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Ulna of Extant Xenarthrans: Shape, Size, and Function

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Abstract

Xenarthra, one of the major clades of placentals, comprises two different lineages (sloths and anteaters, and armadillos) with extant representatives showing strongly different morphologies and life habits. Sloths are arboreal herbivores, anteaters are insectivores with digging/climbing abilities, and armadillos are terrestrial diggers with varied diets. The ulna is one of the forelimb elements that exhibits distinct morphological specializations for different abilities (e.g., digging and climbing). A sample of xenarthrans was analyzed in this work from a functional and ecological perspective, using 2-D geometric morphometry. The analyses performed were a Principal Components Analysis (PCA), a regression of the shape on the centroid size, and a PCA with the residuals from the regression. The first PCA shows that the morphospace is strongly influenced by differences in length of the olecranon with respect to the shaft between the three clades. Allometry was detected for the whole sample. In the residual PCA, the allometry-free morphospace allows the differentiation between the ecological categories of substrate preference: armadillos and giant anteaters (terrestrial) are located towards the negative side of PC1, while sloths and silky anteaters (arboreal) are located near the positive end, with collared anteaters (semiarboreal) placed near the center. The terrestrial taxa present a more robust diaphysis, and a comparatively long, diaphysis-aligned olecranon, while the arboreal taxa show a relatively long ulna with an anteriorly curved shaft and an anteriorly deflected carpal facet. The ulnar curvature has biomechanical implications in relation to the bone response to different loadings produced in the context of posture and locomotion in each substrate.

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Data Availability

All data generated during our analyses in the current study are available from the corresponding author on reasonable request.

References

  • Abba AM, Tognelli MF, Seitz VP, Bender JB, Vizcaíno SF (2012) Distribution of extant xenarthrans (Mammalia: Xenarthra) in Argentina using species distribution models. Mammalia 76: 123–136

    Google Scholar 

  • Adams, DC, Collyer ML, Kaliontzopoulou A (2018) Geomorph: software for geometric morphometric analyses. R package version 3.0.6. https://cran.r-project.org/package=geomorph

  • Amson E, Nyakatura JA (2017) The postcranial musculoskeletal system of xenarthrans: insights from over two centuries of research and future. J Mammal Evol. https://doi.org/10.1007/s10914-017-9408-7

    Article  Google Scholar 

  • Amson E, Nyakatura JA (2018) Palaeobiological inferences based on long bone epiphyseal and diaphyseal structure - the forelimb of xenarthrans (Mammalia). bioRxiv: 318121, ver. 5 peer-reviewed and recommended by PCI Paleo. https://doi.org/10.1101/318121

  • Argot C (2001) Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J Morphol 247: 51–79

    CAS  PubMed  Google Scholar 

  • Bargo MS, Vizcaíno SF, Archuby F, 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 

  • Bookstein FL (1989) Principal warps: thin-plate splines and the decomposition of deformations. IEEE T Pattern Anal 11: 567–585

    Google Scholar 

  • Cassini GH, Vizcaíno SF, Bargo MS (2012) Body mass estimation in early Miocene native South American ungulates: a predictive equation based on 3D landmarks. J Zool 287: 53–64

    Google Scholar 

  • Delsuc F, Vizcaíno SF, Douzery EJP (2004) Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans. BMC Evol Biol 4:11

    PubMed  PubMed Central  Google Scholar 

  • Ercoli MD, Prevosti FJ (2011) Estimación de masa de las especies de Sparassodonta (Mammalia, Metatheria) de edad Santacrucense (Mioceno temprano) a partir del tamaño del centroide de los elementos apendiculares: inferencias paleoecológicas. Ameghiniana 48: 462–479

    Google Scholar 

  • de Mendiburu F (2019) agricolae: statistical procedures for agricultural research. R package version 1.3-1. https://CRAN.R-project.org/package=agricolae

  • Fujiwara SI, 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

    PubMed  PubMed Central  Google Scholar 

  • Gardner AL (2007) Magnorder Xenarthra. In: Gardner AL (ed) Mammals of South America; Vol I Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, pp 127–177

    Google Scholar 

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

    Google Scholar 

  • Henderson K, Pantinople J, McCabe K, Richards HL, Milne N (2017) Forelimb bone curvature in terrestrial and arboreal mammals. PeerJ. doi https://doi.org/10.7717/peerj.3229

    Article  PubMed  PubMed Central  Google Scholar 

  • Hildebrand M, Goslow GE (2001) Analysis of Vertebrate Structure, 5th ed. Wiley, New York

    Google Scholar 

  • Kay RF (2019) Leonard B. Radinsky (1937–1985), radical biologist. J Mammal Evol. https://doi.org/10.1007/s10914-019-09479-4

    Article  Google Scholar 

  • Kendall DG (1986) [Size and Shape spaces for landmark data in two dimensions]: comment. Stat Sci 1:222–226

    Google Scholar 

  • Kilbourne BM, Hutchinson JR (2019) Morphological diversification of biomechanical traits: mustelid locomotor specializations and the macroevolution of long bone cross-sectional morphology. BMC Evol Biol. https://doi.org/10.1186/s12862-019-1349-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Klingenberg CP, Zimmermann M (1992) Static, ontogenetic, and evolutionary allometry: a multivariate comparison in nine species of water striders. Am Nat 140:601–620

    Google Scholar 

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

    Google Scholar 

  • 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 24–36

    Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Milne N (2016) Curved bones: an adaptation to habitual loading. J Theor Biol 407: 18–24

    PubMed  Google Scholar 

  • Milne N (2019) Curved bones: primate ulna in arboreal and terrestrial species. J Morphol 280: S18

    Google Scholar 

  • Muñoz NA, Toledo N, Candela AM, Vizcaíno SF (2019) Functional morphology of the forelimb of early Miocene caviomorph rodents from Patagonia. Lethaia 52:91–106

    Google Scholar 

  • Nowak RM (1999) Walker’s Mammals of the World, 6th ed. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Nyakatura JA (2012) The convergent evolution of suspensory posture and locomotion in tree sloths. J Mammal Evol 19:225–234

    Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (https://www.R-project.org/)

    Google Scholar 

  • Radinsky LB (1987) The Evolution of Vertebrate Design. University of Chicago Press, Chicago

    Google Scholar 

  • Rasband WS (1997–2007) ImageJ. US National Institute of Health, Bethesda

  • Rodrigues FHG, Medri IM, de Miranda GHB, Camilo-Alves C, Mourao G (2008) Anteater behavior and ecology. In: Vizcaíno SF, Loughry WJ (eds) The Biology of the Xenarthra. University Press of Florida, Gainesville, pp 257–68

    Google Scholar 

  • Rohlf FJ (2015) The tps series of software. Hystrix 26:1–4

    Google Scholar 

  • Shimer HW (1903) Adaptation to arboreal, aquatic and cursorial habits in mammals. Am Nat 37: 651–825

    Google Scholar 

  • Springer MS, Murphy WJ, Eizirik E, O’Brien SJ (2002) Placental mammal diversification and the Cretaceous–Tertiary boundary. Proc Natl Acad Sci USA 100: 1056–1061

    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, pp 151–171

    Google Scholar 

  • Toledo N (2016) Conceptual and methodological approaches for a paleobiological integration: the Santacrucian sloths (early Miocene of Patagonia) as a study case. 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

    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

    Google Scholar 

  • Vizcaíno SF, Bargo MS (2019) Views on the Form-Function correlation and biological design. J Mammal Evol. https://doi.org/10.1007/s10914-019-09487-4

    Article  Google Scholar 

  • Vizcaíno SF, Bargo MS, Cassini GH, Toledo N (2016) Forma y función en paleobiología de vertebrados. Edulp, La Plata

    Google Scholar 

  • Vizcaíno SF, Blanco ER, Bender BJ, Milne N (2011) Proportions and function of the limbs of glyptodonts. Lethaia, 44: 93–101

    Google Scholar 

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

    Google Scholar 

  • Vizcaíno SF, Loughry WJ (2008) Xenarthran biology, past present and future. In: Vizcaíno SF, Loughry WJ (eds) The biology of the Xenarthra. University Press of Florida, Gainesville, pp 1–7

    Google Scholar 

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

    Google Scholar 

  • Vizcaíno SF, Zárate M, Bargo MS, Dondas A (2001) Pleistocene large burrows in the Mar del Plata area (Buenos Aires Province, Argentina) and their probable builders. Acta Palaeontol Pol 46: 157–169

    Google Scholar 

  • Young RJ, Coelho CM, Wieloch DR (2003) A note on the climbing abilities of the giant anteaters, Myrmecophaga tridactyla (Xenarthra, Myrmecophagidae). Bol Mus Biol Mello Leitão, Nova Sér 15: 41–46

    Google Scholar 

  • Zar JH (1999) Biostatistical Analysis, 4 ed. Prentice Hall, Eryelwood Cliffs

    Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric Morphometrics for Biologists: A Primer. Elsevier, New York

    Google Scholar 

Download references

Acknowledgements

We thank the following persons and institutions: D. Verzi and I. Olivares (MLP), Pablo Teta (MACN), N. Simmons (AMNH), and B. Patterson (FMNH) for access to mammalogy collections; to the organizers of the XXXI Jornadas Argentinas de Mastozoologia, A. Chemisquy and F. Prevosti for allowing GHC and NT to organize the symposium “El paradigma de correlación forma-función en mastozoología: un tributo a Leonard Radinsky (1937–1985)”; La Rioja, Argentina, October 25th, 2018. To S.F. Vizcaíno and M.S. Bargo for introducing us to the impressive work and conceptualizations of Radinsky. The comments and corrections of the Editor and Guest Editor, Nick Milne, and one anonymous reviewer greatly enhanced this manuscript. This is a contribution to the projects PICT 2013 − 0143 of the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) and Universidad Nacional de La Plata (UNLP) N750.

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Authors and Affiliations

  1. División Paleontología Vertebrados, Museo de La Plata, Unidades de Investigación Anexo Museo, Facultad de Ciencias Naturales y Museo, Av. 60 and 122, 1900, La Plata, Argentina

    Néstor Toledo & Nahuel A. Muñoz

  2. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ciudad Autónoma de Buenos Aires, Argentina

    Néstor Toledo, Nahuel A. Muñoz & Guillermo H. Cassini

  3. Departamento de Ciencias Básicas, Universidad Nacional de Luján, Ruta 5 and Av. Constitución s/n, Luján, Buenos Aires, 6700, Argentina

    Nahuel A. Muñoz & Guillermo H. Cassini

  4. División Mastozoología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Ángel Gallardo 470, C1405DJR, Ciudad Autónoma de Buenos Aires, Argentina

    Guillermo H. Cassini

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  1. Néstor Toledo
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  2. Nahuel A. Muñoz
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  3. Guillermo H. Cassini
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Correspondence to Néstor Toledo.

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Toledo, N., Muñoz, N.A. & Cassini, G.H. Ulna of Extant Xenarthrans: Shape, Size, and Function. J Mammal Evol 28, 35–45 (2021). https://doi.org/10.1007/s10914-020-09503-y

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