipitation at nearby reference stations in Slovakia (-7.5‰) and Vienna (-7.2‰) (IAEA), indicating that seasonal changes in climate were considerably milder during the early Late Miocene.

On the other hand, several of the results presented here were surprising and require further investigation. For example, MAT estimates calculated from the average δ18O value of H. intrans ranged between 11 and 14°C. This temperature range is unrealistically low given the subtropical character of the R. II fauna (Bernor et al., 2003, 2004) and is inconsistent with estimates derived from other proxies (Damuth et al., 2003; Mosbrugger et al., 2005; Montuire et al., 2006; Utescher et al., 2017). There are two factors that could explain the relatively low MAT estimates calculated from the R. II equids: 1) drinking from water sources with low oxygen isotope values distinct from local precipitation, such as rivers and streams flowing from higher elevations, and 2) the amount effect. To better understand the factors that could have influenced the low MAT estimates calculated in this study further research is required evaluating the ranging and drinking behaviours of Late Miocene equids within the Pannonian Basin.

146

Trophic behaviours inferred from Sr/Ca ratios were generally concordant with those reconstructed from stable isotope and morphological proxies. However, the elevated Sr/Ca ratios of the large-bodied bovid Miotragocerus sp. were inconsistent with both stable isotope and morphological data indicating a diet dominated by leaves (Solounias and Dawson-Saunders, 1988; Spassov and Geraads, 2004; Merceron et al. 2007; Merceron, 2009; Eastham et al., 2016). This discrepancy could be accounted for by differences in the digestive physiology of ruminating ungulates. Several studies have reported higher Sr/Ca and barium/calcium (Ba/Ca) ratios in the hard tissues of ruminants compared to contemporaneous mongastric ungulates (Gilbert et al., 1994; Burton et al., 1999; Balter et al., 2002; Domingo et al., 2009, 2012). It has been argued that the prolonged retention of digesta in ruminant bodies, in addition to more efficient cellulose digestion, results in a greater concentration of non-essential trace elements in their bones and teeth (Balter et al., 2002). Surprisingly, the Sr/Ca ratios of Miotragocerus sp. were significantly higher than those of the small-bodied tragulid Micromeryx flourensianus. These results were unexpected given that both species were browsing ruminants (Tütken et al., 2006; Merceron et al., 2007; Merceron, 2009; Aiglstorfer et al., 2014; Eastham et al., 2016). The behaviour of strontium in the gastrointestinal tracts of small vs. large-bodied ruminants has not yet been studied, so no conclusive remarks can be made. However, it is possible that the unique digestive adaptations of extant small-bodied ruminant frugivores could account for this finding. Testing hypotheses surrounding the behaviour of non-essential trace elements under different digestive physiologies requires much further baseline research with modern ungulates.

In summary, the research presented in this dissertation highlights the utility of geochemical approaches for reconstructing the paleoecology and paleoclimate of Miocene great ape localities. The humid wetland-forest environment that Rudapithecus inhabited was most similar to that of contemporaneous hominoids in Western Europe, but strikingly different from that of hominoids in the Eastern Mediterranean. While adaptations for efficient suspensory arboreality and hard fruit feeding would have allowed Rudapithecus to endure some degree of environmental deterioration, the restriction and fragementation of wetland-forest habitats following the retreat of Lake Pannon would have greatly influenced its extinction. No single ecological factor can account for the decline of European great apes during the Late Miocene. The continued analysis of regional paleoecology will allow for a better understanding the evolution of this highly diverse group.

147

5.2 Directions of Future Research

R. II is extremely rare among Eurasian Miocene mammalian localities in preserving both a hominoid and pliopithecoid, and as such provides the unique opportunity to evaluate the factors that acted to promote co-occurrence. Analysis of incisor shape and curvature indicates that while the diets of Rudapithecus and Anapithecus may have overlapped considerably, the two primates likely differed in their use of fallback resources (Deane et al., 2013). Deane et al. (2013) suggest that during seasonal periods of ripe fruit shortage Anapithecus may have consumed a greater proportion of leaves, while Rudapithecus consumed harder fruits. I am interested in expanding upon the results of my dissertation research by analyzing the enamel stable isotope and trace element ratios of the R. II primates. Using a geochemical approach I will evaluate: 1) dietary resource use, 2) resource partitioning, and 3) seasonal variation in diet. If granted permission to sample the R. II primates, I will measure stable carbon (δ13C) and oxygen isotope ratios (δ18O) in enamel carbonate, as well as Sr/Ca, Ba/Ca, and zinc/calcium (Zn/Ca) trace element ratios. I will also utilize a suite of next generation isotopic ratios including magnesium (δ26Mg), zinc (δ66Zn), and calcium (δ44Ca). Recent studies have highlighted the utility of these new isotope systems for distinguishing trophic behaviour in both modern and ancient ecosystems (Martin et al., 2014; 2015, Melin et al., 2014, Jaouen et al., 2016).

While the depositional sequence at R. II records critical information for understanding the ecology of early Vallesian mammals, it lacks the depth of time required to evaluate potential changes in species diversity and community structure that occurred in association with the regression of Lake Pannon. A comparative meso- and microwear study of European ruminants indicates the onset of more open environments in Hungary during the early Turolian (Merceron et al., 2010). These findings were recently supported by the results of an enamel stable isotope study by Johnson and Geary (2016), which found evidence for open to water-stressed conditions in the central Pannonian Basin beginning in the late Vallesian and continuing throughout the

Turolian. Interestingly, these authors report lower carbon isotope values in early Turolian equids from several localities in the northern Pannonian region (Pannonian Basin and Vienna Basin), suggesting the persistence of restricted forest environments. Paleobotanical data supports the persistence of humid and wet conditions along the northern margin of the Lake Pannon throughout the Vallesian and early Turolian (Utescher et al., 2017). I am interested in utilizing a

148 geochemical approach to reconstruct the paleoecology and paleoclimate of the northern Pannonian region during this period. If granted access to ungulate collections from localities such as Ferihegy II., Prottes, Gols Burgenland, Mannersdorf bei Angern, I will measure a suite of enamel stable isotope and trace element ratios to evaluate: 1) vegetation cover, 2) climatic regime, and 3) trophic resource use and breadth. The existence of a humid forest refugium in the northern Pannonian region would have critical implications for both primates and browsing ungulates during the Late Miocene.

The Middle Miocene Climatic Optimum (MMCO; 17 – 15 Ma) represents an important period in the evolution of terrestrial ecosystems when global warming interrupted the long-term trend of Cenozoic cooling and aridification (Zachos et al., 2008). Important faunal exchanges between Africa and Eurasia took place during the MMCO, in particular the dispersal of hominoids and pliopithecoids into Eurasia. It is hypothesized that elevated atmospheric CO2 levels influenced the expansion of subtropical forests and allowed for the abundant adaptive radiation of Eurasian catarrhines (Hamon et al., 2012). Browsing ungulate communities in Europe and North America reached peak levels of species diversity during the MMCO, far exceeding that of any modern ungulate community (Fritz et al., 2016). The assembly of high diversity ungulate communities during this period has been related to the effects of higher atmospheric CO2 levels on primary productivity (Fritz et al., 2016). I am interested in applying the geochemical methods learned throughout my doctoral research to examine the paleoecology of primate and ungulate communities in Europe during the MMCO. In particular, I would like to examine the stable isotope paleoecology of Sansan, a rich Middle Miocene (15 Ma) mammalian locality in southwestern France. Sansan is unique among Eurasian Miocene localities in preserving 20 species of ungulates, including 9 megaherbivores (>1000 kg), and two species of pliopithecoids. Further, the depositional sequence at Sansan records the final stages of the MMCO and onset of the Miocene Cooling Event (14.8 Ma). Because of the high faunal diversity and unique paleoenvironmental and paleoclimatic situation, Sansan is an ideal site to examine questions related to the influence of global climate change on mammalian biodiversity and niche dynamics. Using a suite of stable isotope ratios measured in fossil enamel I will evaluate: 1) trophic niche dynamics among the ungulate and primate communities, 2) types of habitats present in terms of vegetation cover, 3) climatic regime in terms of MAP, MAT, and degree of seasonality, and 4) evidence for changes in dietary resource use and breadth through time in

149 evaluation of the niche conservatism hypothesis. Examining how past species reacted to climate change allows for a better understanding of ecosystem dynamics and insight into how extant species will react to current and projected climate change.

References

Aiglstorfer, M., Bocherens, H., Böhme, M., 2014. Large mammal ecology in the late Middle Miocene locality Gratkorn (Austria). Palaeobiodivers. Palaeoenviron. 94, 189–213.

Balter,V., Bocherens, H., Person, A., Labourdette, N., Renard, M., Vandermeersch, B., 2002. Ecological and physiological variability of Sr/Ca and Ba/Ca in mammals of West European mid-Wü rmian food webs. Palaeogeogr. Palaeoclimatol. Palaeoecol. 186, 127– 143.

Bernor, R.L., Fahlbusch, V., Andrews, P., de Bruijn, H., Fortelius, M., Rögl, F., Steininger, F.F., Werdelin, L., 1996. The evolution of European and West Asian later Neogene faunas: a biogeographic and paleoenvironmental synthesis. In: Bernor, R., Fahlbusch, V., Mittmann, W. (Eds.), The Evolution of Western Eurasian Neogene Mammal Faunas. Columbia University Press, pp. 449–470.

Bernor, R.L., Armour-Chelu,M., Kaiser, T.M., Scott, R.S., 2003. An evaluation of the late MN 9 (Late Miocene, Vallesian age), hipparion assemblage from Rudabánya (Hungary): systematic background, functional anatomy and paleoecology. Coloquios De Paleontología, Volumen Extraordinario Vol. 1, pp. 35–45.

Bernor, R.L., Kordos, L., Rook, L., Agustí, J., Andrews, P., Armour-Chelu, M., Begun, D.R., de Bonis, L., Cameron, D.W., Damuth, J., Daxner-Höck, G., Fessaha, N., Fortelius, M., Franzen, J.L., Gasparik, M., Gentry, A., Heissig, K., Hernyak, G., Kaiser, T.M., Koufos, G.D., Krolopp, E., Jánossy, D., Llenas, M., Meszáros, L., Mü ller, P., Renne, P.R., Rocek, Z., Sen, S., Scott, R.S., Szindlar, Z., Topál, G.Y., Ungar, P.S., Untescher, T., van Dam, J.A., Werdelin, L., Ziegler, R., 2004. Recent advances on multidisciplinary research at Rudabanya, Late Miocene (MN9), Hungary: a compendium. Paleontogr. Ital. 89, 3–36.

150

Böhme, M., Ilg, A., Winklhofer, M., 2008. Late Miocene “washhouse” climate in Europe. Earth Planet. Sci. Lett. 275, 393–401.

Böhme, M., Winklhofer, M., Ilg, A., 2011. Miocene precipitation in Europe: temporal trends and spatial gradients. Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, 212–218.

Burton, J.H., Price, T.D., Middleton, W.D., 1999. Correlation of bone Ba/Ca and Sr/Ca due to biological purification of calcium. J. Arch. Sci. 26, 609–616.

Damuth, J., J.A., v.D., Utescher, T., 2003. Palaeoclimate proxies from biotic proxies. In: Bernor, R.L., Kordos, L., Rook, L. (Eds.), Recent Advances on Multidisciplinary Research at Rudabánya, Late Miocene (MN9), Hungary: A Compendium. Palaeontographica Italica Vol. 89, pp. 1–34.

Daxner-Höck, G., 2004. Biber und ein zwerghamster aus Mataschen (unter-pannonium, steirisches becken). Joannea Geol. Paläontol. 5, 19–33

Daxner-Höck, G., Harzhauser, M., Göhlich, U., 2016. Fossil record and dynamics of the Late Miocene small mammal faunas of the Vienna Basin and adjacent basins. Austria. C.R. Palevol. 15, 855–862.

Deane, A.S., Nargolwalla, M.C., Kordos, L., Begun, D.R., 2013. New evidence for diet and niche partitioning in Rudapithecus and Anapithecus from Rudabánya, Hungary. J. Hum. Evol. 65, 704–714.

Domingo, L., Cuevas-González, J., Grimes, S.T., Hernández Fernández, M., López-Martínez, N., 2009. Multiproxy reconstruction of the palaeoclimate and palaeoenvironment of the MiddleMiocene Somosaguas site (Madrid, Spain) using herbivore dental enamel. Palaeogeogr. Palaeoclimatol. Palaeoecol. 272, 53–68.

Eastham, L. C., Feranec, R.S., Begun, D.R., 2016. Stable isotopes show resource partitioning among the early Late Miocene herbivore community at Rudabánya II: Paleoenvironmental

151

implications for the hominoid, Rudapithecus hungaricus. Palaeogeogr. Palaeoclimatol. Palaeoecol. 454, 161–174.

Eronen, J., Rook, L., 2004. The Mio-Pliocene European primate fossil record: dynamics and habitat tracking. J. Hum. Evol. 47, 323–341.

Fritz, S.A., Eronen, J.A., Schnitzler, J., Hof, C., Janis, C.M., Mulch, A., Böhning-Gaese, K., Graham, C.H., 2016. Twenty-million-year relationship between mammalian diversity and primary productivity. PNAS. 113, 10908–10913.

Gilbert, C., Sealy, J., Sillen, A., 1994. An investigation of barium, calcium and strontium as palaeodietary indicators in the Southwestern Cape, South Africa. J. Arch. Sci. 21, 173–184.

Hably, L., Erdei, B., 2013. A refugium of mastixia in the Late Miocene of eastern central Europe. Rev. Palaeobot. Palynol. 197, 218–225.

Hamon, N., Sepulchre, P., Donnadieu, Y., Henrot, A-J., Francois, L., Jaeger, J-J., Ramstein, G., 2012. Growth of subtropical forests in Miocene Europe: The roles of carbon dioxide and Antarctic ice volume. Geology, 40, 567–570.

Harzhauser, M., Daxner-Höck, G., Piller, W.E., 2004. An integrated stratigraphy of the Pannonian (Late Miocene) in the Vienna Basin. Austrian Journal of Earth Sciences, 95/96, 6–19

Harzhauser, M., Latal, C., Piller, W.E., 2007. The stable isotope archive of Lake Pannon as a mirror of Late Miocene climate change. Palaeogeogr. Palaeoclimatol. Palaeoecol. 249, 335–350.

IAEA, 2016. Global network of isotopes in precipitation, the GNIP Database; available at http://www-naweb.iaea.org/napc/ih/IHS_resources_isohis.html

152

Jaouen, K., Beasley, M., Schoeninger, M., Hublin, J-J., Richards, M.P., 2016. Zinc isotope ratios of bones and teeth as new dietary indicators: results from a modern food web (Koobi Fora, Kenya). Scientific Reports 6, Article number: 26281.

Johnson, M., Geary, D., 2016. Stable isotope ecology of Hippotherium from the Late Miocene Pannonian Basin system. Palaeogeogr. Palaeoclimatol. Palaeoecol. 459, 44–52.

Kordos, L., Begun, D.R., 2002. Rudabánya: a Late Miocene subtropical swamp deposit with evidence of the origin of the African apes and humans. Evol. Anthropol. 11, 45–57.

Kretzoi, M., Krolopp, E., Lörincz, H., Pálfalvy, I., 1976. A Rudabanyai also pannonai prehominidas lelohely floraja, faunaja es retegtani helyzete. Annual Report of the Hungarian Geological Institute, pp. 365–394.

Lueger, J.P., 1978. Klimaentwicklung im Pannon und Pont des Wiener Beckens aufgrund von Landschneckenfaunen. Anzeiger der math.-naturw. Klasse der Österreichischen Akademie der Wissenschaften, Vol. 6, pp. 137–149.

Martin, J.E., Vance, D., Balter, V., 2014. Natural variation in magnesium isotopes in mammal bones and teeth from two South African trophic chains. Geochim. Cosmochim. Acta, 130, 12–20.

Martin, J.E., Vance, D., Balter, V., 2015. Magnesium isotope ecology using mammal tooth enamel. PNAS. 13, 430–5.

Melin, A.D., Crowley, B.E., Brown, S.T., Wheatley, P.V., Moritz, G.L., Tuh Yit Yu, F., Bernard, H., DePaolo, D.J., Jacobson, A.D., Dominy, N.J., 2014. Calcium and carbon stable isotope ratios as paleodietary indicators. Am. J. Phys. Anth. 154, 633–643.

Merceron, G., 2009. The early Valleisan vertebrates of Atzelsdorf (Late Miocene, Austria). Ann. Nat. Hist. Mus. Vienna 111A, 647–660

Merceron, G., Schulz, E., Kordos, L., Kaiser, T.M., 2007. Paleoenvironment of Dryopithecus brancoi at Rudabánya, Hungary: evidence from dental meso- and micro-wear analyses of large vegetarian mammals. J. Hum. Evol. 53, 331–349.

153

Merceron, G., Kaiser, T.M., Kostopoulos, D.S., Schulz, E., 2010. Ruminant diets and the Miocene extinction of European great apes. Proc. R. Soc. Biol. 277, 3105–3112.

Montuire, S., Maridet, O., Legendre, S., 2006. Late Miocene–Early Pliocene temperature estimates in Europe using rodents. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, 247–262.

Mosbrugger, V., Utescher, T., Dilcher, D.L., 2005. Cenozoic continental climatic evolution of central Europe. Proc. Natl. Acad. Sci. 102, 14964–14969.

Pianka, E.R., 1981. Competition and niche theory. In: May, R.M. (Ed.), Theoretical Ecology: Principles and Applications. Blackwell Scientific Publications, Oxford, United Kingdom, pp. 167–196.

Schoener, T.W., 1974. Resource partitioning in ecological communities. Science 185, 27–39.

Scott, R.S., Amour-Chelu, M., Bernor, R.L., 2005. Hipparionine horses of the greater Pannonian Basin: morphometric evidence from the postcranial skeleton. Paleontogr. Ital. 90, 193–212

Solounias, N., Dawson-Saunders, B., 1988. Dietary adaptations and palaeoecology of the Late Miocene ruminants from Pikermi and Samos in Greece. Palaeogeogr. Palaeoclimatol. Palaeoecol. 65, 149–172

Sukselainen, L., Fortelius, M., Harrison, T., 2015. Co-occurrence of pliopithecoid and hominoid primates in the fossil record: An ecometric analysis. J. Hum. Evol. 84, 25–41.

Utescher, T., Erdei, B., Hably, L., Mosbrugger, V., 2017. Late Miocene vegetation of the Pannonian Basin. Palaeogeogr. Palaeoclimatol. Palaeoecol. 467, 131–148.

154 van Dam, J.A., 2006. Geographic and temporal patterns in the late Neogene (12–3 Ma) aridification of Europe: the use of small mammals as paleoprecipitation proxies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, 190–218.

Zachos, J.C., Dickens, G.R., Zeebe, R.E., 2008. Age and δ18O analysis relating to Cenozoic greenhouse climates. Nature, 451, 279–28.

155

Appendicies

13 18 Appendix A: δ CE and δ OE values from the sampled R. II fauna.

13 18 18 Specimen Tooth δ CE δ OE δ OE Taxon Family No. position (V-PDB, ‰) (V-PDB, ‰) (V-SMOW, ‰) Hippotherium intrans Equidae RUD782 M3 –12.9 –7.2 23.4 Hippotherium intrans Equidae RUD729 M2 –13.2 –7.0 23.6 Hippotherium intrans Equidae RUD1082 m3 –11.0 –4.2 26.5 Hippotherium intrans Equidae RUD1014 m3 –12.9 –8.0 22.6 Hippotherium intrans Equidae RUD804 M2 –12.7 –8.0 22.6 Hippotherium intrans Equidae RUD794 m2 –12.9 –8.3 22.3 Hippotherium intrans Equidae RUD139 M3 –12.9 –8.0 22.6 Hippotherium intrans Equidae RUD429 m3 –13.0 –7.4 23.2 Hippotherium intrans Equidae RUD628 m2 –13.0 –7.2 23.4 Hippotherium intrans Equidae RUD721 M3 –13.0 –7.5 23.1 Hippotherium intrans Equidae RUD728 M3 –13.0 –8.2 22.4 Hippotherium intrans Equidae RUD762 M2 –12.0 –5.5 25.2 Lucentia aff. pierensis Cervidae RUD1851 P3 –13.1 –5.0 25.7 Lucentia aff. pierensis Cervidae RUD279 m2 –11.8 –8.2 22.4 Lucentia aff. pierensis Cervidae RUD486 m3 –12.4 –4.2 26.5 Lucentia aff. pierensis Cervidae RUD1011 M2 –12.0 –8.0 22.6 Lucentia aff. pierensis Cervidae RUD699 P2 –11.0 –4.2 26.5 Lucentia aff. pierensis Cervidae RUD1547 M1 –11.4 –5.9 24.8 Lucentia aff. pierensis Cervidae RUD154 M2 –12.9 –2.6 28.2 Lucentia aff. pierensis Cervidae RUD637 m3 –12.6 –4.8 25.9 Lucentia aff. pierensis Cervidae RUD695 m2 –12.0 –5.3 25.4 Lucentia aff. pierensis Cervidae RUD801 M1 –11.3 –6.3 24.4 Lucentia aff. pierensis Cervidae RUD1457 m2 –12.2 –7.5 23.1 Lucentia aff. pierensis Cervidae RUD1513 M3 –13.3 –5.9 24.8 Lucentia aff. pierensis Cervidae RUD579 m1 –13.0 –3.8 26.9 Miotragocerus sp. Bovidae RUD1611 m2 –13.5 –6.8 23.9 Miotragocerus sp. Bovidae RUD1530 M3 –13.5 –8.4 22.2 Miotragocerus sp. Bovidae RUD167 M1 –14.1 –7.2 23.4 Miotragocerus sp. Bovidae RUD176 M2 –11.5 –4.0 26.7 Miotragocerus sp. Bovidae RUD377 m3 –13.2 –7.0 23.6 Miotragocerus sp. Bovidae RUD391 m2 –13.9 –3.6 27.1 Miotragocerus sp. Bovidae RUD699 M3 –12.8 –5.9 24.8 Miotragocerus sp. Bovidae RUD693 m1 –13.0 –6.5 24.2 Parachleuastochoerus kretzoii Suidae RUD543 P3 –12.3 –6.8 23.9 Parachleuastochoerus kretzoii Suidae RUD1026 M2 –12.5 –8.5 22.1 Parachleuastochoerus kretzoii Suidae RUD1673 M3 –12.5 –6.8 23.9

156

Parachleuastochoerus kretzoii Suidae RUD1096 m3 –11.6 –7.8 22.8 Parachleuastochoerus kretzoii Suidae RUD668 p4 –12.5 –7.7 22.9 Propotamochoerus palaeochoerus Suidae RUD1021 M3 –11.8 –8.3 22.3 Propotamochoerus palaeochoerus Suidae RUD1355 M2 –9.7 –7.5 23.1 Propotamochoerus palaeochoerus Suidae RUD1343 M1 –10.2 –6.2 24.5 Propotamochoerus palaeochoerus Suidae RUD1331 P3 –10.3 –7.2 23.4 Micromeryx flourensianus Moschidae RUD1760 m2 –13.1 –8.2 22.4 Micromeryx flourensianus Moschidae RUD563 M3 –12.8 –5.5 25.2 Micromeryx flourensianus Moschidae RUD1361 M3 –13.8 –7.1 23.5 Micromeryx flourensianus Moschidae RUD135 p4 –14.1 –7.2 23.4 Micromeryx flourensianus Moschidae RUD130 m2 –14.6 –7.9 22.7 Micromeryx flourensianus Moschidae RUD1844 M3 –14.7 –2.3 28.5 Micromeryx flourensianus Moschidae RUD692 M2 –13.3 –2.6 28.2 Micromeryx flourensianus Moschidae RUD1613 P3 –13.3 –6.6 24.1 Aceratherium incisivum Rhinocerotidae MAFI1 M2 –10.2 –9.2 21.4 Aceratherium incisivum Rhinocerotidae MAFI2 m3 –10.1 –9.6 21 Aceratherium incisivum Rhinocerotidae MAFI3 M? –11.5 –8.9 21.7 Aceratherium incisivum Rhinocerotidae MAFI4 M3 –12.4 –9.1 21.5 Aceratherium incisivum Rhinocerotidae MAFI5 m? –12.3 –8.2 22.4 Tetralophodon longirostris Gomphotheriidae MAFI6 M3 -12.8 -8.4 22.2 Tetralophodon longirostris Gomphotheriidae MAFI7 m2 -12.7 -8.9 21.7 Dorcatherium naui Tragulidae RUD181 p2 -16.8 -6.2 24.5 Dorcatherium naui Tragulidae RUD1133 M3 -17 -5.9 24.8 Dorcatherium naui Tragulidae RUD1624 m2 -17 -6.1 24.6 Dorcatherium naui Tragulidae RUD1691 M2 -13.4 -5 25.7 Chalicotherium aff. goldfussi Chalicotheriidae RUD1479 M? -13.9 -4.7 26

157

Appendix B: Sr/Ca ratios of ungulate dental enamel samples from R. II. Specimen Sr/Ca x Species Family No. 1000 RUD1026 P. kretozii Suidae 1.25 RUD1673 P. kretozii Suidae 1.31 RUD668 P. kretozii Suidae 1.52 RUD543 P. kretozii Suidae 2.08 RUD1355 P. palaeochoerus Suidae 1.42 RUD1021 P. palaeochoerus Suidae 1.19 RUD1331 P. palaeochoerus Suidae 1.28 RUD1343 P. palaeochoerus Suidae 0.98 RUD1851 L. aff. pierensis Cervidae 1.26 RUD279 L. aff. pierensis Cervidae 1.15 RUD486 L. aff. pierensis Cervidae 0.67 RUD1547 L. aff. pierensis Cervidae 0.7 RUD695 L. aff. pierensis Cervidae 0.71 RUD579 L. aff. pierensis Cervidae 1.21 RUD1513 L. aff. pierensis Cervidae 0.6 RUD1011 L. aff. pierensis Cervidae 1.17 RUD154 L. aff. pierensis Cervidae 0.8 RUD1611 Miotragocerus sp. Bovidae 0.77 RUD1530 Miotragocerus sp. Bovidae 0.68 RUD167 Miotragocerus sp. Bovidae 0.6 RUD176 Miotragocerus sp. Bovidae 0.58 RUD377 Miotragocerus sp. Bovidae 1.13 RUD391 Miotragocerus sp. Bovidae 0.69 RUD699 Miotragocerus sp. Bovidae 1.2 RUD693 Miotragocerus sp. Bovidae 0.88 RUD1014 H. intrans Equidae 0.63 RUD804 H. intrans Equidae 0.62 RUD794 H. intrans Equidae 1.03 RUD139 H. intrans Equidae 0.84 RUD429 H. intrans Equidae 0.7 RUD628 H. intrans Equidae 0.94 RUD721 H. intrans Equidae 1.21 RUD728 H. intrans Equidae 1.06 MAFI6 T. longirostris Gomphotheriidae 0.73 MAFI7 T. longirostris Gomphotheriidae 0.8 RUD181 D. naui Tragulidae 0.45 RUD1133 D. naui Tragulidae 0.38 RUD1624 D. naui Tragulidae 0.64 RUD1691 D. naui Tragulidae 0.31 RUD130 M. flourensianus Moschidae 0.73

158

RUD1844 M. flourensianus Moschidae 0.58 RUD692 M. flourensianus Moschidae 0.46 RUD1613 M. flourensianus Moschidae 0.7 RUD1760 M. flourensianus Moschidae 0.67 RUD563 M. flourensianus Moschidae 0.48