Skip to main content

The Postcranial Musculoskeletal System of Xenarthrans: Insights from over Two Centuries of Research and Future Directions

Abstract

Xenarthrans stand out among mammals for various reasons, one of them being their musculoskeletal postcranial specializations. Extant armadillos, anteaters, and sloths feature archetypical adaptations to digging and/or diverse arboreal lifestyles. Numerous extinct xenarthrans dramatically depart in size and morphology from their extant relatives, which has sparked functional interpretations since the end of the eighteenth century. Here, we review the diverse methodological approaches that have been used to investigate functional aspects of the postcranial musculoskeletal system in extant and extinct xenarthrans. Specifically, we address qualitative and quantitative bone morphology (including geometric morphometrics), body size and allometry, bone inner structure, myology, as well as in vivo, ex vivo, and in silico experimentation. Finally, a short account is given on those analyses that included xenarthrans to gain insight into primate anatomy. This review helped to identify potential future directions for the functional analysis of the xenarthran anatomy, a tradition over two centuries old.

This is a preview of subscription content, access via your institution.

Fig 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Acuña F, Sidorkewicj NS, Popp AI, Casanave EB (2017) A geometric morphometric study of sex differences in the scapula, humerus and ulna of Chaetophractus villosus (Xenarthra, Dasypodidae). Iheringia Série Zool 107:e2017010. doi: 10.1590/1678-4766e2017010

    Article  Google Scholar 

  • Alexander RM (2003) Principles of Animal Locomotion. Princeton University Press, Princeton

    Google Scholar 

  • Alexander RM, Fariña RA, Vizcaíno SF (1999) Tail blow energy and carapace fractures in a large glyptodont (Mammalia , Xenarthra). Zool J Linn Soc 126:41–49

    Google Scholar 

  • Allen GM (1913) A new Mylodon. Mem Mus Comp Zool 40:319–346

  • Amson E, Argot C, McDonald HG, Muizon C de (2015a) Osteology and functional morphology of the forelimb of the marine sloth Thalassocnus (Mammalia, Tardigrada). J Mammal Evol 22:169–242. doi: 10.1007/s10914-014-9268-3

    Google Scholar 

  • Amson E, Argot C, McDonald HG, Muizon C de (2015b) Osteology and functional morphology of the hind limb of the marine sloth Thalassocnus (Mammalia, Tardigrada). J Mammal Evol 22:355–419. doi: 10.1007/s10914-014-9274-5

    Google Scholar 

  • Amson E, Argot C, McDonald HG, Muizon C de (2015c) Osteology and functional morphology of the axial postcranium of the marine sloth Thalassocnus (Mammalia, Tardigrada) with paleobiological implications. J Mammal Evol 22:473–518. doi: 10.1007/s10914-014-9280-7

    Google Scholar 

  • Amson E, Muizon C de, Domning DP, Argot C, Buffrénil V de (2015d) Bone histology as a clue for resolving the puzzle of a dugong rib in the Pisco Formation, Peru. J Vertebr Paleontol 35:e922981. doi: 10.1080/02724634.2014.922981

    Google Scholar 

  • Amson E, Muizon C de, Gaudin TJ (2016) A reappraisal of the phylogeny of the Megatheria (Mammalia: Tardigrada), with an emphasis on the relationships of the Thalassocninae, the marine sloths. Zool J Linn Soc. doi:10.1111/zoj.12450

  • Amson E, Muizon C de, Laurin M, Argot C, Buffrénil V de (2014) Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru. Proc R Soc B 281:20140192. doi: 10.1098/rspb.2014.0192

    PubMed  PubMed Central  Google Scholar 

  • Anthony MR (1905) Note préliminaire sur les attitudes et les caractères d’adaptation des édentés de la famille des Bradipodydae. Bull Mus Natl Hist Nat 6:385–388

    Google Scholar 

  • Anthony R (1907) Études et recherches sur les Edentés tardigrades et gravigrades. — I. Les coupures génériques de la famille des Bradipodidae. — II. Les attitudes et la locomotion des Paresseux. Arch Zool expérimentale générale 4:31–72

    Google Scholar 

  • Anthony HE (1918) The indigenous land mammals of Porto Rico, living and extinct. Mem Am Mus Nat Hist, new ser 2:334–435

  • Aramayo S, Manera de Bianco TM (1987) Hallazgo de una icnofauna continental (Pleistoceno tardío) en la localidad de Pehuén-Có (partido de Coronel Rosales), Provincia de Buenos Aires. Parte I: Edentata, Litopterna, Proboscidea. In: IV Congreso Latinoamericano de Paleontología, pp 516–531

  • Argot C (2008) Changing views in paleontology: the story of a giant (Megatherium, Xenarthra). In: Sargis EJ, Dagosto M (eds) Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay. Springer, Dordrecht, pp 37–50

  • Arnold P, Fischer MS, Nyakatura JA (2014) Soft tissue influence on ex vivo mobility in the hip of Iguana: comparison with in vivo movement and its bearing on joint motion of fossil sprawling tetrapods. J Anat 225:31–41. doi: 10.1111/joa.12187

    Article  PubMed  PubMed Central  Google Scholar 

  • Bardeleben K von (1894) On the bones and muscles of the mammalian hand and foot. Proc Zool Soc Lond 1894:354–376

  • Bargo MS (2003) Biomechanics and palaeobiology of the Xenarthra: the state of the art. Senckenb Biol 83:41–50

    Google Scholar 

  • Bargo MS, Toledo N, Vizcaíno SF (2012) Paleobiology of the Santacrucian sloths and anteaters (Xenarthra, Pilosa). In: Vizcaíano SF, Kay RF, Bargo MS (eds) Early Miocene Paleobiology in Patagonia: High-Latitude Paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 216–242

  • 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). J Vertebr Paleontol 20:601–610

    Google Scholar 

  • Barlow C (1967) Edentates and Pholidotes. In: Anderson S, Knox Jones JJ (eds) Recent Mammals of the World. The Ronald Press Co, New York, pp 181–185

    Google Scholar 

  • Beebe W (1926) The three-toed sloth. Bradypus cucullinger cucullinger Wagler. Zoologica 7:1–67

    Google Scholar 

  • Bell C (1833) Bridgewater Treatise IV. The Hand, its Mechanism and Vital Endowments as Evincing Design. Carey, Lea and Blanchard, Philadelphia

  • Bell T (1834) Observations on the neck of the three-toed sloth, Bradypus tridactylus, Linn. Trans Zool Soc Lond 1:113–116. doi: 10.1111/j.1096-3642.1835.tb00608.x

    Article  Google Scholar 

  • Biknevicius AR (1999) Body mass estimation in armoured mammals: cautions and encouragements for the use of parameters from the appendicular skeleton. J Zool 248:179–187. doi: 10.1017/S0952836999006056

    Article  Google Scholar 

  • 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 279:3932–3939. doi: 10.1098/rspb.2012.1212

    Article  PubMed  PubMed Central  Google Scholar 

  • Blanco RE, Czerwonogora A (2003) The gait of Megatherium Cuvier 1796. Senckenb Biol 83:61–68

    Google Scholar 

  • Blanco RE, Jones WW, Rinderknecht A (2009) The sweet spot of a biological hammer: the centre of percussion of glyptodont (Mammalia: Xenarthra) tail clubs. Proc R Soc B Biol Sci 276:3971–3978. doi: 10.1098/rspb.2009.1144

    Article  Google Scholar 

  • Brandoni D, Carlini AA, Pujos F, Scillato-Yané GJ (2004) The pes of Pyramiodontherium bergi (Moreno & Mercerat, 1891) (Mammalia, Xenarthra, Phyllophaga): the most complete pes of a Tertiary Megatheriinae. Geodiversitas 26:643–659

    Google Scholar 

  • Brassey CA, Gardiner JD (2015) An advanced shape-fitting algorithm applied to quadrupedal mammals: improving volumetric mass estimates. R Soc Open Sci 2:150302

    PubMed  PubMed Central  Google Scholar 

  • Britton SW (1941a) Form and function in the sloth. Q Rev Biol 16:13–34

    Google Scholar 

  • Britton SW (1941b) Form and function in the sloth (concluded). Q Rev Biol 16:190–207. doi: 10.1086/394628

    Article  Google Scholar 

  • Britton SW, Kline RF (1939) On deslothing the sloth. Science 90:16–17. doi: 10.1126/science.90.2323.16-a

    CAS  Article  PubMed  Google Scholar 

  • Buckland W (1834) On the adaptation of the structure of the sloths to their peculiar mode of life. Trans Linn Soc Lond 17:17–27

  • Buckland W (1836) Bridgewater Treatise VI. Geology and Mineralogy considered with reference to Natural Theology. Vol. I. William Pickering, London

    Google Scholar 

  • Burmeister G (1864) Fauna Argentina. Primera parte. Mamíferos fósiles. An del Mus Público Buenos Aires 1:87–300

    Google Scholar 

  • Cabrera A (1929) Sobre la estructura de la mano y del pie en el megaterio. An la Soc Cient Argentina 107:425–433

    Google Scholar 

  • Carleton A (1936) The limb-bones and vertebrae of the extinct lemurs of Madagascar. Proc Zool Soc Lond 106:281–307. doi: 10.1111/j.1096-3642.1936.tb02290.x

    Article  Google Scholar 

  • Cartmill M (1985) Climbing. In: Hildebrand M (ed) Functional Vertebrate Morphology. Cambridge University Press, Cambridge, pp 73–88

    Google Scholar 

  • Casinos A (1996) Bipedalism and quadrupedalism in Megatherium: an attempt at biomechanical reconstruction. Lethaia 29:1–112

    Google Scholar 

  • Chiarello AG (1998) Activity budgets and ranging patterns of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J Zool 246:1–10

    Google Scholar 

  • Christiansen P, Fariña RA (2003) Mass estimation of two fossil ground sloths. Senckenb Biol 83:95–101

    Google Scholar 

  • Coombs MC (1983) Large mammalian clawed herbivores: a comparative study. Trans Am Philos Soc New Ser 73:1–96

    Google Scholar 

  • Copploe JV II, Blob RW, Parrish JHA, Butcher MT (2015) In vivo strains in the femur of the nine-banded armadillo (Dasypus novemcinctus). J Morphol 276:889–899. doi: 10.1002/jmor.20387

    Article  PubMed  Google Scholar 

  • Croft DA (2000) Archaeohyracidae (Mammalia: Notoungulata) from the Tinguiririca fauna, central Chile, and the evolution and paleoecology of South American mammalian herbivores. PhD dissertaion, University of Chicago

    Google Scholar 

  • Cuenca Anaya J (1995) El Aparato Locomotor de los Escelidoterios (Edentata, Mammalia) y su Paleobiologia. Ajuntament de Valencia, Valencia, 452 pp

    Google Scholar 

  • Cunningham JA, Rahman IA, Lautenschlager S, Rayfield EJ, Donoghue PCJ (2014) A virtual world of paleontology. Trends Ecol Evol 29:347–357. doi: 10.1016/j.tree.2014.04.004

    Article  PubMed  Google Scholar 

  • Cuvier G (1796) Notice sur le squelette d’une très grande espèce de quadrupède inconnue jusqu’à présent, trouvé au Paraguay, et déposé au cabinet d’Histoire naturelle de Madrid. Mag Encycl 1:303–310.

    Google Scholar 

  • Cuvier G (1804) Sur le Megatherium. Ann Mus Natl Hist Nat 5:376–400

    Google Scholar 

  • Cuvier G (1812a) Sur le Megatherium, autre animal de la famille des paresseux, mais de la taille du rhinocéros, dont un squelette fossile presque complet est conservé au cabinet Royal d’Histoire naturelle à Madrid. In: Recherches sur les ossemens fossiles de quadrupèdes. Vol. IV, part IV. Deterville, Paris, pp 19–43

  • Cuvier G (1812b) Observations sur l’ostéologie des paresseux. In: Recherches sur les ossemens fossiles de quadrupèdes. Vol. IV, part IV. Deterville, Paris, pp 1–27

  • Cuvier G (1812c) Sur le Megalonix, animal de la famille des paresseux, mais de la taille du boeuf, dont les ossemens ont été découverts en Virginie, en 1796. In: Recherches sur les ossemens fossiles de quadrupèdes. Vol. IV, part IV. Deterville, Paris, pp 1–18

  • Cuvier G, Laurillard CL (1849) Anatomie Comparée: Recueil de Planches de Myologie. Chez Dusac, Paris

  • Czerwonogora A, Fariña RA (2013) How many Pleistocene species of Lestodon (Mammalia, Xenarthra, Tardigrada)? J Syst Palaeontol 11:251–263. doi: 10.1080/14772019.2012.660993

    Article  Google Scholar 

  • Daston L, Galison P (2007) Objectivity. Zone Books, New York

    Google Scholar 

  • De Esteban-Trivigno S, Mendoza M, De Renzi M (2008) Body mass estimation in Xenarthra: a predictive equation suitable for all quadrupedal terrestrial placentals? J Morphol 269:1276–1293. doi: 10.1002/jmor.10659

    Article  PubMed  Google Scholar 

  • De Faria LG, Rahal SC, dos Reis Mesquita L, Agostinho FS, Kano T, Teixeira CR, Barros Monteiro FO (2015) Gait analysis in giant anteater (Myrmecophaga tridactyla) with the use of a pressure-sensitive. J Zoo Wildl Med 46:286–290

    PubMed  Google Scholar 

  • De Iuliis G (1996) A systematic review of the Megatheriinae (Mammalia: Xenarthra: Megatheriidae). PhD dissertation, University of Toronto

    Google Scholar 

  • De Iuliis G, Ré GH, Vizcaíno SF (2004) The Toro Negro megatheriine (Mammalia, Xenathra): a new species of Pyramiodontherium and a review of Plesiomegatherium. J Vertebr Paleontol 24:214–227

    Google Scholar 

  • Delsuc F, Douzery EJP (2008) Recent advances and future prospects in xenarthran molecular phylogenetics. In: Vizcaino SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 11–23

    Google Scholar 

  • Delsuc F, Gibb GC, Kuch M, Billet G, Hautier L, Southon J, Rouillard JM, Fernicola JC, Vizcaíno SF, MacPhee RD, Poinar HN (2016) The phylogenetic affinities of the extinct glyptodonts. Curr Biol 26:R155–R156. doi: 10.1016/j.cub.2016.01.039

    CAS  PubMed  Google Scholar 

  • Dor M (1937) La morphologie de la queue des mammifères dans ses rapports avec la locomotion. Impressions Pierre André, Paris, 184 pp

    Google Scholar 

  • Enders RK (1940) Observations on sloths in captivity at higher altitudes in the tropics and in Pennsylvania. J Mammal 21:5–7

    Google Scholar 

  • Enger S, Bullock TH (1965) Physiological basis of slothfulness in the sloth. Hvalrådets Skr 48:143–160

    Google Scholar 

  • Fariña RA (1995) Limb bone strength and habits in large glyptodonts. Lethaia 28:189–196

    Google Scholar 

  • Fariña RA (1996) Trophic relationships among Lujanian mammals. Evol Theory 11:125–134

    Google Scholar 

  • Fariña RA, Blanco RE (1996) Megatherium, the stabber. Proc R Soc B 263:1725–1729

    PubMed  Google Scholar 

  • Fariña RA, Vizcaíno SF (1997) Allometry of the bones of living and extinct armadillos (Xenarthra, Dasypoda). Z Säugetierkd 62:65–70

    Google Scholar 

  • Fariña RA, Vizcaíno SF, Blanco RE (1997) Scaling of the indicator of athletic capability in fossil and extant land tetrapods. J Theor Biol 185:441–446. doi: 10.1006/jtbi.1996.0323

    Article  Google Scholar 

  • Fariña RA, Vizcaíno SF, Bargo MS (1998) Body mass estimations in Lujanian (late Pleistocene-early Holocene of South America) mammal megafauna. Mastozoología Neotrop 5:87–108

    Google Scholar 

  • Frechkop S (1949) Explication biologique, fournie par les tatous, d’un des caractères distinctifs des xénarthres et d’un caractère adaptatif analogue chez les pangolins. Inst R des Sci Nat Belgique 25:1–12

    Google Scholar 

  • Fujiwara S, Endo H, Hutchinson JR (2011) Topsy-turvy locomotion: biomechanical specializations of the elbow in suspended quadrupeds reflect inverted gravitational constraints. J Anat 219:176–191. doi: 10.1111/j.1469-7580.2011.01379.x

    PubMed  PubMed Central  Google Scholar 

  • Galton JC (1869) The muscles of the fore and hind limbs in Dasypus sexcinctus. Trans Linn Soc Lond 26:523–566

    Google Scholar 

  • Gambaryan PP, Zherebtsova O V, Perepelova AA, Platonov V V (2009) Pes muscles and their action in giant anteater Myrmecophaga tridactyla (Myrmecophagidae, Pilosa) compared with other plantigrade mammals Russ J Theriol 8:1–15

    Google Scholar 

  • Gatesy SM, Baier DB, Jenkins FA Jr, Dial KP (2010) Scientific rotoscoping: a morphology-based method of 3-D motion analysis and visualization. J Exp Zool A Ecol Genet Physiol 313:244–261. doi: 10.1002/jez.588

    Article  PubMed  Google Scholar 

  • Gaudin TJ (1999) The morphology of xenarthrous vertebrae (Mammalia: Xenarthra). Fieldiana Geol New Ser 41:1–38

    Google Scholar 

  • Gaudin TJ (2004) Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zool J Linn Soc 140:255–305. doi: 10.1111/j.1096-3642.2003.00100.x

    Article  Google Scholar 

  • Gaudin TJ, Biewener AA (1992) The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra). J Morphol 214:63–81

    CAS  PubMed  Google Scholar 

  • Gaudin TJ, Branham D (1998) The phylogeny of the Myrmecophagidae (Mammalia, Xenarthra, Vermilingua) and the relationship of Eurotamandua to the Vermilingua. J Mammal Evol 5:237–265

    Google Scholar 

  • Gaudin TJ, Croft DA (2015) Paleogene Xenarthra and the evolution of South American mammals. J Mammal 96:622–634. doi: 10.1093/jmammal/gyv073

    Article  Google Scholar 

  • Gaudin TJ, Nyakatura JA (in press) A comparison of the epaxial muscles of the Common long-nosed armadillo, the two-toed sloth, and the Virginia opossum: functional significance and implications for the evolution of back muscles in the Xenarthra. J Mamm Evol. doi:10.1007/s10914-017-9402-0

  • Gibb GC, Condamine FL, Kuch M, Enk J, Moraes-Barros N, Superina M, Poinar HN, Delsuc F (2016) Shotgun mitogenomics provides a reference phylogenetic framework and timescale for living xenarthrans. Mol Biol Evol 33:621–642. doi: 10.1093/molbev/msv250

    CAS  Article  PubMed  Google Scholar 

  • Gignac PM, Kley NJ, Clarke JA, Colbert MW, Morhardt AC, Cerio D, Cost IN, Cox PG, Daza JD, Early CM, Echols MS, Henkelman RM, Herdina AN, Holliday CM, Li Z, Mahlow K, Merchant S, Müller J, Orsbon CP, Paluh DJ, Thies ML, Tsai HP, Witmer LM (2016) Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. J Anat 228:889–909. doi:10.1111/joa.12449

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gillette DD, Ray CE (1981) Glyptodonts of North America. Smithson Contrib Paleobiol 40:1–255

    Google Scholar 

  • Giné GAF, Cassano CR, de Almeida SS, Faria D (2015) Activity budget, pattern and rhythm of maned sloths (Bradypus torquatus): responses to variations in ambient temperature. Mammal Biol 80:459–467. doi: 10.1016/j.mambio.2015.07.003

    Article  Google Scholar 

  • Goffart M (1971) Function and Form in the Sloth. Pergamon Press, New York

    Google Scholar 

  • Goffart M, Holmes O, Bacq ZM (1962) Some mechanical properties of skeletal muscle in the sloth. Arch Int Physiol Biochim 70:103–106. doi: 10.3109/13813456209092846

    CAS  Article  PubMed  Google Scholar 

  • Granatosky MC (2016) A mechanical analysis of suspensory locomotion in primates and other mammals. PhD dissertation, Duke University

    Google Scholar 

  • Granatosky MC, Miller CE, Boyer DM, Schmitt D (2014) Lumbar vertebral morphology of flying, gliding, and suspensory mammals: implications for the locomotor behavior of the subfossil lemurs Palaeopropithecus and Babakotia. J Hum Evol 75:40–52. doi: 10.1016/j.jhevol.2014.06.011

    Article  PubMed  Google Scholar 

  • Granatosky MC, Schmitt D (2017) Forelimb and hind limb loading patterns during below branch quadrupedal locomotion in the two-toed sloth. J Zool. doi: 10.1111/jzo.12455

    Google Scholar 

  • Grand TI (1978) Adaptations of tissue and limb to facilitate moving and feeding in arboreal folivores. In: Montgomery GG (ed) The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, D. C., pp 231–241

  • Grass AD (2014) Inferring lifestyle and locomotor habits of extinct sloths through scapula morphology and implications for convergent evolution in extant sloths. PhD dissertation, University of Iowa

    Google Scholar 

  • Grassé P-P (1955) Ordre des Édentés. In: Grassé P-P (ed) Traité de Zoologie, vol. 17 Mammifères. Masson et Cie, Paris, pp 1182–1246

    Google Scholar 

  • Haro JA, Tauber AA, Krapovickas JM (2016) The manus of Mylodon darwinii Owen (Tardigrada, Mylodontidae) and its phylogenetic implications. J Vertebr Paleontol 36:e1188824. doi: 10.1080/02724634.2016.1188824

    Article  Google Scholar 

  • Hildebrand M (1985) Digging of quadrupeds. In: Hildebrand M (ed) Functional Vertebrate Morphology. Cambridge University Press, Cambridge, pp 89–109

    Google Scholar 

  • Hirschfeld SE (1976) A new fossil anteater (Edentata, Mammalia) from Colombia, S.A. and evolution of the Vermilingua. J Paleontol 50:419–432

    Google Scholar 

  • Hirschfeld SE (1985) Ground sloths from the Friasian La Venta fauna, with additions to the Pre-Friasian Coyaima fauna of Colombia, South America. Univ Calif Publ Geol Sci 128:1–91

    Google Scholar 

  • Hoffstetter R (1958) Xenarthra. In: Piveteau J (ed) Traité de Paléontologie, Vol. 6(2). Masson et Cie, Paris, pp 535–636

  • Humphry GM (1869) The myology of the limbs of the unau, the aï, the two-toed anteater, and the pangolin. J Anat Physiol 4:17–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hutchinson JR (2011) On the inference of function from structure using biomechanical modelling and simulation of extinct organisms. Biol Lett 8:115–118. doi: 10.1098/rsbl.2011.0399

    Article  PubMed  PubMed Central  Google Scholar 

  • Hutchinson JR, Rankin JW, Rubenson J, Rosenbluth KH, Siston RA, Delp SL (2015) Musculoskeletal modelling of an ostrich (Struthio camelus) pelvic limb: influence of limb orientation on muscular capacity during locomotion. PeerJ 3:e1001. doi: 10.7717/peerj.1001

    Article  PubMed  PubMed Central  Google Scholar 

  • Jasinski SE, Wallace SC (2014) Investigation into the paleobiology of Dasypus bellus using geometric morphometrics and variation of the calcaneus. J Mammal Evol 21:285–298. doi: 10.1007/s10914-013-9239-0

    Article  Google Scholar 

  • Jenkins FA Jr (1970) Anatomy and function of expanded ribs in certain edentates and primates. J Mammal 51:288–301

    PubMed  Google Scholar 

  • Jouffroy F-K, Lessertisseur J, Vassal P (1961) Particularités musculaires des extrémités du bradype aï (Bradypus tridactylus L.) dans leurs rapports avec la suspension arboricole. Comptes Rendus l’Association des Anat 47:392–400

    Google Scholar 

  • Kawashima T, Thorington RW, Bohaska PW, Chen Y-J, Sato F (2015) Anatomy of shoulder girdle muscle modifications and walking adaptation in the scaly Chinese pangolin (Manis pentadactyla pentadactyla: Pholidota) compared with the partially osteoderm-clad armadillos (Dasypodidae). Anat Rec 298:1217–1236. doi: 10.1002/ar.23170

    Article  Google Scholar 

  • Kley NJ, Kearney M (2007) Adaptations for digging and burrowing. In: Hall BK (ed) Fins into Limbs: Evolution, Development, and Transformation. University of Chicago Press, Chicago, pp 284–309

    Google Scholar 

  • Kolb C, Scheyer T, Veitschegger K, Forasiepi AM, Amson E, Van der Geer AAE, van den Hoek Ostende LW, Hayashi S, Sánchez-Villagra MR (2015) Mammalian bone palaeohistology: a survey and new data with emphasis on island forms. PeerJ 3:e1358. doi: 10.7717/peerj.1358

    Article  PubMed  PubMed Central  Google Scholar 

  • Krmpotic CM, Ciancio MR, Carlini AA, Castro MC, Scarano AC, Barbeito CG (2015) Comparative histology and ontogenetic change in the carapace of armadillos (Mammalia: Dasypodidae). Zoomorphology 134:601–616. doi: 10.1007/s00435-015-0281-8

    Article  Google Scholar 

  • Kupczik K, Stark H, Mundry R, Neininger FT, Heidlauf T, Röhrle O (2015) Reconstruction of muscle fascicle architecture from iodine-enhanced microCT images: a combined texture mapping and streamline approach. J Theor Biol 382:34–43. doi: 10.1016/j.jtbi.2015.06.034

    Article  PubMed  Google Scholar 

  • Langworthy OR (1935) A physiological study of the cerebral motor cortex and the control of posture in the sloth. J Comp Neurol 62:333–348

    Google Scholar 

  • Lautenschlager S (2014) Palaeontology in the third dimension: a comprehensive guide for the integration of three-dimensional content in publications. Paläontol Z 88:111–121. doi: 10.1007/s12542-013-0184-2

    Google Scholar 

  • Lewton KL, Dingwall HL (2016) Morphological convergence in the pubis of slow-moving primates and xenarthrans. Am J Phys Anthropol 161:381–397. doi: 10.1002/ajpa.23038

    Article  PubMed  Google Scholar 

  • Lucae J (1882) The Muscles and the Skeleton of the Black Lemur and the Sloth (Lemur macaco and Choloepus didactylus). Mahlau and Waldschmidt Verlag, Senckenbergische Naturforschende Gesellschaft, Frankfurt am Main

  • Luederwaldt H (1918) Observações sobre a preguiça (Bradypus tridactylus, L.) em liberdade e no captiveiro. Rev Mus Paul 10:793–812

    Google Scholar 

  • Lundy WE (1952) The upside-down animal. Nat Hist 61:114–119

    Google Scholar 

  • Macalister A (1875) A monograph of the anatomy of Chlamydophorus truncatus (Harlan), with notes on the structure of other species of Edentata. Trans R Irish Acad 25:219–278

    Google Scholar 

  • Mackintosh H (1870) On the myology of the genus Bradypus. Proc R Irish Acad Sci 1:517–529

    Google Scholar 

  • Mackintosh H (1875) On the muscular anatomy of Cholœpus didactylus. Proc R Irish Acad Sci 2:66–78

    Google Scholar 

  • Marchi D, Ruff CB, Capobianco A, Rafferty KL, Habib MB, Patel BA (2016) The locomotion of Babakotia radofilai inferred from epiphyseal and diaphyseal morphology of the humerus and femur. J Morphol 277:1199–1218. doi: 10.1002/jmor.20569

    Article  PubMed  Google Scholar 

  • Maréchal G, Goffart M, Aubert X (1963) Nouvelles recherches sur les propriétés du muscle squelettique du paresseux (Choloepus hoffmani Peters). Arch Int Physiol Biochim 71:236–240. doi: 10.3109/13813456309092164

    Article  PubMed  Google Scholar 

  • Matthew WD (1912) The ancestry of edentates: as illustrated by the skeleton of Hapalops, a Tertiary ancestor of the ground sloths. Am Mus J 12:300–303

  • Maynard Smith J, Savage RJG (1956) Some locomotory adaptations in mammals. Zool J Linn Soc 42:603–622

    Google Scholar 

  • McAfee RK (2009) Reassessment of the cranial characters of Glossotherium and Paramylodon (Mammalia: Xenarthra: Mylodontidae). Zool J Linn Soc 155:885–903

    Google Scholar 

  • McAfee RK (2016) Description of new postcranial elements of Mylodon darwinii Owen 1839 (Mammalia: Pilosa: Mylodontinae), and functional morphology of the forelimb. Ameghiniana 53:418–433

    Google Scholar 

  • McDonald HG (1977) Description of the osteology of the extinct gravigrade edentate Megalonyx with observations on its ontogeny, phylogeny, and functional anatomy. MS dissertation, University of Florida.

  • McDonald HG (1995) Gravigrade xenarthrans from the middle Pleistocene Leisey Shell Pit 1A, Hillsborough County, Florida. Bull Florida Mus Nat Hist 37:345–373

    Google Scholar 

  • McDonald HG (2003) Xenarthran skeletal anatomy: primitive or derived? Senckenb Biol 83:5–17

    Google Scholar 

  • McDonald HG (2005) Palecology of extinct xenarthrans and the great American biotic interchange. Bull Florida Mus Nat Hist 45:319–340

    Google Scholar 

  • McDonald HG (2007) Biomechanical inferences of locomotion in ground sloths: integrating morphological and track data. New Mex Mus Nat Hist Sci Bull 42:201–208

    Google Scholar 

  • McDonald HG (2012) Evolution of the pedolateral foot in ground sloths: patterns of change in the astragalus. J Mammal Evol 19:209–215. doi: 10.1007/s10914-011-9182-x

    Article  Google Scholar 

  • McDonald HG (under review) Osteoderms in ground sloths: plesiomorphic or apomorphic? J Mammal Evol.

  • McDonald HG, De Iuliis G (2008) Fossil history of sloths. In: Vizcaíno SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 39–55

  • McDonald HG, Vizcaíno SF, Bargo MS (2008) Skeletal anatomy and the fossil history of the vermilingua. In: Vizcaíno SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 64–78

  • McNab BK (1985) Energetics, population biology, and distribution of xenarthrans, living and extinct. In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington D. C., pp 219–232

    Google Scholar 

  • Meincke F (1911) Morphologische Untersuchungen über die Myologie an den Extremitäten bei Bradypus tridactylus. Morphol Jahrb 2:311–358

    Google Scholar 

  • Mendel FC (1979) The wrist joint of two-toed sloths and its relevance to brachiating adaptations in the hominoidea. J Morphol 162:413–424. doi: 10.1002/jmor.1051620308

    Article  PubMed  Google Scholar 

  • Mendel FC (1981a) The hand of two-toed sloths (Choloepus): its anatomy and potential uses relative to size of support. J Morphol 169:1–19

    PubMed  Google Scholar 

  • Mendel FC (1981b) Foot of two-toed sloths: its anatomy and potential uses relative to size of support. J Morphol 170:357–372. doi: 10.1002/jmor.1051700307

    Article  PubMed  Google Scholar 

  • Mendel FC (1981c) Use of hands and feet of two-toed sloths (Choloepus hoffmanni) during climbing and terrestrial locomotion. J Mammal 62:413–421

    Google Scholar 

  • Mendel FC (1985a) Adaptions for suspensory behavior in the limbs of two-toed sloths. In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, D. C., pp 151–162

    Google Scholar 

  • Mendel FC (1985b) Use of hands and feet of three-toed sloths (Bradypus variegatus) during climbing and terrestrial locomotion. J Mammal 66:359–366

    Google Scholar 

  • Ménégaux MA (1908) La marche et la façon de grimper des paresseux, d’après les observations récentes et notamment celles de M. et Mme Geay, voyageurs du Muséum d’Histoire naturelle. Bull Mus Natl Hist Nat 14:334–337

    Google Scholar 

  • Meritt DA (1977) The natural history, behavior, nutrition, physiology, reproduction, development and management of Hoffman’s sloth, Choloepus hoffmanni (Peters). PhD dissertation, Northeastern Illinois Univeristy

  • Miles SS (1941) The shoulder anatomy of the armadillo. J Mammal 22:157–169

    Google Scholar 

  • Miller RA (1935) Functional adaptations in the forelimb of the sloths. J Mammal 16:38–51

    Google Scholar 

  • Milne N, O’Higgins P (2012) Scaling of form and function in the xenarthran femur: a 100-fold increase in body mass is mitigated by repositioning of the third trochanter. Proc Biol Sci. doi: 10.1098/rspb.2012.0593

    PubMed  PubMed Central  Google Scholar 

  • Milne N, Toledo N, Vizcaíno SF (2012) Allometric and group differences in the xenarthran femur. J Mammal Evol 19:199–208. doi: 10.1007/s10914-011-9171-0

    Google Scholar 

  • Milne N, Vizcaíno SF, Fernicola JC (2009) A 3D geometric morphometric analysis of digging ability in the extant and fossil cingulate humerus. J Zool 278:48–56. doi: 10.1111/j.1469-7998.2008.00548.x

    Google Scholar 

  • Miño-Boilini ÁR, Tomassini RL, Oliva C, de Bianco TM (2011) Adiciones al conocimiento de Proscelidodon Bordas, 1935 (Mammalia, Xenarthra, Scelidotheriinae). Rev Bras Paleontol 14:269–278. doi: 10.4072/rbp.2011.3.06

    Article  Google Scholar 

  • Monteiro LR (2000) Geometric morphometrics and the development of complex structures: ontogenetic changes in scapular shape of dasypodid armadillos. Hystrix 11:91–98

    Google Scholar 

  • Monteiro LR, Abe AS (1999) Functional and historical determinants of shape in the scapula of xenarthran mammals: evolution of a complex morphological structure. J Morphol 241:251–263. doi: 10.1002/(SICI)1097-4687(199909)241:3<251::AID-JMOR7>3.0.CO;2-7

    CAS  Article  PubMed  Google Scholar 

  • Montgomery GG, Sunquist ME (1975) Impact of sloths on Neotropical forest energy flow and nutrient cycling. In: Golley FB, Medina E (eds) Tropical Ecological Systems. Springer, Berlin, pp 69–98

    Google Scholar 

  • Montgomery GG, Sunquist ME (1978) Selection and use by two-toed and three-toed sloths. In: Montgomery GG (ed) The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, D. C., pp 329–359

    Google Scholar 

  • Muizon C de, McDonald HG (1995) An aquatic sloth from the Pliocene of Peru. Nature 375:224–227. doi: 10.1038/375224a0

    Article  Google Scholar 

  • Murie J (1874) On the habits, structure, and relations of the three-banded armadillo (Tolypeutes conurus, Is. Geoff.). Trans Linn Soc Lond 30:71–132

    Google Scholar 

  • Muybridge E (1887) Animal Locomotion: An Electrophotographic Investigation of Consecutive Phases of Animal Movements. 1872-1875. University of Pennsylvania, Philadelphia

  • Nodot L (1856) Description d’un Nouveau Genre d’Édenté fossile renfermant Plusieurs Espèces Voisines du Glyptodon, Suivie d’une Nouvelle Méthode de Classification Applicable à Toute l’Histoire Naturelle, et Spécialement à ces Animaux. Loireau-Feuchot, Dijon

    Google Scholar 

  • Nyakatura JA (2012) The convergent evolution of suspensory posture and locomotion in tree sloths. J Mammal Evol 19:225–234. doi: 10.1007/s10914-011-9174-x

    Article  Google Scholar 

  • Nyakatura JA (2016) Learning to move on land. Science 353:120–121

    CAS  PubMed  Google Scholar 

  • Nyakatura JA, Andrada E (2013) A mechanical link model of two-toed sloths: no pendular mechanics during suspensory locomotion. Acta Theriol 58:83–93. doi: 10.1007/s13364-012-0099-4

    Article  Google Scholar 

  • Nyakatura JA, Fischer MS (2010a) Three-dimensional kinematic analysis of the pectoral girdle during upside-down locomotion of two-toed sloths (Choloepus didactylus, Linné 1758). Front Zool 7:1–16

    Google Scholar 

  • Nyakatura JA, Fischer MS (2010b) Functional morphology and three-dimensional kinematics of the thoraco-lumbar region of the spine of the two-toed sloth. J Exp Biol 213:4278–4290. doi: 10.1242/jeb.047647

    Article  PubMed  Google Scholar 

  • Nyakatura JA, Fischer MS (2011) Functional morphology of the muscular sling at the pectoral girdle in tree sloths: convergent morphological solutions to new functional demands? J Anat 219:360–374. doi: 10.1111/j.1469-7580.2011.01394.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Nyakatura JA, Petrovitch A, Fischer MS (2010) Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus. Zoology 113:221–234. doi: 10.1016/j.zool.2009.11.003

    Article  PubMed  Google Scholar 

  • Nyakatura JA, Stark H (2015) Aberrant back muscle function correlates with intramuscular architecture of dorsovertebral muscles in two-toed sloths. Mammal Biol 80:114–121. doi: 10.1016/j.mambio.2015.01.002

    Article  Google Scholar 

  • Oliver JD, Jones KE, Hautier L, Loughry WJ, Pierce SE (2016) Vertebral bending mechanics and xenarthrous morphology in the nine-banded armadillo (Dasypus novemcinctus). J Exp Biol 219:2991–3002. doi: 10.1242/jeb.142331

    Article  PubMed  Google Scholar 

  • Olson RA, Glenn ZD, Cliffe RN, Butcher MT (under review) Architectural properties of sloth forelimb muscles (Pilosa: Bradypodidae). J Mammal Evol

  • Olson RA, Womble MD, Thomas DR, Glenn ZD, Butcher MT (2016) Functional morphology of the forelimb of the nine-banded armadillo (Dasypus novemcinctus): comparative perspectives on the myology of Dasypodidae. J Mammal Evol 23:49–69. doi: 10.1007/s10914-015-9299-4

    Google Scholar 

  • Orr CM (2005) Knuckle-walking anteater: a convergence test of adaptation for purported knuckle-walking features of African Hominidae. Am J Phys Anthropol 128:639–658. doi: 10.1002/ajpa.20192

    Article  PubMed  Google Scholar 

  • Owen R (1832) On the osteology of the weasel-headed armadillo (Dasypus 6-cinctus, L.). Proc Zool Soc Lond 1832:134–138

    Google Scholar 

  • Owen R (1838) Geology of the Pampas. Note on the Glyptodon. In: Parish W (ed) Buenos Ayres and the Provinces of the Río de La Plata. John Murray, London, p 178b-e

  • Owen R (1839) Part I. Fossil Mammalia. In: The Zoology of the Voyage of HMS Beagle. Smith Elder and Co, London, p 111

    Google Scholar 

  • Owen R (1841) Description of a tooth and part of the skeleton of the Glyptodon clavipes, a large quadruped of the edentate order, to which belongs the tesselated bony armour described and figured by Mr. Clift in the former volume of the Transactions of the Geological Society; with a consideration of the question whether the Megatherium possessed an analogous dermal armour. Trans Geol Soc Lond 6:81–106. doi: 10.1038/004443a0

    Google Scholar 

  • Owen R (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 Megatherioid Quadrupeds in General. R. and J. E. Taylor, London

  • Owen R (1851) On the Megatherium (Megatherium americanum, Blumenbach). Part I. Preliminary observations on the exogenous processes of vertebrae. Phil Trans R Soc Lond 141:719–764

    Google Scholar 

  • Owen R (1855) On the Megatherium (Megatherium americanum, Cuvier and Blumenbach). Part II. Vertebrae of the trunk. Phil Trans R Soc Lond 145:359–388

    Google Scholar 

  • Owen R (1856) On the Megatherium (Megatherium americanum, Cuvier and Blumenbach). Part III. The skull. Phil Trans R Soc Lond 146:571–589

    Google Scholar 

  • Owen R (1858) On the Megatherium (Megatherium americanum, Cuvier and Blumenbach). Part IV. Bones of the anterior extremities. Phil Trans R Soc Lond 148:261–278

    Google Scholar 

  • Owen R (1859) On the Megatherium (Megatherium americanum, Cuvier and Blumenbach). Part V. Bones of the posterior extremities. Phil Trans R Soc Lon149:809–829

    Google Scholar 

  • Owen R (1861) Memoir on the Megatherium, or Giant Ground-sloth of America (Megatherium americanum, Cuvier). Williams and Norgate, London

    Google Scholar 

  • Oxnard CE (1993) Bone and bones, architecture and stress, fossils and osteoporosis. J Biomech 26:63–79. doi: 10.1016/0021-9290(93)90080-X

    Article  PubMed  Google Scholar 

  • Pander C, D’Alton E (1821) Das Riesen-Faulthier, Bradypus giganteus, abgebildet, beschrieben und mit den verwandten Geschlechtern verglichen. Isis Encycl Zeitschrift, Vorz für Naturgeschichte, vergleichende Anat u Physiol 862–863

  • Patel BA, Carlson KJ (2008) Apparent density patterns in subchondral bone of the sloth and anteater forelimb. Biol Lett 4:486–489. doi: 10.1098/rsbl.2008.0297

    Article  PubMed  PubMed Central  Google Scholar 

  • Patel BA, Ruff CB, Simons ELR, Organ JM (2013) Humeral cross-sectional shape in suspensory primates and sloths. Anat Rec 556:545–556. doi: 10.1002/ar.22669

    Article  Google Scholar 

  • Patiño SJ, Fariña RA (2017) Ungual phalanges analysis in Pleistocene ground sloths (Xenarthra, Folivora). Hist Biol. doi: 10.1080/08912963.2017.1286653

    Google Scholar 

  • Paula Couto C de (1979) Tratado de Paleomastozoologia. Academia Brasileira de Ciências, Rio de Janeiro

    Google Scholar 

  • Pictet FJ (1845) Traité Élémentaire de Paléontologie ou Histoire Naturelle des Animaux Fossiles Considérés dans leur Rapports Zoologiques et Géologiques.Tome 2. J.-B. Baillière, Paris

  • Pocock RI (1924) The external characters of the South American edentates. Proc Zool Soc Lond 1924:983–1031

    Google Scholar 

  • Pujos F, De Iuliis G, Argot C, Werdelin L (2007) A peculiar climbing Megalonychidae from the Pleistocene of Peru and its implication for sloth history. Zool J Linn Soc 149:179–235

    Google Scholar 

  • Pujos F, Gaudin TJ, De Iuliis G, Cartelle C (2012) Recent advances on variability, morpho-functional adaptations, dental terminology, and evolution of sloths. J Mammal Evol 19:159–169. doi: 10.1007/s10914-012-9189-y

    Article  Google Scholar 

  • Pujos F, Salas R (2004) A new species of Megatherium (Mammalia: Xenarthra: Megatheriidae) from the Pleistocene of Sacaco and Tres Ventanas, Peru. Palaeontology 47:579–604. doi: 10.1111/j.0031-0239.2004.00376.x

    Article  Google Scholar 

  • Quekett J (1849) On the intimate structure of bone, as composing the skeleton, in the four great classes of animals, viz., mammals, birds, reptiles, and fishes, with some remarks on the great value of the knowledge of such structure in determining the affinities of minute. Trans Microsc Soc Lond 2:46–58. doi: 10.1111/j.1365-2818.1849.tb05102.x

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Raj Pant S, Goswami A, Finarelli JA (2014) Complex body size trends in the evolution of sloths (Xenarthra: Pilosa). BMC Evol Biol 14:184. doi: 10.1186/s12862-014-0184-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Reynolds E (1931) The evolution of the human pelvis in relation to the mechanics of the erect posture. Pap Peabody mus Am Archaeol Ethnol Harvard Univ 11:255–334

    Google Scholar 

  • Ribeiro PRQ, Santos ALQ, Ribeiro LA, Souza TAM, Borges DCS, Souza RR, Pereira SG (2016) Movement anatomy of the gluteal region and thigh of the giant anteater Myrmecophaga tridactyla (Myrmecophagidae: Pilosa ). Pesqui Veterinária Bras 36:539–544

    Google Scholar 

  • Rincón AD, McDonald HG, Solórzano A, Núñez Flores M, Ruiz-Ramoni D (2015) A new enigmatic late Miocene mylodontoid sloth from northern South America. R Soc Open Sci 2:140256

    PubMed  PubMed Central  Google Scholar 

  • Rose KD, Emry RJ (1993) Relationships of Xenarthra, Pholidota, and Fossil “edentates”: the morphological evidence. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Placentals. Springer-Verlag, New York, pp 81–102

    Google Scholar 

  • Ryan TM, Ketcham RA (2005) Angular orientation of trabecular bone in the femoral head and its relationship to hip joint loads in leaping primates. J Morphol 265:249–263. doi: 10.1002/jmor.10315

    Article  PubMed  Google Scholar 

  • Saint-André P-A, De Iuliis G (2001) The smallest and most ancient representative of the genus Megatherium Cuvier, 1796 (Xenarthra, Tardigrada, Megatheriidae), from the Pliocene of the Bolivian Altiplano. Geodiversitas 23:625–645

    Google Scholar 

  • Salas R, Pujos F, Muizon C de (2005) Ossified meniscus and cyamo-fabella in some fossil sloths: a morpho-functional interpretation. Geobios 38:389–394. doi: 10.1016/j.geobios.2003.11.009

    Article  Google Scholar 

  • Santos PM, Chiarello AG, Ribeiro MC, Ribeiro JW, Paglia AP (2016) Local and landscape influences on the habitat occupancy of the endangered maned sloth Bradypus torquatus within fragmented landscapes. Mammal Biol 81:447–454. doi: 10.1016/j.mambio.2016.06.003

    Article  Google Scholar 

  • Scott WB (1903-1904) Mammalia of the Santa Cruz beds. Reports Princeton University Expedition to Patagonia 5:1–490. doi: 10.1525/mua.2006.29.2.153

    Article  Google Scholar 

  • Scott KM (1990) Postcranial dimensions of ungulates as predictors of body mass. In: Damuth J, MacFadden BJ (eds) Body Size in Mammalian Paleobiology: Estimation and Biological Implications. Cambridge University Press, Cambridge, pp 301–336

    Google Scholar 

  • Sénéchal L (1865) Notice sur l’Armure ou le Dermato-squelette et le Système Dentaire du Glyptodon clavipes et Particularités Biologiques de cet Animal, Déduites d’Après l’Étude de ses Restes Fossiles. Imprimerie Balitout, Questroy et Ce., Paris

  • Serres M (1863a) Notes sur deux articulations ginglymoïdales nouvelles existant chez le Glyptodon, la première entre la deuxième et la troisième vertèbre dorsale, la seconde entre la première et la deuxième pièce du sternum. C R Hebd Seances Acad Sci 56:885–888

    Google Scholar 

  • Serres M (1863b) Deuximème notes sur deux articulations ginglymoïdales nouvelles existant chez le Glyptodon, la première entre la deuxième et la troisième vertèbre dorsale, la seconde entre la première et la deuxième pièce du sternum. C R Hebd Seances Acad Sci 56:1028–1033

    Google Scholar 

  • Sesoko NF, Rahal SC, Bortolini Z, et al (2016) Gross anatomy and surgical approach to the humeral shaft in giant anteater (Myrmecophaga tridactyla). J Zoo Wildl Med 47:790–796. doi: 10.1638/2015-0236.1

    Article  PubMed  Google Scholar 

  • Shapiro LJ, Seiffert CVM, Godfrey LR, Jungers WL, Simons EL, Randria GFN (2005) Morphometric analysis of lumbar vertebrae in extinct Malagasy strepsirrhines. Am J Phys Anthropol 128:823–839. doi: 10.1002/ajpa.20122

    Article  PubMed  Google Scholar 

  • Shimer H (1903) Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals. III. Fossorial adaptations. Am Nat 37:819–825

    Google Scholar 

  • Shockey BJ (2001) Specialized knee joints in some extinct, endemic, South American herbivores. Acta Palaeontol Pol 46:277–288

    Google Scholar 

  • Shrivastava RK (1962) The deltoid musculature of the Edentata, Pholidota and Tubulidentata. Okajimas Folia Anat Jpn 38:25–38

    CAS  PubMed  Google Scholar 

  • Silla LM da R, Stephens NL (1976) Mechanical properties of diaphragm of three-toed sloth. Comp Biochem Physiol Part A Physiol 55:393–397. doi: 10.1016/0300-9629(76)90067-0

    CAS  Google Scholar 

  • Slijper EJ (1946) Comparative biologic-anatomical investigations on the vertebral column and spinal musculature of mammals. Verh der K Ned Akad van Wet Natuurkd 42:1–128

    Google Scholar 

  • Steadman DW, Martin PS, MacPhee RDE, Jull AJT, McDonald HG, Woods CA, Iturralde-Vinent M, Hodgins GWL (2005) Asynchronous extinction of late Quaternary sloths on continents and islands. Proc Natl Acad Sci U S A 102:11763–11768. doi: 10.1073/pnas.0502777102

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Steven E (2010) The ground sloth: Megalonyx. Trans Am Phil Soc New Ser 100:1–76.

    Google Scholar 

  • Stock C (1925) Cenozoic gravigrade edentates of western North America, with special reference to the Pleistocene Megalonychinae and Mylodontidae of Rancho La Brea. Carnegie Inst Wash Publ 331:1–206

    Google Scholar 

  • Straehl FR, Scheyer TM, Forasiepi AM, MacPhee RDE, Sánchez-Villagra MR (2013) Evolutionary patterns of bone histology and bone compactness in xenarthran mammal long bones. PLoS One 8:e69275. doi: 10.1371/journal.pone.0069275

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Straus JWL, Wislocki GB (1932) On certain similarities between sloths and slow lemurs. Bull Mus Comp Zool 74:45–56

    Google Scholar 

  • Sunquist ME, Montgomery GG (1973) Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). J Mammal 54:946–954

    CAS  PubMed  Google Scholar 

  • Superina M, Loughry WJ (2015) Why do xenarthrans matter? J Mammal 96:617–621. doi: 10.1093/jmammal/gyv099

    Article  Google Scholar 

  • Swanson PL (1945) Nature’s strap-hanger. Fauna 7:104–108

    Google Scholar 

  • Talmage RV, Buchanan GD (1954) The armadillo: a review of its natural history, ecology, anatomy and reproductive physiology. Rice Inst Pam 41:1–135

    Google Scholar 

  • Taylor BK (1978) The anatomy of the forelimb in the anteater (Tamandua) and its functional implications. J Morphol 157:347–368

    PubMed  Google Scholar 

  • Taylor BK (1985) Functional anatomy of the forelimb in vermilinguas (anteaters). In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, D. C., pp 163–171

    Google Scholar 

  • Tito G (2008) New remains of Eremotherium laurillardi (Lund, 1842) (Megatheriidae, Xenarthra) from the coastal region of Ecuador. J So Am Earth Sci 26:424–434. doi: 10.1016/j.jsames.2008.05.001

    Article  Google Scholar 

  • Tito G, De Iuliis G (2003) Morphofunctional aspects and palaeobiology of the manus in the giant ground sloth Eremotherium Spillmann 1948. Senckenb Biol 83:79–94

    Google Scholar 

  • Toledo PM (1996) Locomotor patterns within the Pleistocene sloths. PhD dissertation, University of Colorado, Boulder

    Google Scholar 

  • Toledo N (2016) Paleobiological integration of Santacrucian sloths (early Miocene of Patagonia). Ameghiniana 53:100–141

    Google Scholar 

  • Toledo N, Bargo MS, Cassini GH, Vizcaíno SF (2012) The forelimb of early Miocene sloths (Mammalia, Xenarthra, Folivora): morphometrics and functional implications for substrate preferences. J Mammal Evol 19:185–198. doi: 10.1007/s10914-012-9185-2

    Article  Google Scholar 

  • Toledo N, Bargo MS, Vizcaíno SF (2013) Muscular reconstruction and functional morphology of the forelimb of early Miocene sloths (Xenarthra, Folivora) of Patagonia. Anat Rec 296:305–325. doi: 10.1002/ar.22627

    Article  Google Scholar 

  • Toledo N, Bargo MS, Vizcaíno SF (2015) Muscular reconstruction and functional morphology of the hind limb of Santacrucian (early Miocene) sloths (Xenarthra, Folivora) of Patagonia. Anat Rec 298:842–864. doi: 10.1002/ar.22627

    PubMed  Google Scholar 

  • Toledo N, Bargo MS, Vizcaíno SF, De Iuliis G, Pujos F (2017) Evolution of body size in anteaters and sloths (Xenarthra, Pilosa): phylogeny, metabolism, diet and substrate preferences. Earth Environ Sci Trans R Soc Edinburgh 1–13. doi: 10.1017/S1755691016000177

    Google Scholar 

  • Toledo N, Cassini GH, Vizcaíno SF, Bargo MS (2014) Mass estimation in fossil sloths (Xenarthra, Folivora) from the early Miocene Santa Cruz Formation of Patagonia, Argentina. Acta Palaeontol Pol 59:267–280

  • Toledo N, De Iuliis G, Vizcaíno SF, Bargo MS (2017) Concept of pedolateral pes revisited: megatheriine ground sloths (Xenarthra, Folivora) as a study case. J Mammal Evol. (in press)

  • Urbani B, Bosque C (2007) Feeding ecology and postural behaviour of the three-toed sloth (Bradypus variegatus flaccidus) in northern Venezuela. Z Säugetierkd 72:321–329

    Google Scholar 

  • Ursing B (1932) Über Entwicklung und Bau des Hand-und Fuss-Skeletts bei Bradypus tridactylus. Acta Univ Lund 43:1–107

    Google Scholar 

  • VanBuren CS, Evans DC (2017) Evolution and function of anterior cervical vertebral fusion in tetrapods. Biol Rev 92:608–626. doi: 10.1111/brv.12245

    Article  PubMed  Google Scholar 

  • Vassal PA, Jouffroy FK, Lessertisseur J (1962) Musculature de la main et du pied du Paresseux Ai (Bradypus tridactylus L.). Folia Clin Biol (Sao Paulo) 31:142–153

    Google Scholar 

  • Vaughan TA (1972) Mammalogy. WB Saunders Co, Philadelphia

    Google Scholar 

  • Vickaryous MK, Sire JY (2009) The integumentary skeleton of tetrapods: origin, evolution, and development. J Anat 214:441–464. doi: 10.1111/j.1469-7580.2008.01043.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Vizcaíno SF, Bargo MS, Fariña RA (2008) Form, function, and paleobiology in xenarthrans. In: Vizcaino SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 87–99

  • Vizcaíno SF, Bargo MS, Kay RF, Milne N (2006) The armadillos (Mammalia, Xenarthra, Dasypodidae) of the Santa Cruz Formation (early–middle Miocene): an approach to their paleobiology. Palaeogeogr Palaeoclimatol Palaeoecol 237:255–269. doi: 10.1016/j.palaeo.2005.12.006

    Google Scholar 

  • Vizcaíno SF, Blanco RE, Bender JB, Milne N (2011) Proportions and function of the limbs of glyptodonts. Lethaia 44:93–101. doi: 10.1111/j.1502-3931.2010.00228.x

    Google Scholar 

  • Vizcaíno SF, Cassini GH, Toledo N, Bargo MS (2012b) On the evolution of large size in mammalian herbivores of Cenozoic faunas of Southern South America. In: Patterson B, Costa L (eds) Bones, Clones and Biomes. The History and Geography of Recent Neotropical Mammals. University Chicago Press, Chicago, pp 76–101

  • Vizcaíno SF, Fariña RA (1997) Diet and locomotion of the armadillo Peltephilus: a new view. Lethaia 30:79–86

    Google Scholar 

  • Vizcaíno SF, Fariña RA, Mazzetta GV (1999) Ulnar dimensions and fossoriality in armadillos. Acta Theriol 44:309–320

    Google Scholar 

  • Vizcaíno SF, Fernicola JC, Bargo MS (2012a) Paleobiology of Santacrucian glyptodonts and armadillos (Xenarthra, Cingulata). In: Vizcaíno SF, Kay RF, Bargo MS (eds) Early Miocene Paleobiology in Patagonia. Cambridge University Press, Cambridge, pp 194–215

  • Vizcaíno SF, Milne N (2002) Structure and function in armadillo limbs (Mammalia: Xenarthra: Dasypodidae). J Zool 257:117–127. doi: 10.1017/S0952836902000717

    Article  Google Scholar 

  • Vizcaíno SF, Milne N, Bargo MS (2003) Limb reconstruction of Eutatus seguini (Mammalia: Xenarthra: Dasypodidae). Paleobiological implications. Ameghiniana 40:89–101

  • Vizcaíno SF, Toledo N, Bargo MS (2017) Advantages and limitations in the use of extant xenarthrans (Mammalia) as morphological models for paleobiological reconstruction. J Mammal Evol. doi:10.1007/s10914-017-9400-2

  • Wainwright PC, Reilly SM (1994) Ecological Morphology: Integrative Organismal Biology. University of Chicago Press, Chicago

    Google Scholar 

  • Webb SD (1989) Osteology and relationships of Thinobadistes segnis, the first mylodont sloth in North America. In: Redford K, Eisenberg JF (eds) Adavances in Neotropical Mammalogy. The Sandhill Crane Press, Inc., Gainesville, pp 469–532

    Google Scholar 

  • White JL (1993) Indicators of locomotor habits in xenarthrans: evidence for locomotor heterogeneity among fossil sloths. J Vertebr Paleontol 13:230–242

    Google Scholar 

  • White JL (1997) Locomotor adaptations in Miocene xenarthrans. 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, pp 246–264

  • Windle BCA, Parsons FG (1899a) On the myology of the Edentata. Part I. Muscles of the head, neck and forelimb. Proc Zool Soc London 314–339

  • Windle BCA, Parsons FG (1899b) On the myology of the Edentata. Part II. Muscles of the hind limb; and summary of the conclusions respecting the musculature of the order. Proc Zool Soc Lond 990–1017

  • Wislocki GB (1928) Observations on the gross and microscopic anatomy of the sloths (Bradypus griseus griseus Gray and Choloepus hoffmanni Peters). J Morphol 46:317–397

    Google Scholar 

  • Witmer LM (1995) The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason J (ed) Functional Morphology in Vertebrate Paleontology. Cambridge University Press, Cambridge, pp 19–33

    Google Scholar 

  • Wolf D (2007) Osteoderm histology of extinct and recent Cingulata and Phyllophaga (Xenarthra, Mammalia): implications for systematics and biomechanical adaptation. Hallesches Jahrb Geowiss / Beih 23:145–151

    Google Scholar 

  • Wolf D, Kalthoff DC, Sander PM (2012) Osteoderm histology of the Pampatheriidae (Cingulata, Xenarthra, Mammalia): implications for systematics, osteoderm growth, and biomechanical adaptation. J Morphol 273:388–404. doi: 10.1002/jmor.11029

    Article  PubMed  Google Scholar 

  • Wood Jones F (1953) Some readaptations of the mammalian pes in response to arboreal habits. Proc Zool Soc Lond 123:33–41. doi: 10.1111/j.1096-3642.1953.tb00152.x

    Article  Google Scholar 

  • Yalden DW (1972) The form and function of the carpal bones in some arboreally adapted mammals. Acta Anat 82:383–406

    CAS  PubMed  Google Scholar 

  • Zeiger K (1927) Beitrage zur Kenntnis der Hautmuskulatur der Säugetiere. II Die Hautmuskeln am Rumpf des Kugelgürteltieres (Tolypeutes). Gegenbaurs Morphol Jahrb Leipzig 58:64

  • Zeiger K (1929) Beitrage zur Kenntnis der Hautmuskulatur der Säugetiere. III Die Hautmuskeln am Rumpf von Dasypus novemcinctus. Gegenbaurs Morphol Jahrb 63:260–291

    Google Scholar 

Download references

Acknowledgements

Olivier Lambert is acknowledged for helping to recover a bibliographical reference. Cécile Colin-Fromont is thanked for providing the photograph of the glyptodonts formerly exhibited at the Muséum national d’Histoire naturelle (Paris, France). Steven Jasinsky, Nick Milne, Stephanie Pierce, Sergio Vizcaíno, and Néstor Toledo should receive our gratitude for allowing reproduction of figures from their articles. Susana Bargo is thanked for co-organizing the Xenarthran symposium at the International Congress of Vertebrate Morphology (2016), from which this article stems, and for improving the manuscript acting as Guest Editor. Two anonymous reviewers and the Editor, John Wible, are also acknowledged for their useful inputs. EA was funded by the Alexander von Humboldt Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eli Amson.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Online Resource 1

(DOCX 67 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Amson, E., Nyakatura, J.A. The Postcranial Musculoskeletal System of Xenarthrans: Insights from over Two Centuries of Research and Future Directions. J Mammal Evol 25, 459–484 (2018). https://doi.org/10.1007/s10914-017-9408-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-017-9408-7

Keywords

  • Functional anatomy
  • Musculoskeletal system
  • Postcranium
  • Primates
  • Xenarthra