The Science of Nature

, 105:28 | Cite as

Phylogenetic and functional implications of the ear region anatomy of Glossotherium robustum (Xenarthra, Mylodontidae) from the Late Pleistocene of Argentina

  • Alberto Boscaini
  • Dawid A. Iurino
  • Guillaume Billet
  • Lionel Hautier
  • Raffaele Sardella
  • German Tirao
  • Timothy J. Gaudin
  • François Pujos
Original Paper

Abstract

Several detailed studies of the external morphology of the ear region in extinct sloths have been published in the past few decades, and this anatomical region has proved extremely helpful in elucidating the phylogenetic relationships among the members of this mammalian clade. Few studies of the inner ear anatomy in these peculiar animals were conducted historically, but these are increasing in number in recent years, in both the extinct and extant representatives, due to wider access to CT-scanning facilities, which allow non-destructive access to internal morphologies. In the present study, we analyze the extinct ground sloth Glossotherium robustum and provide a description of the external features of the ear region and the endocranial side of the petrosal bone, coupled with the first data on the anatomy of the bony labyrinth. Some features observable in the ear region of G. robustum (e.g., the shape and size of the entotympanic bone and the morphology of the posteromedial surface of the petrosal) are highly variable, both intraspecifically and intraindividually. The form of the bony labyrinth of G. robustum is also described, providing the first data from this anatomical region for the family Mylodontidae. The anatomy of the bony labyrinth of the genus Glossotherium is here compared at the level of the superorder Xenarthra, including all available extant and extinct representatives, using geometric morphometric methods. In light of the new data, we discuss the evolution of inner ear anatomy in the xenarthran clade, and most particularly in sloths, considering the influence of phylogeny, allometry, and physiology on the shape of this highly informative region of the skull. These analyses show that the inner ear of Glossotherium more closely resembles that of the extant anteaters, and to a lesser extent those of the giant ground sloth Megatherium and euphractine armadillos, than those of the extant sloths Bradypus and Choloepus, further demonstrating the striking morphological convergence between the two extant sloth genera.

Keywords

Glossotherium Ground sloth Ear region Bony labyrinth Phylogeny Function 

Abbreviations

FMNH

Field Museum of Natural History (Chicago, USA)

FUESMEN

Fundación Escuela de Medicina Nuclear (Mendoza, Argentina)

MACN Pv

Colección de Paleontología de Vertebrados, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (Buenos Aires, Argentina)

MLP

División Paleontología de Vertebrados, Museo de La Plata (La Plata, Argentina)

ROM

Royal Ontario Museum (Toronto, Canada)

Notes

Acknowledgments

We are grateful to the FUESMEN institute (Fundación Escuela de Medicina Nuclear, Mendoza, Argentina) for access to CT-scanning facilities, and we are particularly indebted to Sergio Mosconi and collaborators for assistance with image processing. We thank A. Kramarz, S.M. Alvarez and L. Chornogubsky (MACN, Buenos Aires, Argentina) and M. Reguero, S.C. Scarano and M.L. de los Reyes (MLP, La Plata, Argentina), who kindly gave access to the specimens under their care. We thank the PaleoFactory Lab (Sapienza Università di Roma, Italy) for access to their facilities, without which this work would not have been possible. We also thank M. Fernández-Monescillo, S. Hernández del Pino and A. Forasiepi (IANIGLA, CCT-CONICET-Mendoza, Argenina) for their useful suggestions. This paper greatly benefited from the careful reading and thoughtful comments by the editor S. Thatje, Prof. G. De Iuliis and other two anonymous reviewers.

Supplementary material

114_2018_1548_MOESM1_ESM.pdf (2.8 mb)
ESM 1 (PDF 2829 kb)

References

  1. Ameghino F (1902) Notas sobre algunos mamíferos fósiles, nuevos ó poco conocidos del valle de Tarija. Anales Mus Nac Hist Nat Buenos Aires 8:225–261Google Scholar
  2. Bargo MS, Toledo N, Vizcaíno SF (2006) Muzzle of south American Pleistocene ground sloths (Xenarthra, Tardigrada). J Morphol 267:248–263CrossRefPubMedGoogle Scholar
  3. Bargo MS, Vizcaíno SF (2008) Paleobiology of Pleistocene ground sloths (Xenarthra, Tardigrada): biomechanics, morphogeometry and ecomorphology applied to the masticatory apparatus. Ameghiniana 45(1):175–196Google Scholar
  4. Benoit J, Essid EM, Marzougui W, Ammar HK, Lebrun R, Tabuce R, Marivaux L (2013) New insights into the ear region anatomy and cranial blood supply of advanced stem Strepsirhini: evidence from three primate petrosals from the Eocene of Chambi, Tunisia. J Hum Evol 65(5):551–572CrossRefPubMedGoogle Scholar
  5. Berlin JC, Kirk EC, Rowe TB (2013) Functional implications of ubiquitous semicircular canal non-orthogonality in mammals. PLoS One 8(11):e79585CrossRefPubMedPubMedCentralGoogle Scholar
  6. Billet G, Hautier L, Asher RJ, Schwarz C, Crumpton N, Martin T, Ruf I (2012) High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths. Proc R Soc B 279:3932–3939CrossRefPubMedPubMedCentralGoogle Scholar
  7. Billet G, Germain D, Ruf I, de Muizon C, Hautier L (2013) The inner ear of Megatherium and the evolution of the vestibular system in sloths. J Anat 223(6):557–567CrossRefPubMedPubMedCentralGoogle Scholar
  8. Billet G, Hautier L, Lebrun R (2015a) Morphological diversity of the bony labyrinth (inner ear) in extant xenarthrans and its relation to phylogeny. J Mammal 96(4):658–672CrossRefGoogle Scholar
  9. Billet G, de Muizon C, Schellhorn R, Ruf I, Ladevèze S, Bergqvist L (2015b) Petrosal and inner ear anatomy and allometry amongst specimens referred to Litopterna (Placentalia). Zool J Linn Soc 173(4):956–987CrossRefGoogle Scholar
  10. Blanco RE, Rinderknecht A (2008) Estimation of hearing capabilities of Pleistocene ground sloths (Mammalia, Xenarthra) from middle-ear anatomy. J Vertebr Paleontol 28(1):274–276CrossRefGoogle Scholar
  11. Blanco RE, Rinderknecht A (2012) Fossil evidence of frequency range of hearing independent of body size in South American Pleistocene ground sloths (Mammalia, Xenarthra). C R Palevol 11(8):549–554CrossRefGoogle Scholar
  12. Clack AA, MacPhee RD, Poinar HN (2012) Mylodon darwinii DNA sequences from ancient fecal hair shafts. Ann Anat 194(1):26–30CrossRefPubMedGoogle Scholar
  13. Cope ED (1889) The Edentata of North America. Am Nat 23(272):657–664CrossRefGoogle Scholar
  14. Coutier F, Hautier L, Cornette R, Amson E, Billet G (2017) Orientation of the lateral semicircular canal in Xenarthra and its links with head posture and phylogeny. J Morphol 278(5):704–717CrossRefPubMedGoogle Scholar
  15. Danilo L, Remy J, Vianey-Liaud M, Mérigeaud S, Lihoreau F (2015) Intraspecific variation of endocranial structures in extant Equus: a prelude to endocranial studies in fossil equoids. J Mamm Evol 22(4):561–582CrossRefGoogle Scholar
  16. David R, Droulez J, Allain R, Berthoz A, Janvier P, Bennequin D (2010) Motion from the past. A new method to infer vestibular capacities of extinct species. C R Palevol 9(6):397–410CrossRefGoogle Scholar
  17. David R, Stoessel A, Berthoz A, Spoor F, Bennequin D (2016) Assessing morphology and function of the semicircular duct system: introducing new in-situ visualization and software toolbox. Sci Rep 6:32772CrossRefPubMedPubMedCentralGoogle Scholar
  18. De Iuliis G (2017) Recent progress and future prospects in fossil xenarthran studies, with emphasis on current methodology in sloth taxonomy. J Mamm Evol DOI.  https://doi.org/10.1007/s10914-017-9407-8
  19. De Iuliis G, Gaudin TJ, Vicars M (2011) A new genus and species of Nothrotheriid sloth (Xenarthra, Tardigrada, Nothrotheriidae) from the Late Miocene (Huayquerian) of Peru. Palaeontology 54(1):171–205CrossRefGoogle Scholar
  20. De Iuliis G, Cartelle C, McDonald HG, Pujos F (2017) The mylodontine ground sloth Glossotherium tropicorum from the Late Pleistocene of Ecuador and Peru. Pap Palaeontol 3:613–636CrossRefGoogle Scholar
  21. Delsuc F, Catzeflis FM, Stanhope MJ, Douzery EJ (2001) The evolution of armadillos, anteaters and sloths depicted by nuclear and mitochondrial phylogenies: implications for the status of the enigmatic fossil Eurotamandua. Proc R Soc B 268(1476):1605–1615CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ekdale EG (2013) Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PLoS One 8(6):e66624CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ekdale EG (2016) Form and function of the mammalian inner ear. J Anat 228(2):324–337CrossRefPubMedGoogle Scholar
  24. Ekdale EG, Racicot RA (2015) Anatomical evidence for low frequency sensitivity in an archaeocete whale: comparison of the inner ear of Zygorhiza kochii with that of crown Mysticeti. J Anat 226(1):22–39CrossRefPubMedGoogle Scholar
  25. Ekdale EG, Rowe T (2011) Morphology and variation within the bony labyrinth of zhelestids (Mammalia, Eutheria) and other therian mammals. J Vertebr Paleontol 31(3):658–675CrossRefGoogle Scholar
  26. Esteban GI (1996) Revisión de los Mylodontinae cuaternarios (Edentata-Tardigrada) de Argentina, Bolivia y Uruguay. Sistemática, filogenia, paleobiología, paleozoogeografía y paleoecología. Dissertation, Universidad Nacional de TucumánGoogle Scholar
  27. Fariña RA, Vizcaíno SF, Bargo MS (1998) Body mass estimations in Lujanian (late Pleistocene-early Holocene of South America) mammal megafauna. Mastozool Neotrol 5(2):87–108Google Scholar
  28. Fariña RA, Vizcaíno SF (2003) Slow moving or browsers? A note on nomenclature. Senckenb Biol 83(1):3–4Google Scholar
  29. Fernicola JC, Vizcaíno SF, De Iuliis G (2009) The fossil mammals collected by Charles Darwin in South America during his travels on board the HMS Beagle. Rev Asoc Geol Argent 64(1):147–159Google Scholar
  30. Flower W (1883) On the arrangement of the orders and families of existing Mammalia. Proc Zool Soc Lond 1883:178–186Google Scholar
  31. Gaudin TJ (1995) The ear region of edentates and the phylogeny of the Tardigrada (Mammalia, Xenarthra). J Vertebr Paleontol 15(3):672–705CrossRefGoogle Scholar
  32. Gaudin TJ (2004) Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zool J Linnean Soc 140(2):255–305CrossRefGoogle Scholar
  33. Gaudin TJ (2011) On the osteology of the auditory region and orbital wall in the extinct west Indian sloth genus Neocnus Arredondo, 1961 (Placentalia, Xenarthra, Megalonychidae). Ann Carnegie Mus 80(1):5–28CrossRefGoogle Scholar
  34. Gaudin TJ, Biewener AA (1992) The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra). J Morphol 214(1):63–81CrossRefPubMedGoogle Scholar
  35. Gaudin TJ, Wible JR (2006) The phylogeny of living and extinct armadillos (Mammalia, Xenarthra, Cingulata): a craniodental analysis. In: Carrano MT, Gaudin TJ, Blob RW, Wible JR (eds) Amniote paleobiology: perspectives on the evolution of mammals, birds and reptiles. University of Chicago Press, Chicago, pp 153–198Google Scholar
  36. Gaudin TJ, Croft DA (2015) Paleogene Xenarthra and the evolution of South American mammals. J Mammal 96(4):622–634CrossRefGoogle Scholar
  37. Gaudin TJ, De Iuliis G, Toledo N, Pujos F (2015) The basicranium and orbital region of the early Miocene Eucholoeops ingens Ameghino, (Xenarthra, Pilosa, Megalonychidae). Ameghiniana 52(2):226–240CrossRefGoogle Scholar
  38. Gill T (1872) Arrangement of the families of mammals, with analytical tables. Smithson Misc Collect 11:1–98Google Scholar
  39. Gosselin-Ildari AD (2006) Functional morphology of the bony labyrinth in primates. The University of Texas at Austin, DissertationGoogle Scholar
  40. Greenwood AD, Castresana J, Feldmaier-Fuchs G, Pääbo S (2001) A molecular phylogeny of two extinct sloths. Mol Phylogenet Evol 18(1):94–103CrossRefPubMedGoogle Scholar
  41. Guth C (1961) La région temporale des Edentés. Université de Paris, DissertationGoogle Scholar
  42. Illiger K (1811) Prodromus systematis mammalium et avium. C. Salfeld, BerlinGoogle Scholar
  43. Jones MG, Spells KE (1963) A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc R Soc B 157(968):403–419CrossRefGoogle Scholar
  44. van der Klaauw CJ (1931) On the tympanic region of the skull in the Mylodontidae. Proc Zool Soc Lond 1931:607–655Google Scholar
  45. Lebrun R (2008) Evolution and development of the strepsirrhine primate skull. Université Montpellier II and University of Zürich, DissertationGoogle Scholar
  46. Lebrun R (2014) ISE-MeshTools software. http://morphomuseum.com/meshtools
  47. Lebrun R, de León MP, Tafforeau P, Zollikofer C (2010) Deep evolutionary roots of strepsirrhine primate labyrinthine morphology. J Anat 216(3):368–380CrossRefPubMedGoogle Scholar
  48. Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, 10th edn, vol 1. Holmiae, StockholmGoogle Scholar
  49. Lydekker R (1894) The extinct edentates of Argentina. An Mus La Plata 3(2):1–118Google Scholar
  50. Macrini TE, Flynn JJ, Ni X, Croft DA, Wyss AR (2013) Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters. J Anat 223(5):442–461PubMedPubMedCentralGoogle Scholar
  51. Malinzak MD, Kay RF, Hullar TE (2012) Locomotor head movements and semicircular canal morphology in primates. Proc Natl Acad Sci U S A 109(44):17914–17919CrossRefPubMedPubMedCentralGoogle Scholar
  52. Manoussaki D, Chadwick RS, Ketten DR, Arruda J, Dimitriadis EK, O'Malley JT (2008) The influence of cochlear shape on low-frequency hearing. Proc Natl Acad Sci U S A 105(16):6162–6166CrossRefPubMedPubMedCentralGoogle Scholar
  53. McAfee RK (2009) Reassessment of the cranial characters of Glossotherium and Paramylodon (Mammalia: Xenarthra: Mylodontidae). Zool J Linnean Soc 155(4):885–903CrossRefGoogle Scholar
  54. McKenna MC, Bell SK (1997) Classification of mammals above the species level. Columbia University Press, New YorkGoogle Scholar
  55. Mones A (1986) Palaeovertebrata Sudamericana. Catálogo sistemático de los vertebrados fósiles de América del Sur. Parte I. Lista preliminar y bibliografía. Cour Forsch Inst Senckenberg 82:1–625Google Scholar
  56. Muller M (1999) Size limitations in semicircular duct systems. J Theor Biol 198(3):405–437CrossRefPubMedGoogle Scholar
  57. Nyakatura JA (2012) The convergent evolution of suspensory posture and locomotion in tree sloths. J Mamm Evol 19(3):225–234CrossRefGoogle Scholar
  58. Orliac MJ, Benoit J, O'Leary MA (2012) The inner ear of Diacodexis, the oldest artiodactyl mammal. J Anat 221(5):417–426CrossRefPubMedPubMedCentralGoogle Scholar
  59. Orliac MJ, O’Leary MA (2016) The inner ear of Protungulatum (pan-Euungulata, Mammalia). J Mamm Evol 23(4):337–352CrossRefGoogle Scholar
  60. Owen FRS (1840) Fossil Mammalia. In: Darwin C (ed) The zoology of the voyage of the Beagle. Smith, Elder and Co., London, pp 13–111Google Scholar
  61. Owen FRS (1842) Description of the skeleton of an extinct gigantic sloth, Mylodon robustus, Owen, with observations on the osteology, natural affinities, and probable habits of the megatheroid quadrupeds in general. Direction of the Council, LondonGoogle Scholar
  62. Patterson B, Segall W, Turnbull WD (1989) The ear region in xenarthrans (= Edentata: Mammalia). Part I. Cingulates. Fieldiana Geol 18:1–46Google Scholar
  63. Patterson B, Turnbull WD, Segall W, Gaudin TJ (1992) The ear region in xenarthrans (= Edentata: Mammalia). Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana Geol 24:1–78Google Scholar
  64. Perier A, Lebrun R, Marivaux L (2016) Different level of intraspecific variation of the bony labyrinth morphology in slow- versus fast-moving primates. J Mamm Evol 23(4):353–368CrossRefGoogle Scholar
  65. Pitana VG, Esteban GI, Ribeiro AM, Cartelle C (2013) Cranial and dental studies of Glossotherium robustum (Owen, 1842) (Xenarthra: Pilosa: Mylodontidae) from the Pleistocene of southern Brazil. Alcheringa 37(2):147–162CrossRefGoogle Scholar
  66. Pujos F, De Iuliis G (2007) Late Oligocene Megatherioidea Fauna (Edentata: Xenarthra) from Salla-Luribay (Bolivia): new data on basal sloth radiation and Cingulata-Phyllophaga split. J Vertebr Paleontol 27(1):132–144CrossRefGoogle Scholar
  67. Pujos F, De Iuliis G, Cartelle C (2017) A paleogeographic overview of tropical fossil sloths: towards an understanding of the origin of extant suspensory sloths? J Mamm Evol 24(1):1–20CrossRefGoogle Scholar
  68. Pujos F, Gaudin TJ, De Iuliis G, Cartelle C (2012) Recent advances on variability, morpho-functional adaptations, dental terminology, and evolution of sloths. J Mamm Evol 19(3):159–169CrossRefGoogle Scholar
  69. Ruf I, Volpato V, Rose KD, Billet G, de Muizon C (2016) Digital reconstruction of the inner ear of Leptictidium auderiense (Leptictida, Mammalia) and north American leptictids reveals new insight into leptictidan locomotor agility. PalZ 90(1):153–171CrossRefGoogle Scholar
  70. Silcox MT, Bloch JI, Boyer DM, Godinot M, Ryan TM, Spoor F, Walker A (2009) Semicircular canal system in early primates. J Hum Evol 56(3):315–327CrossRefPubMedGoogle Scholar
  71. Sipla JS, Spoor F (2008) The physics and physiology of balance. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley and Los Angeles, pp 227–232Google Scholar
  72. Slater GJ, Cui P, Forasiepi AM, Lenz D, Tsangaras K, Voirin B, de Moraes-Barros N, MacPhee RDE, Greenwood AD (2016) Evolutionary relationships among extinct and extant sloths: the evidence of mitogenomes and retroviruses. Genome Biol Evol 8(3):607–621CrossRefPubMedPubMedCentralGoogle Scholar
  73. Specht M (2007) Spherical surface parameterization and its application to geometric morphometric analysis of the braincase. University of Zürich, DissertationGoogle Scholar
  74. Specht M, Lebrun R, Zollikofer CPE (2007) Visualizing shape transformation between chimpanzee and human braincases. Vis Comput 23(9):743–751CrossRefGoogle Scholar
  75. Spoor F, Garland T, Krovitz G, Ryan TM, Silcox MT, Walker A (2007) The primate semicircular canal system and locomotion. Proc Natl Acad Sci U S A 104(26):10808–10812CrossRefPubMedPubMedCentralGoogle Scholar
  76. Toledo N (2016) Paleobiological integration of Santacrucian sloths (early Miocene of Patagonia). Ameghiniana 53(2):100–141CrossRefGoogle Scholar
  77. Varela L, Tambusso PS, Fariña RA (2016) Inner and middle ear 3D reconstruction of the extinct giant sloth Lestodon armatus. ICVM-11 abstracts, Washington DCGoogle Scholar
  78. Vizcaíno SF, Zárate M, Bargo MS, Dondas A (2001) Pleistocene burrows in the mar del Plata area (Argentina) and their probable builders. Acta Palaeontol Pol 46(2):289–301Google Scholar
  79. Wible JR (2010) Petrosal anatomy of the nine-banded armadillo, Dasypus novemcinctus Linnaeus, 1758 (Mammalia, Xenarthra, Dasypodidae). Ann Carnegie Mus 79(1):1–28CrossRefGoogle Scholar
  80. Wible JR, Gaudin TJ (2004) On the cranial osteology of the yellow armadillo Euphractus sexinctus (Dasypodidae, Xenarthra, Placentalia). Ann Carnegie Mus 73(3):117–196Google Scholar
  81. Zárate MA, Bargo MS, Vizcaíno SF, Dondas A, Scaglia O (1998) Estructuras biogénicas en el Cenozoico tardío de Mar del Plata (Argentina) atribuibles a grandes mamíferos. Rev Asoc Argent Sedimentol 5(2):95–103Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales (IANIGLA)CCT-CONICET-MendozaMendozaArgentina
  2. 2.Dipartimento di Scienze della TerraSapienza Università di RomaRomeItaly
  3. 3.PaleoFactorySapienza Università di RomaRomeItaly
  4. 4.Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements (CR2P)UMR CNRS 7207, MNHN, Sorbonne UniversitésParisFrance
  5. 5.Institut des Sciences de l’Evolution, CNRS, IRD, EPHEUniversité de MontpellierMontpellierFrance
  6. 6.IFEG (CONICET), Facultad de Matemática, Astronomía y FísicaUniversidad Nacional de CórdobaCórdobaArgentina
  7. 7.Department of Biology, Geology, and Environmental ScienceUniversity of Tennessee at ChattanoogaChattanoogaUSA

Personalised recommendations