Skip to main content
Log in

The Narial Anatomy of Extinct and Extant Sloths (Xenarthra, Folivora): Osteological Anomalies in the Extant Two-Toed Sloth Choloepus

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The skeletal anatomy of the anterior narial region in mammals is complex, comprised of several bony and cartilaginous elements. Because it includes many cartilaginous components, preservation of this area in extant and extinct specimens is often incomplete. This, along with its complexity, means that this region of the cranium is generally understudied, with the exception of humans and a few select mammal species. The present study began with a cranial specimen of the extant Hoffmann’s two-toed sloth, Choloepus hoffmanni (Xenarthra, Folivora, Megalonychidae), that possessed several unusual well-preserved narial anomalies. In order to determine whether such features are present in other extant sloths, and if so, how frequently, we examined two- and three-toed sloth specimens from a variety of museum collections. Additionally, we examined museum specimens of extinct sloths known to possess unusual osseous narial structures, with the goal of better understanding the anatomy of the anterior opening of the nasal cavity in all sloths, living and extinct. A diverse series of unusual narial elements were found, including an internasal bone, an ossified anterior nasal septum, an os nariale, an ossified processus lateralis ventralis of the nasal capsule, and an internarial bar of varying composition and completeness. All of these features are present in Choloepus, although they are preserved in museum skulls infrequently, but none were found to be present in the three-toed sloth, Bradypus. An internarial bar, anteriorly elongated ossified nasal septum, and ossified processus lateralis ventralis were observed in several species of extinct mylodontid and megatheriid sloths, and an os nariale was recorded in the extant vermilinguan anteaters Cyclopes and Tamandua. It is not known how much of the variation we document in these features is genuine and how much is due to preservation issues. Given such uncertainty, it is difficult to assess the phylogenetic or functional significance of these features. We believe, however, that this is an area of the skull in Pilosa (sloths and anteaters) that merits further study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

modified from Bargo et al. (2006). Abbreviations: inb internarial bar, mx maxilla, n nasal, ns nasal septum, pm premaxilla, sp septal process of premaxilla. Scale bars equal 10 cm

Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adam PJ (1999) Choloepus didactylus (Pilosa: Megalonychidae). Mammal Species 621:1–8

    Article  Google Scholar 

  • Bargo MS (2001) The ground sloth Megtherium americanum: skull shape, bite forces, and diet. Acta Palaeontol Pol 46:173–192

    Google Scholar 

  • Bargo MS, Toledo N, Vizcaíno SF (2006) Muzzle of South American Pleistocene ground sloths (Xenarthra, Tardigrada). J Morphol 267:248–263

    Article  Google Scholar 

  • Brandoni D, Soibelzon E, Scarano A (2008) On Megatherium gallardoi (Mammalia, Xenarthra, Megatheriidae) and the Megatheriinae from the Ensenadan (lower to middle Pleistocene) of the Pampean region, Argentina. Geodiversitas 30 (4):793–804

  • Broom R (1927) Some further points on the structure of the mammalian basicranial axis. Proc Zool Soc Lond 1927:233–244

    Article  Google Scholar 

  • Buchholtz EA, Yozgyur ZM, Feldman A, Weaver AA, Gaudin TJ (2020) The therian sternum at the lateral somitic frontier: evolution of a composite structure J Zool:1–10. https://doi.org/10.1111/jzo.12809

  • Clifford AB, Witmer LM (2004) Case studies in novel narial anatomy: 3. Structure and function of the nasal cavity of saiga (Artiodactyla: Bovidae: Saiga tatarica). J Zool 264:217–230

    Article  Google Scholar 

  • DeBeer GR (1937) The Development of the Vertebrate Skull. University of Chicago Press, Chicago

    Google Scholar 

  • Evans HE, de Lahunta A (2012) Miller’s Anatomy of the Dog. Elsevier, St. Louis

    Google Scholar 

  • Ferigolo J (1981) The mesethmoid bone and the Edentata. An Acad brasil Ciênc 53:817–824

    Google Scholar 

  • Gardner AL (2007) Suborder Folivora Delsuc, Catzeflis, Stanhope and Douzery, 2001. In: Gardner AL (ed) Mammals of South America. Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, pp 157–168

    Google Scholar 

  • Gaudin TJ (2004) Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zool J Linnean Soc 140:255–305

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gaudin TJ, Nyakatura JA (2018) Epaxial musculature in armadillos, sloths, and opossums: functional significance and implications for the evolution of back muscles in the Xenarthra. J Mammal Evol 25(4):565–572. https://doi.org/10.1007/s10914-017-9402-0

    Article  Google Scholar 

  • Gaudin TJ, Wible JR (2006) Chapter 6. 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 153–198

    Google Scholar 

  • Gaudin TJ, Wible JR, Hopson JA, Turnbull WD (1996) Reexamination of the morphological evidence for the Cohort Epitheria (Mammalia, Eutheria). J Mammal Evol 3(1):1–79

    Article  Google Scholar 

  • Grassé P-P (1955) Ordre des Édentés. In: Grassé PP (ed) Traité de Zoologie, vol. 17 Mammifères. Masson et Cie, Paris, pp 1182–1266

    Google Scholar 

  • Hayssen V (2009) Bradypus tridactylus (Pilosa: Bradypodidae). Mammal Species 839:1–9

    Article  Google Scholar 

  • Hayssen V (2010) Bradypus variegatus (Pilosa: Bradypodidae). Mammal Species 42:19–32. https://doi.org/10.1644/850.1

    Article  Google Scholar 

  • Hayssen V (2011) Choloepus hoffmanni (Pilosa: Megalonychidae). Mammal Species 43:37–55. https://doi.org/10.1644/873.1

    Article  Google Scholar 

  • Hoffstetter R (1952) Les mammifères Pléistocènes de la République de l’Équateur. Soc Géol France 31:375–488

    Google Scholar 

  • Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the Age of Dinosaurs. Origins, Evolution and Structure. Columbia University Press, New York

    Book  Google Scholar 

  • Kraglievich L (1934) Conocimiento de Mylodon darwinii Owen y especies afines. Rev Mus. de La Plata 34:255–292

    Google Scholar 

  • Kuhn HJ (1971) Die Entwicklung und Morphologie des Schädels von Tachyglossus aculeatus. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 528:1–224.

  • Lyon LM, Powell C, McDonald HG, Gaudin TJ (2016) Premaxillae of the extinct megalonychid sloths Acratocnus, Neocnus, and Megalonyx, and their phylogenetic implications (Mammalia, Xenarthra). J Mammal Evol 23:121–132. https://doi.org/10.1007/s10914-015-9308-7

  • Macrini T (2012) Comparative morphology of the internal nasal skeleton of adult marsupials based on X-ray computed tomography. Bull Am Mus Nat Hist 365:1–91

    Article  Google Scholar 

  • McDonald HG (1987) A systematic review of the Plio-Pleistocene scelidotherine ground sloths (Mammalia: Xenarthra: Mylodontidae). Dissertation, University of Toronto, Toronto

  • McDonald HG (2003) Xenarthran skeletal anatomy: primitive or derived? (Mammalia, Xenarthra). Senckenberg biol 83(1):5–17

    Google Scholar 

  • McKenna MC (1975) Towards a phylogenetic classification of the Mammalia. In: Luckett WP, Szalay FS (eds) Phylogeny of the Primates: A Multidisciplinary Approach. Plenum Press, New York, pp 21–46

    Chapter  Google Scholar 

  • Moore WJ (1981) The Mammalian Skull. Cambridge University Press, Cambridge

    Google Scholar 

  • Novacek MJ (1993) Patterns of diversity in the mammalian skull. In: Hanken J, Hall BK (eds) The Skull, Volume 2: Patterns of Structural and Systematic Diversity. University of Chicago Press, Chicago, pp 438–546

    Google Scholar 

  • O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, Goldberg SL, Kraatz BP, Luo Z-X, Meng J, Ni X, Novacek MJ, Perini FA, Randall Z, Rougier GW, Sargis EJ, Silcox MT, Simmons NB, Spaulding M, Velazco PM, Weksler M, Wible JR, Cirranello AL (2013) The placental mammal ancestor and the post-KPg radiation of placentals. Science 339:662–667. https://doi.org/10.1126/science.1229237

    Article  CAS  PubMed  Google Scholar 

  • Owen R (1856) On the Megatherium. Part III. The skull. Philos Trans R Soc Lond 146:571–589

    Google Scholar 

  • Parker WK (1885) On the structure and development of the skull in the Mammalia. Part II. Edentata. Philos Trans R Soc Lond 176:1–1199

    Google Scholar 

  • Patterson B, Segall W, Turnbull WD, Gaudin TJ (1992) The ear region in xenarthrans (= Edentata: Mammalia). Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana Geol new series 24:1–78

  • Pick TP, Howden R (1977) Gray’s Anatomy, 15th ed. Bounty Books, New York

    Google Scholar 

  • Reinhardt J (1879) Beskrivelse af Hovedskallen af et Kæmpe- dovendyr, Grypotherium darwinii, fra La Plata-Landenes plejstocene Dannelser. Vidensk Selsk Skr 5: 355–380

    Google Scholar 

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

    Chapter  Google Scholar 

  • Springer MS, Foley NM, Brady PL, Gatesy J, Murphy WJ (2019) Evolutionary models for the diversification of placental mammals across the KPg boundary. Front Genetics 10:1241. https://doi.org/10.3389/fgene.2019.01241

  • Upham NS, Esselstyn JA, Jetz W (2019) Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol 17(12):e3000494

  • Weber M (1928) Die Säugetiere. Gustav Fischer, Jena

  • Wegner G (1950) Unterschiede der Nasenlochgestaltung und des Os nariale bei den Säugetieren (Choloepus) und den Bauriamorphen. Verh Anat Gesell 28:104–111

  • Wetzel R (1985) The identification and distribution of recent Xenarthra (= Edentata). In: Montgomery GG (ed) The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington DC, pp 5–21

    Google Scholar 

  • Wible JR (2008) On the cranial osteology of the Hispaniolan solenodon, Solenodon paradoxus Brandt, 1833 (Mammalia, Lipotyphla, Solenodontidae). Ann Carnegie Mus 77:321–402

    Article  Google Scholar 

  • Wible JR, Gaudin TJ (2004) On the cranial osteology of the yellow armadillo Euphractus sexcinctus (Dasypodidae, Xenarthra, Placentalia). Ann Carnegie Mus 73:117–196

    Google Scholar 

  • Wible JR, Miao D, Hopson JA (1990) The septomaxilla of fossil and recent synapsids and the problem of the septomaxilla of monotremes and armadillos. Zool J Linnean Soc 98:203–228

    Article  Google Scholar 

  • Wible JR, Rougier GW (2017) Craniomandibular anatomy of the subterranean meridiolestidan Necrolestes patagonensis Ameghino, 1891 (Mammalia, Cladotheria) from the early Miocene of Patagonia. Ann Carnegie Mus 84:183–252

    Article  Google Scholar 

  • Woodward AS (1900) On some remains of Grypotherium (Neomylodon) listai and associated mammals from a cavern near Consuelo Cove, Last Hope Inlet, Patagonia. Proc Zool Soc Lond 1900:64–79

    Article  Google Scholar 

  • Zeller U, Wible JR, Elsner M (1993) New ontogenetic evidence on the septomaxilla of Tamandua and Choloepus (Mammalia, Xenarthra), with a reevaluation of the homology of the mammalian septomaxilla. J Mammal Evol 1:31–44

    Article  Google Scholar 

Download references

Acknowledgements

We thank Andy Biewener (Harvard University, Cambridge, MA) for donation of the original Choloepus hoffmanni specimen (UTCM 1912) used in this report. That skull was cleaned by the late great Bill Stanley (Department of Mammalogy, Field Museum of Natural History [FMNH], Chicago, IL), with special attention paid to preserving nasal structures. For access to additional specimens, we thank Bill Simpson, John Flynn, and Ken Angielcyzk (Department of Geology, FMNH); Adam Ferguson, Bill Stanley, Bruce Patterson (Department of Mammalogy, FMNH); Bernardino Mamani Quispe (Museo Nacional de Historia Natural, La Paz, Bolivia); Martin Ezcurra, Laura Cruz, and Alejandro Kramarz (Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina); and Susana Bargo and Sergio Vizcaíno (Museo de La Plata [MLP], La Plata, Argentina). We thank François Pujos (IANIGLA, CONICET, Mendoza, Argentina), Alberto Boscaini (Univ. of Buenos Aires & CONICET, Buenos Aires, Argentina), and Adam Ferguson (FMNH) for graciously providing specimen photos used in this work, and Susana Bargo (MLP) for permission to modify photos from her excellent work on the muzzle of sloths. We also thank Julia Morgan Scott for her ever-excellent work in preparing the drawings for this paper. Lastly, we thank the two anonymous reviewers who helped in improving the manuscript. The work of TJG and KMS was supported in part by the University of Tennessee at Chattanooga and the Bramblett gift fund. The work of JRW was supported by National Science Foundation Grant DEB 1654949, and the R.K. Mellon North American Mammal Research Institute.

TJG: I want to begin this personal acknowledgement by stating what an honor it is to participate in this festschrift honoring my colleague and co-author, Dr. John Wible. Let me also make clear that John was unaware he was contributing to his own festschrift, a fact for which I hope he will forgive me. After some discussion with the other co-editors of this volume, we decided that his participation in this paper, and hence, in this volume, was appropriate. Certainly this is the kind of paper for which he is justifiably well-known – one that describes in detail novel aspects of mammalian cranial anatomy, interpreting it in the light of John’s vast knowledge of the subject. I also want to affirm how appropriate it is that John is being honored with this festschrift. His work with the Journal of Mammalian Evolution has been transformative, and he is personally responsible for its success to a remarkable degree. For myself, it has been my privilege to work with John for many years. I have not always been the best collaborator, often weighed down by teaching and administrative duties, but his understanding and support have been critical to whatever research success I have achieved. I am grateful for all he has taught me, but moreso, for the years of friendship we have enjoyed!

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy J. Gaudin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gaudin, T.J., Smith, K.M. & Wible, J.R. The Narial Anatomy of Extinct and Extant Sloths (Xenarthra, Folivora): Osteological Anomalies in the Extant Two-Toed Sloth Choloepus. J Mammal Evol 28, 1181–1192 (2021). https://doi.org/10.1007/s10914-021-09562-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-021-09562-9

Keywords

Navigation