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Internal Morphology of Osteoderms of Extinct Armadillos and Its Relationship with Environmental Conditions

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Abstract

The most complete and continuous fossil record of armadillos is composed mostly by isolated osteoderms, frequently found in paleontological and archaeological sites that bear continental South American mammals. Their external morphology has been used to define several species. In the last decade, many authors have focused on the internal structure of vertebrate osteoderms using histological and paleohistological studies. These studies allowed identification of useful features in systematic and phylogenetic contexts. In armadillos, osteoderms are constituted by compact bone tissue (primary and secondary osteons, and concentric layers or lamellae) that delimits cavities, which could contain different soft tissues (adipose tissue, hair follicles, bone marrow, and sweat and sebaceous glands). Traditional paleohistological techniques have allowed the recognition of homologous cavities to those found in osteoderms of current species and from comparison deduce which kind of tissue could had occupied them. We have recently utilized 3D reconstructions in osteoderms of extant species of armadillos to analyze the micromorphology, disposition, and the relationship of different cavities and understand them in depth. Here, we present the results of the application of paleohistology and microtomography in osteoderms of representatives of diferent taxa of extinct Dasypodidae (Astegotheriini, Stegotheriini, “Utaetini,” Euphractini, Eutatini), which allowed us to compare homologous structures based on their three-dimensional reconstruction. The results, added to the previous external morphology studies, have allowed us to define morphological patterns (consistent within each linage). The variation of the volume and extension of cavities associated with different tissues could be strongly associated with changes in the climate and environmental conditions of the species distribution areas.

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References

  • Abrantes EAL, Bergqvist LP (2006) Proposta filogenética para os Dasypodidae (Mammalia: Cingulata). In: Gallo V, Brito PM, Silva HMA, Figueiredo FJ (Org) Paleontologia de Vertebrados: Grandes Temas e Contribuições Científicas. 1 ed. Interciência, Rio de Janeiro v 1, pp 261–274

    Google Scholar 

  • Alexander CM, Kasza I, Yen CE, Reeder SB, Hernando D, Gallo RL, Jahoda CAB, Horsley V, MacDougald OA (2015) Dermal white adipose tissue: a new component of the thermogenic response. J Lip Res 56 (11): 2061–2069

    Article  CAS  Google Scholar 

  • Asher RJ, Bennett N, Lehmann T (2009) The new framework for understanding placental mammal evolution. BioEssays 31:853–864

  • Billet G, Hautier L, Muizon C de, Valentin X (2011) Oldest cingulate skulls provide congruence between morphological and molecular scenarios of armadillo evolution. Proc R Soc B 278: 2791–2797. doi: 10.1098/rspb.2010.2443

  • Carlini AA, Ciancio MR, Chimento NR (2008) Neoglyptatelus (Mammalia, Cingulata), caracteres y latitudes, en una discusión de afinidades. III Congreso Latinoamericano de Paleontología de Vertebrados Resúmenes: 49. Neuquén, Argentina

  • Carlini AA, Ciancio MR, Flynn JJ, Scillato-Yané GJ, Wyss AR (2009) The phylogenetic and biostratigraphic significance of new armadillos (Mammalia, Xenarthra, Dasypodidae, Euphractinae) from the Tinguirirican (early Oligocene) of Chile. J Syst Palaeontol 7(4):489–503

    Article  Google Scholar 

  • Carlini AA, Ciancio MR, Scillato-Yané GJ (2010) Middle Eocene-early Miocene Dasypodidae (Xenarthra) of southern South America, successive faunas in Gran Barranca; biostratigraphy and palaeoecology. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 106–129

    Google Scholar 

  • Carlini AA, Scillato-Yané GJ (1996) Chorobates recens (Xenarthra, Dasypodidae) y un análisis de la filogenia de los Euphractini. Rev Mus La Plata (NS) 9 (59): 225–238

    Google Scholar 

  • Castro MC, Ciancio MR, Pacheco V, Salas-Gismondi RM, Bostelmann JE, Carlini AA (2015) Reassessment of the hairy longnosed armadillo “Dasypus” pilosus (Xenarthra, Dasypodidae) and revalidation of the genus Cryptophractus Fitzinger, 1856. Zootaxa 3947(1):30–48

    Article  PubMed  Google Scholar 

  • Cena K, Monteith JL (1975a) Transfer processes in animal coats. I. Radiative transfer. Proc R Soc Lond B 188: 377–393

    Article  CAS  PubMed  Google Scholar 

  • Cena K, Monteith JL (1975b) Transfer processes in animal coats. II. Conduction and convection. Proc R Soc Lond B 188: 395–411

    Article  CAS  PubMed  Google Scholar 

  • Ciancio MR (2010) Los Dasypodoidea (Mammalia, Xenarthra) del Deseadense (Oligoceno) de América del Sur. Su importancia filogenética y bioestratigráfica. Unpublished Doctoral Thesis, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, n°1098. Pp. 290 + XVI, 106 figures, 5 tables and 4 appendices

  • Ciancio MR (2016) Los armadillos (Dasypodidae, Xenarthra) del Cenozoico temprano-medio de Argentina: Aspectos evolutivos, bioestratigráficos y biogeográficos. Contrib Cient MACN “Bernardino Rivadavia” 6:231-247

  • Ciancio MR, Carlini AA (2007) Morfología del sistema pilífero en Eutatinos (Xenarthra, Dasypodidea) del Oligoceno de Patagonia (Argentina). III Congreso de Mastozoología en Bolivia. Santa Cruz de La Sierra, Bolivia. Resúmenes: 49-50

  • Ciancio MR, Carlini AA, Campbell, KE, Scillato-Yané, GJ (2013) New Palaeogene cingulates (Mammalia, Xenarthra) from Santa Rosa, Perú and their importance in the context of South American faunas. J Syst Palaeontol 11(6):727–741

    Article  Google Scholar 

  • Da Costa Pereira PVLG, Victer GD, Porpino KO, Bergqvist LP (2014) Osteoderm histology of late Pleistocene cingulates from the intertropical region of Brazil. Acta Palaeontol Pol 59 (3): 543–552

  • Davis LB, Birkebak CB (1974) On the transfer of energy in layers of fur. Biophysical Journal 14 (4):249–268

    Article  PubMed  PubMed Central  Google Scholar 

  • Delsuc F, Superina M, Tilak MK, Douzery EJ, Hassanin A (2012) Molecular phylogenetics unveils the ancient evolutionary origins of the enigmatic fairy armadillos. Mol Phylogenet Evol 62(2): 673–680

  • Dozo MT, Ciancio MR, Bouza P, Martínez G (2014) Nueva asociación de mamíferos del Paleógeno en el este de la Patagonia (provincia de Chubut, Argentina): implicancias biocronológicas y paleobiogeográficas. Andean Geol 41 (1): 224–247

    Google Scholar 

  • Engelmann GF (1985) The phylogeny of the Xenarthra. In: Montgomery GG (ed) The Evolution and Ecology of Armadillos, Sloths and Vermilinguas. Smithsonian Institution Press, Washington, D.C., pp 51–64

    Google Scholar 

  • Feng X, Castro MC, McBee AK, Papeş M (2017) Hiding in a cool climatic niche in the tropics? An assessment of the ecological biogeography of hairy long-nosed armadillos (Dasypus pilosus). J Trop Conserv Sci 10:1–13

    Google Scholar 

  • Fernícola JC, Vizcaíno SF (2008) Revisión del género Stegotherium Ameghino, 1887 (Mammalia, Xenarthra, Dasypodidae). Ameghiniana 45 (2): 321–332

    Google Scholar 

  • Francia A, Ciancio MR (2013) First record of Chaetophractus villosus (Mammalia, Dasypodidae) in the late Pleistocene of Corrientes Province (Argentina). Rev Mus La Plata 13 (70): 1–9

    Google Scholar 

  • Gaudin TJ, Wible JR (2006) The phylogeny of living and extinct armadillos (Mammalia, Xenarthra, Cingulata): a craniodental analysis. In: Carrano MT, Gaudin TJ, Blob RW, Wible JR (eds) Amniote Paleobiology: Perspectives on the Evolution of Mammals, Birds and Reptiles. University of Chicago Press, Chicago, pp 153–198

    Google Scholar 

  • Goin FJ, Woodburne MO, Zimicz AM, Martin GM, Chornogubsky L (2016) A Brief History of South American Metatherians. Evolutionary Contexts and Intercontinental Dispersals. Springer Earth System Sciences series, Springer, Dordretch, 237 pp

    Book  Google Scholar 

  • González-Ruiz LR, Góis F, Ciancio MR, Scillato-Yané GJ (2013) Los Peltephilidae (Mammalia, Xenarthra) de la Formación Collón Curá (Colloncurense, Mioceno Medio) Argentina. Rev Bras Paleontol 16(2): 319–330

    Article  Google Scholar 

  • Hill RV (2005) Integrative morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. Syst Biol 54: 530–547

    Article  PubMed  Google Scholar 

  • Hill RV (2006) Comparative anatomy and histology of xenarthran osteoderms. J Morphol 267:1441–1460

    Article  PubMed  Google Scholar 

  • Holmes WW, Simpson GG (1931) Pleistocene exploration and fossil edentates in Florida. Bull Am Mus Nat His 59: 383–418

    Google Scholar 

  • Krmpotic CM, Carlini AA, Scillato-Yané GJ (2009a) The species of Eutatus (Mammalia, Xenarthra): assessment, morphology and climate. Quaternary Internatl 210: 66–75

    Article  Google Scholar 

  • Krmpotic CM, Ciancio MR, Barbeito CG, Mario RC, Carlini AA (2009b) Osteoderm morphology in recent and fossil Euphractinae xenarthrans. Acta Zool 90:339–351

    Article  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(4): 601–616

    Article  Google Scholar 

  • Kvadsheim PH, Aarseth JJ (2002) Thermal function of phocid seal fur. Marine Mammal Sci 18(4):952–962

    Article  Google Scholar 

  • Kvadsheim PH, Folkow LP, Blix AS (1994) A new device for measurement of the thermal conductivity of fur and blubber. J Thermal Biol 19(6): 431–435

    Article  Google Scholar 

  • Legarreta L, Uliana MA (1994) Asociaciones de fósiles y hiatos en el Supracretácico-Neógeno de Patagonia: una perspectiva estratigráfico-secuencial. Ameghiniana 31:257–281

    Google Scholar 

  • Liwanag HE, Berta A, Costa DP, Budge SM, Williams TM (2012) Morphological and thermal properties of mammalian insulation: The evolutionary transition to blubber in pinnipeds. Biol J Linn Soc 107(4): 774–787

    Article  Google Scholar 

  • McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. J Mammal 61(4):606–627

    Article  Google Scholar 

  • Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Taiz LLS, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2013) Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science 334(6055):521–524

  • Ortiz-Jaureguizar E, Cladera G (2006) Paleoenvironmental evolution of southern South America during the Cenozoic. J Arid Environ 66: 489–532

    Article  Google Scholar 

  • Pascual R, Odreman Rivas OE (1971) Evolución de las comunidades de vertebrados del Terciario argentino. Los aspectos paleozoogeográficos y paleoclimáticos relacionados. Ameghiniana 8: 372–412

    Google Scholar 

  • Pascual R, Ortiz-Jaureguizar E (1990) Evolving climates and mammal faunas in Cenozoic South America. J Hum Evol 19: 23–60

    Article  Google Scholar 

  • Pascual R, Ortiz-Jaureguizar E, Prado JL (1996) Land-mammals: paradigm for Cenozoic South American geobiotic evolution. In: Arratia G (ed) Contributions of Southern South America to Vertebrate Paleontology. Münchner Geowiss Abh 30(A): 265–319

    Google Scholar 

  • Porpino KDO, Fernicola JC, Bergqvist LP (2009) A new cingulate (Mammalia: Xenarthra), Pachyarmatherium brasiliense sp. nov., from the late Pleistocene of northeastern Brazil. J Vertebr Paleontol 29(3): 881–893

    Article  Google Scholar 

  • Rodriguez-Bualó S, Zurita AE, Góis F, Miño-Boilini AR, Soibelzon E (2014) Pampatheriidae (Xenarthra, Cingulata) from Tarija Valley, Bolivia: a taxonomic update. Riv Ital Paleontol S 120 (2): 253–259

    Google Scholar 

  • Scheyer TM, Sánchez-Villagra MR (2007) Carapace bone histology in the giant pleurodiran turtle Stupendemys geographicus: phylogeny and function. Acta Palaeontol Pol 52(1):137–154

    Google Scholar 

  • Scillato-Yané GJ (1982) Los Dasypodidae (Mammalia, Edentata) del Plioceno y Pleistoceno de Argentina. Doctoral Thesis (unpublished), Facultad de Ciencias Naturales y Museo, UNLP

  • Scillato-Yané GJ, Krmpotic CM, Esteban GI (2010) Las especies del género Chasicotatus Scillato-Yané (Eutatini, Dasypodidae). Rev Mex Cs Geol 27(1): 43–55

    Google Scholar 

  • Soibelzon E, Avilla LS, Castro M (2015) The cingulates (Mammalia: Xenarthra) from the late Quaternary of northern Brazil: fossil records, paleoclimates and displacements in America. Quaternary Internatl 377: 118–125

  • Soibelzon E, León DC (2017) Effects of climatic oscillations on the faunas. The Holocene Thermal Maximum and the displacement of armadillos in Argentina: anatomical features and conservation. J Arch Sci Reports 11: 90–98

    Google Scholar 

  • Soibelzon E, Medina M, Abba AM (2013) Late Holocene armadillos (Mammalia, Dasypodidae) of the sierras of Córdoba, Argentina: Zooarchaeology, diagnostic characters and their paleozoological relevance. Quaternary Internatl 299: 72–79

  • Soibelzon E, Miño-Boilini AR, Zurita AE, Krmpotic CM (2010) Los Xenarthra (Mammalia) del Ensenadense (Pleistoceno Inferior a Medio) de la Región Pampeana (Argentina). Rev Mex Cs Geol 27: 449–469

  • Soibelzon E, Zurita AE, Carlini AA (2006) Glyptodon munizi Ameghino (Mammalia, Cingulata, Glyptodontidae): redescripción y anatomía. Ameghiniana 43: 377–384

    Google Scholar 

  • Vickaryous MK, Hall BK (2006) Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata). J Morphol 267(11):1273–1283

    Article  PubMed  Google Scholar 

  • Vickaryous MK, Sire JY (2009) The integumentary skeleton of tetrapods: origin, evolution, and development. J Anat 214(4):441–464

    Article  PubMed  PubMed Central  Google Scholar 

  • Vizcaíno SF (1994a) Sistemática y anatomía de los Astegotheriini Ameghino, 1906 (nuevo rango) (Xenarthra, Dasypodidae, Dasypodinae). Ameghiniana 31(1): 3–13

    Google Scholar 

  • Vizcaíno SF (1994b) Mecánica masticatoria de Stegotherium tessellatum Ameghino (Mammalia, Xenarthra) del Mioceno de Santa Cruz (Argentina). Algunos aspectos paleoecológicos relacionados. Ameghiniana 31: 283–290

    Google Scholar 

  • Vucetich MG, Verzi DH (1991) Un nuevo Echimydae (Rodentia, Histricognathi) de la Edad Colhuehuapense de Patagonia y consideraciones sobre la sistemática de la familia. Ameghiniana 28(1–2): 67–74

    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, Kalthoff DC, Sander PM (2012) Osteoderm histology of the Pampatheriidae (Cingulata, Xenarthra, Mammalia): implications for systematics, osteoderm growth, and biomechanical adaptation. J Morphol 273(4):388–404

  • Zachos JC, Stott LD, Lohmann KC (1994) Evolution of early Cenozoic marine temperatures. Paleoceanography 9(2): 353–387

    Article  Google Scholar 

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 ma to present. Science 292: 686–693

    Article  CAS  PubMed  Google Scholar 

  • Zurita AE, González Ruiz LR, Gómez-Cruz AJ, Arenas-Mosquera JE (2013) The most complete known Neogene Glyptodontidae (Mammalia, Xenarthra, Cingulata) from northern South America: taxonomic, paleobiogeographic, and phylogenetic implications. J Vertebr Paleontol 33: 696–708

    Article  Google Scholar 

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Acknowledgments

We acknowledge the curators that allowed the study of specimens under their care, Marcelo Reguero (División Paleontología de Vertebrados del Museo de La Plata, UNLP), Sr. Eduardo “Dudu” Ruigómez (Colección de Paleomastozoología del Museo Paleontológico “Edigio Feruglio”). We also thank E. Soibelzon, an anonymous reviewer, John Wible (Editor-in-chief), and Mariela Castro (Guest editor) for providing insightful comments and corrections that improved the manuscript. The digital radiographic images were acquired in YPF-Tecnología (Y-TEC). This work was supported by the Consejo Nacional de Investigaciones Científicas y Técnicas in Argentina (CONICET), Agencia Nacional de Promoción Científica y Tecnológica (BID - PICT 2013-2633, FONCyT-PICTO 105) y Universidad Nacional de La Plata (UNLP N-724).

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Authors and Affiliations

  1. División Paleontología Vertebrados, Museo de La Plata, CONICET, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA, La Plata, Argentina

    M. R. Ciancio, C. M. Krmpotic & A. C. Scarano

  2. Departamento de Ambiente y Turismo, Universidad Nacional de Avellaneda, España 350 Avellaneda, Buenos Aires, Argentina

    A. C. Scarano

  3. Laboratorio de Métodos Analíticos, YPF Tecnología (Y-TEC), Avenida del Petroleo s/n, Berisso, Buenos Aires, Argentina

    M. B. Epele

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  1. M. R. Ciancio
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Ciancio, M.R., Krmpotic, C.M., Scarano, A.C. et al. Internal Morphology of Osteoderms of Extinct Armadillos and Its Relationship with Environmental Conditions. J Mammal Evol 26, 71–83 (2019). https://doi.org/10.1007/s10914-017-9404-y

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