Journal of Mammalian Evolution

, Volume 23, Issue 3, pp 221–235 | Cite as

Hyperspecialization in Some South American Endemic Ungulates Revealed by Long Bone Microstructure

  • Alexandra Houssaye
  • Vincent Fernandez
  • Guillaume Billet
Original Paper

Abstract

Adaptation to aquatic or semi-aquatic habits has been demonstrated in several distantly related mammalian clades worldwide during the Cenozoic, but curiously none has been conclusively evidenced inland for South America although a few South American native ungulates (SANU) have been proposed as possible subaquatic taxa. These taxa mostly correspond to large-sized herbivorous forms among astrapotheres, pyrotheres, and some toxodontid notoungulates, found at the end of the Paleogene and/or beginning of the Neogene. As no clear argument was provided for these ecological hypotheses, an analysis of the microanatomical features of long bones of some of these taxa in a comparative context was conducted in order to address the question of the paleoecology of these organisms. Our study highlights a variety of osseous specializations in the stylopod bones of SANU, and notably that Parastrapotherium, Pyrotherium, and Nesodon are affected by bone mass increase. If the microanatomical features of Parastrapotherium and Nesodon evoke what is observed in some terrestrial or semi-aquatic graviportal taxa, the very high compactness of Pyrotherium suggests extreme functional requirements in this taxon such as a graviportal hyperspecialization. This study thus evidences the occurrence of several convergent adaptations to graviportality and/or subaquatic habits within SANU and contributes to an important step towards a better integration of South American endemic mammals in large-scaled paleoecological studies.

Keywords

Bone mass increase Graviportality Microanatomy Ungulates South America 

Abbreviations

SANU

South American endemic native ungulates

Notes

Acknowledgments

We warmly thank C. Lefèvre, J. Lesur, V. Pernègre, and C. Argot (Muséum national d’Histoire naturelle, Paris, France), C. Norris, D. Brinkman, and M. Fox (Yale Peabody Museum, New Haven, USA) for the loan and packing of specimens, J.R. Hutchinson (Royal Veterinary College, London, United Kingdom) for the loan of some scans, Y Nakajima (Bonn Universität, Germany) for the loan of some sections, A. Kramarz (Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina) for helpful comments on astrapothere temporal distribution, and R. Cornette for fruitful advice with statistics. We thank the Steinmann Institut (University of Bonn, Germany) and the ESRF (Grenoble, France) for providing beamtime and support, the ESRF in the framework of the proposal ES-223 on the beamline ID17, UMS 2700 outils et méthodes de la systématique integrative CNRS-MNHN and AST-RX, Plateau technique d’accès scientifique à la tomographie à rayons X du MNHN, M. García-Sanz for performing the scans and reconstructions at the AST-RX platform (MNHN, Paris, France), P. Tafforeau for his help while performing the scans at the ESRF, and UMR 7207 CR2P MNHN CNRS UPMC-Paris6 for 3D imaging facilities. We warmly thank H. Woodward (Oklahoma State University, USA) and an anonymous reviewer for fruitful comments that improved our manuscript, and J.R. Wible for editorial work. A.H. acknowledges financial support from the ANR-13-PDOC-001 and the A. v. Humboldt Foundation.

Compliance with ethical standards

Authors’ Contributions

AH and G.B designed the study. AH, GB and VF participated to the data acquisition. AH conducted the analyses. AH and GB drafted the manuscript. All authors contributed to the final manuscript, read it and approved it.

References

  1. Ameghino F (1897) Mammifères crétacés de 1’Argentine. (Deuxième contribution à la connaissance de la faune mammalogique des couches à Pyrotherium). Bol Inst Geogr Argentina Buenos Aires 18:406–429,431–521Google Scholar
  2. Avilla LDS, Vizcaíno SF (2005) Locomotory pattern of Astrapotherium magnum (Owen) (Mammalia: Astrapotheria) from the Neomiocene (Colhuehuapian–Santacrucian) of Argentina. II Congresso Latino-Americano de Paleontologia de Vertebrados, Boletim de Resumos, p 44Google Scholar
  3. Bellosi ES (2010) Loessic and fluvial sedimentation in Sarmiento Formation pyroclastics, middle Cenozoic of central Patagonia. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 278–292Google Scholar
  4. Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13:166.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Billet G (2010) New observations on the skull of Pyrotherium (Pyrotheria, Mammalia) and new phylogenetic hypotheses on South American ungulates. J Mammal Evol 17: 21–59CrossRefGoogle Scholar
  6. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745CrossRefPubMedGoogle Scholar
  7. Boisserie J-R, Fisher RE, Lihoreau F, Weston EM (2011) Evolving between land and water: key questions on the emergence and history of the Hippopotamidae (Hippopotamoidea, Cetancodonta, Cetartiodactyla). Biol Rev 86:601–625CrossRefPubMedGoogle Scholar
  8. Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biol J Linn Soc 100:384–406CrossRefGoogle Scholar
  9. Carlson KJ, Stout D, Jashashvili T, De Ruiter DJ, Tafforeau P, Carlson K, Berger LR (2011) The endocast of MH1, Australopithecus sediba. Science 333:1402–1407CrossRefPubMedGoogle Scholar
  10. Cassini GH, Cerdeño E, Villafañe AL, Muñoz NA (2012b) Paleobiology of Santacrucian native ungulates (Meridiungulata: Astrapotheria, Litopterna, and Notoungulata). In: Vizcaíno SF, Kay RF, Bargo MS (eds) Early Miocene Paleobiology in Patagonia: High-Latitude Paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 243–286CrossRefGoogle Scholar
  11. Cassini GH, Vizcaíno S, Bargo M (2012a) Body mass estimation in early Miocene native South American ungulates: a predictive equation based on 3D landmarks. J Zool 287:53–64CrossRefGoogle Scholar
  12. Charles C, Solé F, Rodrigues HG, Viriot L (2013) Under pressure? Dental adaptations to termitophagy and vermivory among mammals. Evolution 67:1792–1804CrossRefPubMedGoogle Scholar
  13. Coombs WP (1975) Sauropod habits and habitats. Palaeogeogr Palaeoclimatol Palaeoecol 17:1–33CrossRefGoogle Scholar
  14. Cifelli RL (1985) South American ungulate evolution and extinction. In: Stehli FG, Webb SD (eds) The Great American Biotic Interchange. Topics in Geobiology. Plenum Press, New York, pp 249–266.Google Scholar
  15. Cornette R, Herrel A, Stoetzel E, Moulin S, Hutterer R, Denys C, Baylac M (2015) Specific information levels in relation to fragmentation patterns of shrew mandibles: do fragments tell the same story? J Archaeol Sci 53:323–330CrossRefGoogle Scholar
  16. Croft DA (2001) Cenozoic environmental change in South America as indicated by mammalian body size distributions (cenograms). Divers Distrib 7:271–287CrossRefGoogle Scholar
  17. Croft DA, Radic JP, Zurita E, Charrier R, Flynn JJ, Wyss AR (2003) A Miocene toxodontid (Mammalia: Notoungulata) from the sedimentary series of the Cura-Mallín Formation, Lonquimay, Chile. Revista Geológica de Chile 30:285–298Google Scholar
  18. Domning DP (1997) Sirenia. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, DC, pp 383–391Google Scholar
  19. Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ (2010) BoneJ: free and extensible bone image analysis in ImageJ. Bone 47:1076–1079CrossRefPubMedPubMedCentralGoogle Scholar
  20. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  21. Fish FE (2001) A mechanism for evolutionary transition in swimming mode by mammals. In: Mazin JM, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 261–282Google Scholar
  22. Flynn J, Charrier R, Croft D, Wyss A (2012) Cenozoic Andean faunas: shedding new light on South American mammal evolution, biogeography, environments, and tectonics. In: Patterson BD, Costa LP (eds) Bones, Clones, and Biomes: the History and Geography of Recent Neotropical Mammals. The University of Chicago Press, Chicago and London, pp 51–75Google Scholar
  23. Forasiepi AM, Cerdeño E, Bond M, Schmidt GI, Naipauer M, Straehl FR, Martinelli AG, Garrido AC, Schmitz MD, Crowley JL (2014) New toxodontid (Notoungulata) from the early Miocene of Mendoza, Argentina. Paläontol Z 89: 611–634CrossRefGoogle Scholar
  24. Gaudry A (1909) Fossiles de Patagonie: le Pyrotherium. Masson, Paris, pp 1–28Google Scholar
  25. Germain D, Laurin M (2005) Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool Scr 34:335–350CrossRefGoogle Scholar
  26. Gheerbrant E, Tassy P (2009) L’origine et l’évolution des éléphants. CR Palevol 8:281–294.CrossRefGoogle Scholar
  27. Gilbert C, Ropiquet A, Hassanin A (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography. Mol Phylogenet Evol 40:101–117CrossRefPubMedGoogle Scholar
  28. Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleontol 23:458–461CrossRefGoogle Scholar
  29. Goillot C, Antoine P-O, Tejada J, Pujos F, Gismondi RS (2011) Middle Miocene Uruguaytheriinae (Mammalia, Astrapotheria) from Peruvian Amazonia and a review of the astrapotheriid fossil record in northern South America. Geodiversitas 33:331–345CrossRefGoogle Scholar
  30. Harmon LJ, Kolbe JJ, Cheverud JM, Losos JB (2005) Convergence and the multidimensional niche. Evolution 59:409–421CrossRefPubMedGoogle Scholar
  31. Hayashi S, Carpenter K, Scheyer TM, Watabe M, Suzuki D (2010) Function and evolution of ankylosaur dermal armor. Acta Palaeontol Pol 55:213–228CrossRefGoogle Scholar
  32. Hayashi S, Houssaye A, Nakajima Y, Chiba K, Ando T, Sawamura H, Inuzuka N, Kaneko N, Osaki T (2013) Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). PLoS ONE 8:e59146CrossRefPubMedPubMedCentralGoogle Scholar
  33. Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integr Zool 4:325–340CrossRefPubMedGoogle Scholar
  34. Houssaye A, Lindgren J, Pellegrini R, Lee AH, Germain D, Polcyn MJ (2013) Microanatomical and histological features in the long bones of mosasaurine mosasaurs (Reptilia, Squamata)–implications for aquatic adaptation and growth rates. PloS ONE 8:e76741CrossRefPubMedPubMedCentralGoogle Scholar
  35. Houssaye A, Scheyer TM, Kolb C, Fischer V, Sander PM (2014) A new look at ichthyosaur long bone microanatomy and histology: implications for their adaptation to an aquatic life. PLoS ONE 9:e95637CrossRefPubMedPubMedCentralGoogle Scholar
  36. Houssaye A., Tafforeau P, Muizon C de, Gingerich PD (2015) Transition of Eocene whales from land to sea: evidence from bone microstructure. PloS ONE 10: e0118409Google Scholar
  37. Houssaye A, Waskow K, Hayashi S, Cornette R, Lee AH, Hutchinson JR (In press) Biomechanical evolution of solid bones in large animals: a microanatomical investigation. Biol J Linn SocGoogle Scholar
  38. Johnson SC, Madden RH (1997) Uruguaytheriine astrapotheres of tropical South America. In: Kay RF, Madden RH, Cifelli RL, Flynn JJ (eds) Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Colombia. Smithsonian Institution Press, Washington, DC, pp 355–382Google Scholar
  39. Kay RF, MacFadden BJ, Madden RH, Sandeman H, Anaya F (1998) Revised age of the Salla beds, Bolivia, and its bearing on the age of the Deseadan South American Land Mammal “Age.” J Vertebr Paleontol 18:189–199CrossRefGoogle Scholar
  40. Kay RF, Williams BA, Anaya F (2002) The adaptations of Branisella boliviana, the earliest South American monkey. In: Plavcan JM, Kay RF, Jungers WL, van Schaik CP (eds) Reconstructing Behavior in the Primate Fossil Record. Kluwer Academic/Plenum Publishers, New York, pp 339–370CrossRefGoogle Scholar
  41. Klein N, Houssaye A, Neenan JM, Scheyer TM (2015) Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia). Contrib Zool 84:59–84Google Scholar
  42. Kramarz AG, Bond M (2008) Revisión de Parastrapotherium (Mammalia, Astrapotheria) y otros astrapoterios Deseadenses de Patagonia. Ameghiniana 45:537–551Google Scholar
  43. Kramarz A, Bond M (2011) A new early Miocene astrapotheriid (Mammalia, Astrapotheria) from northern Patagonia, Argentina. Neues Jahrbuch für Geologie und Paläontologie - Abhandlungen 260:277–287CrossRefGoogle Scholar
  44. Kramarz AG, Bond M, Forasiepi AM (2011) New remains of Astraponotus (Mammalia, Astrapotheria) and considerations on astrapothere cranial evolution. Paläontol Z 85:185–200CrossRefGoogle Scholar
  45. Kriloff A, Germain D, Canoville A, Vincent P, Sache M, Laurin M (2008) Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference. J Evol Biol 21:807–826CrossRefPubMedGoogle Scholar
  46. Laurin M, Girondot M, Loth M-M (2004) The evolution of long bone microstructure and lifestyle in lissamphibians. Paleobiology 30:589–613CrossRefGoogle Scholar
  47. Lavocat R (1958) Classification des ongulés d’après leur origine et leur évolution. Mammalia 22:28–44CrossRefGoogle Scholar
  48. Loomis FB (1914) The Deseado Formation of Patagonia. Amherst College, Amherst, 232ppGoogle Scholar
  49. MacFadden BJ (2005) Diet and habitat of toxodont megaherbivores (Mammalia, Notoungulata) from the late Quaternary of South and Central America. Quaternary Res 64:113–124CrossRefGoogle Scholar
  50. MacFadden BJ (2006) Extinct mammalian biodiversity of the ancient New World tropics. Trends Ecol Evol 21:157–165CrossRefPubMedGoogle Scholar
  51. MacFadden BJ, Shockey BJ (1997) Ancient feeding ecology and niche differentiation of Pleistocene mammalian herbivores from Tarija, Bolivia: morphological and isotopic evidence. Paleobiology 23:77–100CrossRefGoogle Scholar
  52. MacFadden BJ, Campbell Jr, KE, Cifelli RL, Siles O, Johnson NM, Naeser CW, Zeitler PK (1985) Magnetic polarity stratigraphy and mammalian fauna of the Deseadan (late Oligocene-early Miocene) Salla beds of northern Bolivia. J Geol 223–250Google Scholar
  53. Marshall LG, Salinas P, Suárez M (1990) Astrapotherium sp.(Mammalia, Astrapotheriidae) from Miocene strata along the Quepuca River, central Chile. Rev Geol Chile, 17:215–223Google Scholar
  54. McKenna MC, Bell SK (1997) Classification of Mammals Above the Species Level. Columbia University Press, New York, 631ppGoogle Scholar
  55. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T (2011) Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334:521–524CrossRefPubMedGoogle Scholar
  56. Miquel SE, Bellosi ES (2010) Middle Eocene–Oligocene gastropods of the Sarmiento Formation, central Patagonia. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 61–68Google Scholar
  57. Mirone A, Brun E, Gouillart E, Tafforeau P, Kieffer J (2014) The PyHST2 hybrid distributed code for high speed tomographic reconstruction with iterative reconstruction and a priori knowledge capabilities. Nucl Instrum Methods Phys Res Sect B Beam Interact Mater At 324:41–48CrossRefGoogle Scholar
  58. Muizon C de, McDonald HG (1995) An aquatic sloth from the Pliocene of Peru. Nature 375:224–227Google Scholar
  59. Nakajima Y, Hirayama R, Endo H (2014) Turtle humeral microanatomy and its relationship to lifestyle. Biol J Linn Soc 112:719–734.CrossRefGoogle Scholar
  60. Nowak RM (1999). Walker’s Mammals of the World (Vol. 2), 6th Edition. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  61. Ortiz-Jaureguizar E, Cladera G (2006) Paleoenvironmental evolution of southern South America during the Cenozoic. J Arid Environ 66:498–532CrossRefGoogle Scholar
  62. Osborn HF (1929) The Titanotheres of Ancient Wyoming, Dakota, and Nebraska. Government Printing Office, Washington, pp 1–953Google Scholar
  63. Palazzesi L, Barreda V (2012) Fossil pollen records reveal a late rise of open-habitat ecosystems in Patagonia. Nat Commun 3:1294CrossRefPubMedGoogle Scholar
  64. Pascual R, Jaureguizar EO (1990) Evolving climates and mammal faunas in Cenozoic South America. J Hum Evol 19:23–60CrossRefGoogle Scholar
  65. Pascual R, Ortiz-Jaureguizar E (2007) The Gondwanan and South American episodes: two major and unrelated moments in the history of the South American mammals. J Mammal Evol 14:75–137CrossRefGoogle Scholar
  66. Paula Couto C de (1979) Tratado de paleomastozoologia. Academia Brasileira de Ciências, Rio de Janeiro, 590ppGoogle Scholar
  67. Quemeneur S, Buffrénil V de, Laurin M (2013) Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Biol J Linn Soc 109:644–655Google Scholar
  68. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  69. Reguero MA, Prevosti FJ (2010) Rodent-like notoungulates (Typotheria) from Gran Barranca, Chubut Province, Argentina: phylogeny and systematics. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 148–165Google Scholar
  70. Ricqlès A de, Buffrénil V de (2001) Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In: Mazin JM, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 289–310Google Scholar
  71. Riggs ES (1935) A skeleton of Astrapotherium. Geol Ser Field Mus Nat Hist 6:167–176Google Scholar
  72. Salas R, Sánchez J, Chacaltana C (2006) A new pre-Deseadan pyrothere (Mammalia) from northern Peru and the wear facets of molariform teeth of Pyrotheria. J Vertebr Paleontol 26:760–769CrossRefGoogle Scholar
  73. Sanchez S, Fernandez V, Pierce SE, Tafforeau P (2013) Homogenization of sample absorption for the imaging of large and dense fossils with synchrotron microtomography. Nat Protoc 8:1708–1717CrossRefPubMedGoogle Scholar
  74. Sánchez-Villagra MR, Aguilera O, Horovitz I (2003) The anatomy of the world’s largest extinct rodent. Science 301:1708–1710CrossRefPubMedGoogle Scholar
  75. Sánchez-Villagra MR, Asher RJ, Rincón AD, Carlini AA, Meylan P, Purdy AW (2004) New faunal reports for the Cerro La Cruz locality (lower Miocene), north-western Venezuela. In: Sánchez-Villagra MR, Clack JA (eds) Fossils of the Miocene Castillo Formation, Venezuela: Contributions in Neotropical Palaeontology. The Palaeontological Society, Special Papers in Palaeontology No. 71, pp. 105–112Google Scholar
  76. Scott WB (1913) Land Mammals in the Western Hemisphere. Macmillan, New York, 786ppGoogle Scholar
  77. Scott WB (1937) The Astrapotheria. Proc Am Phil Soc 77:309–393Google Scholar
  78. Sefve I (1923) Macrauchenia patagonica. Bull Geol Inst Univ Upsala 19:1–21Google Scholar
  79. Shockey BJ (1999) Postcranial osteology and functional morphology of the Litopterna of Salla, Bolivia (late Oligocene). J Vertebr Paleontol 19:383–390CrossRefGoogle Scholar
  80. Shockey BJ (2001) Specialized knee joints in some extinct, endemic, South American herbivores. Acta Palaeontol Pol 46:277–288Google Scholar
  81. Shockey BJ (2005) New leontiniids (Class Mammalia, Order Notoungulata, Family Leontiniidae) from the Salla Beds of Bolivia (Deseadan, late Oligocene). Bull Florida Mus Nat Hist 45:249–260Google Scholar
  82. Shockey BJ, Anaya F (2008) Postcranial osteology of mammals from Salla, Bolivia (late Oligocene): form, function, and phylogenetic implications. In: Sargis EJ, Dagosto M (eds) Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay. Springer, Dordrecht, pp 135–157CrossRefGoogle Scholar
  83. Shockey BJ, Anaya FD (2004) Pyrotherium macfaddeni, sp. nov. (late Oligocene, Bolivia) and the pedal morphology of pyrotheres. J Vertebr Paleontol 24:481–488CrossRefGoogle Scholar
  84. Simpson GG (1980) Splendid Isolation: The Curious History of South American Mammals. Yale University Press, New Heaven, 266ppGoogle Scholar
  85. Steiner CC, Ryder OA (2011) Molecular phylogeny and evolution of the Perissodactyla. Zool J Linn Soc 163:1289–1303CrossRefGoogle Scholar
  86. Strömberg CA, Dunn RE, Madden RH, Kohn MJ, Carlini AA (2013) Decoupling the spread of grasslands from the evolution of grazer-type herbivores in South America. Nat Commun 4:1478CrossRefPubMedGoogle Scholar
  87. Todd NE (2010) New phylogenetic analysis of the family elephantidae based on cranial-dental morphology. Anat Rec 293:74–90CrossRefGoogle Scholar
  88. Uhen MD (2010) The origin(s) of whales. Annu Rev Earth Planet Sci 38:189–219CrossRefGoogle Scholar
  89. Veron G, Patterson BD, Reeves R (2008) Global diversity of mammals (Mammalia) in freshwater. Hydrobiologia 595:607–617CrossRefGoogle Scholar
  90. Vizcaíno SF, Bargo MS, Kay RF, Fariña RA, Di Giacomo M, Perry JM, Prevosti FJ, Toledo N, Cassini GH, Fernicola JC (2010) A baseline paleoecological study for the Santa Cruz Formation (late–early Miocene) at the Atlantic coast of Patagonia, Argentina. Palaeogeogr Palaeoclimatol Palaeoecol 292:507–519CrossRefGoogle Scholar
  91. Vizcaíno SF, Cassini GH, Toledo N, Bargo MS (2012) On the evolution of large size in mammalian herbivores of Cenozoic. In: Patterson BP, Costa LP (eds) Bones, Clones and Biomes: an 80-million year History of Recent Neotropical Mammals. The University of Chicago Press, Chicago and London, pp 76–101Google Scholar
  92. Vucetich GM, Deschamps CM, Vieytes EC, Montalvo CI (2014) Late Miocene capybaras from Argentina: skull anatomy, taxonomy, evolution, and biochronology. Acta Palaeontol Pol 59:517–535Google Scholar
  93. Walker A, Ryan TM, Silcox MT, Simons EL, Spoor F (2008) The semicircular canal system and locomotion: the case of extinct lemuroids and lorisoids. Evol Anthropol Issues News Rev 17:135–145CrossRefGoogle Scholar
  94. Webb SD (1978). A history of savanna vertebrates in the New World. Part II: South America and the Great Interchange. Annu Rev Ecol Syst 9:393–426CrossRefGoogle Scholar
  95. Welker CA, Souza-Chies TT, Longhi-Wagner HM, Peichoto MC, McKain MR, Kellogg EA (2015) Phylogenetic analysis of Saccharum sl (Poaceae; Andropogoneae), with emphasis on the circumscription of the South American species. Am J Bot 102:248–263CrossRefPubMedGoogle Scholar
  96. Weston EM, Madden RH, Sánchez-Villagra MR (2004) Early Miocene astrapotheres (Mammalia) from northern South America. In: Sánchez-Villagra MR, Clack JA (eds) Fossils of the Miocene Castillo Formation, Venezuela: Contributions on Neotropical Palaeontology. The Palaeontological Society, Special Papers in Palaeontology, No. 71, pp 81–97Google Scholar
  97. Wilf P, Cúneo NR, Escapa IH, Pol D, Woodburne MO (2013) Splendid and seldom isolated: the paleobiogeography of Patagonia. Annu Rev Earth Planet Sci 41:561CrossRefGoogle Scholar
  98. Williams TM, Worthy GA (2002) Anatomy and physiology: the challenge of aquatic living. In: Hoelzel AR (ed) Marine Mammal Biology: An Evolutionary Approach. Blackwell Science, Oxford, pp 73–97Google Scholar
  99. Woodburne MO, Goin FJ, Bond M, Carlini AA, Gelfo JN, López GM, Iglesias A, Zimicz AN (2014) Paleogene land mammal faunas of South America; a response to global climatic changes and indigenous floral diversity. J Mammal Evol 21:1–73CrossRefGoogle Scholar
  100. Wroe S, Chamoli U, Parr W, Clausen P, Ridgely R, Evans AR (2013) Comparative biomechanical modeling of metatherian and placental saber-tooths: a. different kind of bite for an extreme pouched predator. PLoS ONE 8(6):e66888CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Alexandra Houssaye
    • 1
  • Vincent Fernandez
    • 2
  • Guillaume Billet
    • 3
  1. 1.Département Ecologie et Gestion de la BiodiversitéUMR 7179 CNRS/Muséum National d’Histoire NaturelleParisFrance
  2. 2.European Synchrotron Radiation FacilityGrenobleFrance
  3. 3.CR2P, UMR CNRS 7207, CP 38, Muséum national d’Histoire naturelleParisFrance

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