Evolutionary Patterns of Bone Histology and Bone Compactness in Xenarthran Mammal Long Bones

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Straehl, Fiona R ^a   Scheyer, Torsten M ^a   Forasiepi, Analía M ^b   MacPhee, Ross D ^c   Sánchez Villagra, Marcelo R ^a  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b INSTITUTO ARGENTINO DE NIVOLOGÍA   (Argentina)

^c DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARMADILLO; ARTICLE; BONE COMPACTNESS; BONE EXAMINATION; BONE HISTOLOGY; BONE REMODELING; BONE STRUCTURE; EVOLUTION; FEMUR; HISTOLOGY; LONG BONE; MUSCULOSKELETAL FUNCTION; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; XENARTHRA;

ANIMALS; BIOLOGICAL EVOLUTION; BODY WEIGHT; BONE AND BONES; FEMUR; HAVERSIAN SYSTEM; HUMERUS; PHYLOGENY; XENARTHRA;

CINGULATA; DASYPODIDAE; MAMMALIA; MYRMECOPHAGIDAE; XENARTHRA;

EID: 84879906914     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069275     Document Type: Article

References (99)

1. Quekett J (1844) Transactions of the Microscopical Society of London. Volume II. London: John Churchill and Sons. 180 p.
2. Quekett J (1855) Descriptive and illustrated catalogue of the histological series contained in the museum of the Royal College of Surgeons of England: structure of the skeleton of vertebrate animals. Volume II. London: R. and J.E. Taylor. 356 p.
3. Enlow DH, Brown SO, (1956) A comparative histological study of fossil and recent bone tissues, Part I. Texas Journal of Science. 8: 405-443.
4. Enlow DH, Brown SO, (1957) A comparative histological study of fossil and recent bone tissues, Part II. Texas Journal of Science 9: 186-214.
5. Enlow DH, Brown SO, (1958) A comparative histological study of fossil and recent bone tissues, Part III. Texas Journal of Science 10: 187-230.
6. Peabody FE, (1961) Annual growth zones in living and fossil vertebrates. Journal of Morphology 108: 11-62.
7. Cubo J, Legendre P, de Ricqlès AJ, Montes L, de Margerie E, et al. (2008) Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evolution & Development 10: 217-227.
8. Casinos A, (1996) Bipedalism and quadrupedalism in Megatherium: an attempt at biomechanical reconstruction. Lethaia 29: 87-96.
9. de Ricqlès AJ, (1983) Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Palaeontologica Polonica 28: 225-232.
10. Germain D, Laurin M, (2005) Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zoologica Scripta 34: 335-350.
11. Kriloff A, Germain D, Canoville A, Vincent P, Sache M, et al. (2008) Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference. Journal of Evolutionary Biology 21: 807-826.
12. Canoville A, Laurin M, (2009) Microanatomical diversity of the humerus and lifestyle in lissamphibians. Acta Zoologica 90: 110-122.
13. Canoville A, Laurin M, (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biological Journal of the Linnean Society 100: 384-406.
14. Hayashi S, Houssaye A, Nakajima Y, Chiba K, Ando T, et al. (2012) Bone inner structure suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). PLoS ONE 8: e59146.
15. Ruff CB, Hayes WC, (1983) Cross-sectional geometry of Pecos Pueblo femora and tibiae- A biomechanical investigation: I. Method and general patterns of variation. American Journal of Physical Anthropology 60: 359-381.
16. Girondot M, Laurin M, (2003) Bone Profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. Journal of Vertebrate Paleontology 23: 458-461.
17. Laurin M, Girondot M, Loth M-M, (2004) The evolution of long bone microstructure and lifestyle in lissamphibians. Paleobiology 30: 589-613.
18. Houssaye A, Mazurier A, Herrel A, Volpato V, Tafforeau P, et al. (2010) Vertebral microanatomy in squamates: structure, growth and ecological correlates. Journal of Anatomy 217: 715-727.
19. Laurin M, Canoville A, Germain D, (2011) Bone microanatomy and lifestyle: a descriptive approach. Comptes Rendus Palevol 10: 381-402.
20. Meier PS, Bickelmann C, Scheyer TM, Koyabu D, Sanchez M, (2013) Evolution of bone compactness in extant and extinct moles (Talpidae): exploring humeral microstructure in small fossorial mammals. BMC Evolutionary Biology 13: 55.
21. Amprino R, Godina G, (1947) La struttura delle ossa nei vertebrati. Pontificia Academia Scientiarum 9: 329-463.
22. Singh IJ, Tonna EA, Gandel CP, (1974) A comparative histological study of mammalian bone. Journal of Morphology 144: 421-438.
23. Klevezal GA (1996) Recording structures of mammals: determination of age and reconstruction of life history. Rotterdam: A.A. Balkema. 274 p.
24. Sander PM, Andrássy P, (2006) Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: what do they tell us about dinosaur physiology? Palaeontographica A 277: 143-159.
25. Köhler M, Marín-Moratalla N, Jordana X, Aanes R, (2012) Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487: 358-361.
26. Chinsamy A, Hillenius WJ (2004) Physiology of non-avian dinosaurs. In: Weishampel DB, Dodson P, Osmólska H, editors. The Dinosauria. Berkeley: University of California Press. 643-659.
27. Padian K, Horner JR (2004) Dinosaur physiology. In: Weishampel DB, Dodson P, Osmólska H, editors. The Dinosauria. Berkeley: University of California Press. 660-671.
28. Asher RJ, Bennett N, Lehmann T, (2009) The new framework for understanding placental mammal evolution. BioEssays 31: 853-864.
29. Vizcaíno SF, Loughry WJ (2008) Xenarthran biology. In: Vizcaíno SF, Loughry WJ, editors. The biology of the Xenarthra. Gainesville: University Press of Florida. 1-7.
30. Taulman JF, Robbins LW, (1996) Recent range expansion and distributional limits of the nine-banded armadillo (Dasypus novemcinctus) in the United States. Journal of Biogeography 23: 635-648.
31. McKenna MC, Bell SK (2008) Classification of mammals above the species level. New York: Columbia University Press. 631 p.
32. Delsuc F, Catzeflis FM, Stanhope MJ, Douzery EJP, (2001) The evolution of armadillos, anteaters and sloths depicted by nuclear and mitochondrial phylogenies: implications for the status of the enigmatic fossil Eurotamandua. Proceedings of the Royal Society of London B 268: 1605-1615.
33. Delsuc F, Superina M, Tilak M-K, Douzery EJP, Hassanin A, (2012) Molecular phylogenetics unveils the ancient evolutionary origins of the enigmatic fairy armadillos. Molecular Phylogenetics and Evolution 62: 673-680.
34. Meredith RW, Janec JE, Gatesy J, Ryder OA, Fisher CA, et al. (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334: 521-524.
35. dos Reis M, Inoue J, Hasegawa M, Asher RJ, Donoghue PCJ, et al. (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proceedings of the Royal Society of London B 279: 3491-3500.
36. O'Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, et al. (2013) The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339: 662-667.
37. Möller-Krull M, Delsuc F, Churakov G, Marker C, Superina M, et al. (2007) Retroposed elements and their flanking regions resolve the evolutionary history of xenarthran mammals (armadillos, anteaters, and sloths). Molecular Biology and Evolution 24: 2573-2582.
38. 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, editors. Amniote paleobiology: Perspectives on the evolution of mammals, birds and reptiles. Chicago: University of Chicago Press. 153-198.
39. Wolf D, Kalthoff DC, Sander PM, (2012) Osteoderm histology of the Pampatheriidae (Cingulata, Xenarthra, Mammalia): implications for systematics, osteoderm growth, and biomechanical adaptation. Journal of Morphology 273: 388-404.
40. Delsuc F, Scally M, Madsen O, Stanhope MJ, De Jong WW, et al. (2002) Molecular phylogeny of living xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Molecular Biology and Evolution 19: 1656-1671.
41. Delsuc F, Stanhope MJ, Douzery EJP, (2003) Molecular systematics of armadillos (Xenarthra, Dasypodidae): contribution of maximum likelihood and Bayesian analyses of mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 28: 261-275.
42. Wible JR, Gaudin TJ, (2004) On the cranial osteology of the yellow armadillo Euphractus sexcintus (Dasypodidae, Xenarthra, Placentalia). Annals of Carnegie Museum 73: 117-196.
43. Gaudin TJ, McDonald HG (2008) Morphology-based investigations of the phylogenetic relationhips among extant and fossil xenarthrans. In: Vizcaíno SF, Loughry WJ, editors. The biology of the Xenarthra. Gainesville: University Press of Florida. 24-36.
44. Pujos F, Gaudin TJ, De Iuliis G, Cartelle C, (2012) Recent advances on variability, morpho-functional adaptations, dental terminology, and evolution of sloths. Journal of Mammalian Evolution 19: 159-169.
45. McDonald HG, De Iuliis G (2008) Fossil history of sloths. In: Vizcaíno SF, Loughry WJ, editors. The biology of the Xenarthra. Gainesville: University Press of Florida. 39-55.
46. de Muizon C, McDonald HG, (1995) An aquatic sloth from the Pliocene of Peru. Nature 375: 224-227.
47. Vizcaíno SF, Bargo MS, Fariña RA (2008) Form, function, and paleobiology in xenarthrans. In: Vizcaíno SF, Loughry WJ, editors. The biology of the Xenarthra. Gainesville: University Press of Florida. 86-99.
48. Asher RJ, Lin KH, Kardjilov N, Hautier L, (2011) Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology 24: 1080-1090.
49. Rager L, Sánchez-Villagra MR (2011) Heterochrony in cranial suture closure of recent and fossil Xenarthra. In: van der Geer A, Athanassiou A, editors. Program and Abstracts of the 9th Annual Meeting of the European Association of Vertebrate Palaeontologists, 14-19 June. Heraklion, Crete, Greece. p. 49.
50. Lara-Ruiz P, Chiarello AG, (2005) Life-history traits and sexual dimorphism of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). Journal of Zoology 267: 63-73.
51. Billet G, Hautier L, Asher RJ, Schwarz C, Crumpton N, et al. (2012) High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths. Proceedings of the Royal Society of London B 279: 3932-3939.
52. Hill R V, (2006) Comparative anatomy and histology of xenarthran osteoderms. Journal of Morphology 267: 1441-1460.
53. Krmpotic CM, Ciancio MR, Barbeito CG, Mario RC, Carlini AA, (2009) Osteoderm morphology in recent and fossil euphractine xenarthrans. Acta Zoologica 90: 339-351.
54. Da Costa Pereira PVLG, Victer GD, Porpino KDO, Bergqvist LP (2012) Osteoderm histology of Late Pleistocene cingulates from the intertropical region of Brazil. Acta Palaeontologica Polonica: In press.
55. Vickaryous MK, Hall BK, (2006) Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata). Journal of Morphology 267: 1273-1283.
56. Wolf D, (2007) Osteoderm histology of extinct and recent Cingulata and Phyllophaga (Xenarthra, Mammalia): implications for systematics and biomechanical adaptation. Hallesches Jahrbuch für Geowissenschaften Beiheft 23: 145-151.
57. Wolf D, (2008) Osteoderm histology of the Cingulata (Xenarthra, Mammalia): implicatios for systematics. Journal of Vertebrate Paleontology 28: 161A.
58. Merriam JC, (1906) Recent discoveries of Quartenary mammals in Southern California. Science 24: 248-250.
59. Sinclair WJ, (1910) Dermal bones of Paramylodon from the Asphaltum Deposits of Rancho la Brea, near Los Angeles, California. Proceedings of the American Philosophical Society 49: 191-195.
60. White JL, MacPhee RDE (2001) The sloths of the West Indies: A systematic and phylogenetic review. In: Woods CA, Sergile FF, editors. Biogeography of the West Indies: Patterns and perspectives. Boca Raton, FL: CRC Press. 201-231.
61. Straehl F, Chassagne M (2012) La diversidad e historia evolutiva de las perezas, cachicamos y sus parientes. In: Sánchez-Villagra MR, editor. Venezuela paleontológica. St. Gallen: Printworkart Press. 283-300.
62. Carlini AA, Brandoni D, Sánchez R, (2006) First megatheriines (Xenarthra, Phyllophaga, Megatheriidae) from the Urumaco (Late Miocene) and Codore (Pliocene) Formations, Estado Falcón, Venezuela. Journal of Systematic Palaeontology 4: 269-278.
63. Carlini AA, Zurita AE, Scillato-Yané GJ, Sánchez R, Aguilera OA, (2008) New glyptodont from the Codore Formation (Pliocene), Falcón State, Venezuela, its relationship with the Asterostemma problem, and the paleobiogeography of the Glyptodontinae. Paläontologische Zeitschrift 82: 139-152.
64. Carlini AA, Zurita AE, Aguilera OA, (2008) North American glyptodontines (Xenarthra, Mammalia) in the Upper Pleistocene of northern South America. Paläontologische Zeitschrift 82: 125-138.
65. Sánchez-Villagra MR, Aguilera OA, Sánchez R, Carlini AA (2010) The fossil vertebrate record of Venezuela of the last 65 million years. In: Sánchez-Villagra MR, Aguilera OA, Carlini AA, editors. Urumaco and venezuelan paleontology: The fossil record of the Northern Neotropics. Bloomington, IN: Indiana University Press. 19-51.
66. Chinsamy A, (1995) Ontogenetic changes in the bone histology of the late Jurassic ornithopod Dryosaurus lettowvorbecki. Journal of Vertebrate Paleontology 15: 96-104.
67. Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ,et al. (1990) Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG, editor. Skeletal biomineralization: patterns, processes and evolutionary trends. New York: Van Nostrand Reinhold. 471-755.
68. Stein KHW, Sander PM (2009) Histological core drilling: a less destructive method for studying bone histology. In: Brown MA, Kane JF, Parker WG, editors. Methods in fossil preparation: Proceedings of the First Annual Fossil Preparation and Collections Symposium. 69-80.
69. Sander PM, (2000) Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26: 466-488.
70. Scheyer TM, Sander PM, (2004) Histology of ankylosaur osteoderms: implications for systematics and function. Journal of Vertebrate Paleontology 24: 874-893.
71. Werning S, (2012) The ontogenetic osteohistology of Tenontosaurus tilletti. PLoS ONE 7: e33539.
72. Chinsamy-Turan A (2005) The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Baltimore: The Johns Hopkins University Press. 216.
73. Castanet J, Croci S, Aujard F, Perret M, Cubo J, et al. (2004) Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. Journal of Zoology 263: 31-39.
74. Chinsamy A, Hurum JH, (2006) Bone microstructure and growth patterns of early mammals. Acta Palaeontologica Polonica 51: 325-338.
75. Hurum JH, Chinsamy-Turan A (2012) The radiation, bone histology, and biology of early mammals. In: Chinsamy-Turan A, editor. Forerunners of mammals: radiation, histology, biology. Bloomington: Indiana University Press. 249-270.
76. Köhler M, Moyà-Solà S, (2009) Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proceedings of the National Academy of Sciences 106: 20354-20358.
77. Curtin AJ, MacDowell AA, Schaible EG, Roth VL, (2012) Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation x-ray microtomography. Journal of Vertebrate Paleontology 32: 939-955.
78. Klevezal GA, Kleinenberg SE (1969) Age determination of mammals from annual layers in teeth and bones. Jerusalem: Israel Program for Scientific Translations. 128 p.
79. Scheyer TM, Klein N, Sander PM, (2010) Developmental palaeontology of Reptilia as revealed by histological studies. Seminars in Cell & Developmental Biology 21: 462-470.
80. Castanet J, (2006) Time recording in bone microstructures of endothermic animals; functional relationships. Comptes Rendus Palevol 5: 629-636.
81. Superina M, Miranda FR, Abba AM, (2010) The 2010 anteater red list assessment. Edentata 11: 96-114.
82. Superina M, Plese T, Moraes-Barros N, Abba AM, (2010) The 2010 sloth red list assessment. Edentata 11: 115-134.
83. Abba AM, Superina M, (2010) The 2009/2010 armadillo red list assessment. Edentata 11: 135-184.
84. Mendel FC, (1981) Use of hands and feet of two-toed sloths (Choloepus hoffmanni) during climbing and terrestrial locomotion. Journal of Mammalogy 62: 413-421.
85. Mendel FC, (1985) Use of hands and feet of three-toed sloths (Bradypus variegatus) during climbing and terrestrial locomotion. Journal of Mammalogy 66: 359-366.
86. Hildebrand M (1985) Digging of quadrupeds. In: Hildebrand M, Bramble DM, Liem KF, Wake DB, editors. Functional vertebrate morphology. Cambridge: Belknap Press of Harvard University Press. 89-109.
87. Vizcaíno SF, Fariña RA, Mazzetta G V, (1999) Ulnar dimensions and fossoriality in armadillos. Acta Theriologica 44: 309-320.
88. Vizcaíno SF, Milne N, (2002) Structure and function in armadillo limbs (Mammalia: Xenarthra: Dasypodidae). Journal of Zoology 257: 117-127.
89. Grzimek B (2003) Grzimek's animal life encyclopedia. 2nd ed. Hutchins M, Kleiman DG, Geist V, McDade MC, editors Farmington Hills: Gale Group. 580 p.
90. Milne N, Vizcaíno SF, Fernicola JC, (2009) A 3D geometric morphometric analysis of digging ability in the extant and fossil cingulate humerus. Journal of Zoology 278: 48-56.
91. Quintana CA, (1992) Estructura interna de una paleocueva, posiblemente de un Dasypodidae (Mammalia, Edentata), del Pleistoceno de Mar del Plata (Provincia de Buenos Aires, Argentina). Ameghiniana 29: 87-91.
92. Gardner AL (2007) Suborder Vermilingua. In: Gardner AL, editor. Mammals of South America, Vol. 1: Marsupials, xenarthrans, shrews and bats. Chicago: The University of Chicago Press. 168-177.
93. Taylor BK, (1978) The anatomy of the forelimb in the anteater (Tamandua) and its functional implications. Journal of Morphology 157: 347-367.
94. Bargo MS, Vizcaíno SF, Archuby FM, Blanco RE, (2000) Limb bone proportions, strength and digging in some Lujanian (Late Pleistocene-Early Holocene) mylodontid ground sloths (Mammalia, Xenarthra). Journal of Vertebrate Paleontology 20: 601-610.
95. Vizcaíno SF, Zárate M, Bargo MS, Dondas A, (2001) Pleistocene burrows in the Mar del Plata area (Argentina) and their probable builders. Acta Palaeontologica Polonica 46: 289-301.
96. Gaudin TJ, (2004) Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zoological Journal of the Linnean Society 140: 255-305.
97. Smith FA, Lyons SK, Ernest SKM, Jones KE, Kaufman DM, et al. (2003) Body mass of late Quaternary mammals. Ecology 84: 3402 (updated version obtained from senior author).
98. White JL, (1993) Indicators of locomotor habits in xenarthrans: evidence for locomotor heterogeneity among fossil sloths. Journal of Vertebrate Paleontology 13: 230-242.
99. Geiger M, Wilson LA, Costeur L, Sánchez R, Sánchez-Villagra M (2012) Diversity and growth in giant caviomorphs from the northern neotropics - a study of femoral variation in Phoberomys (Rodentia). Journal of Vertebrate Paleontology: In press.