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Anatomical, morphometric and radiographic study of the humerus in lesser anteater (Tamandua mexicana Saussure, 1860): terminological and functional analyses

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Abstract

Tamandua is a neotropical mammal genus that belongs to the superorder Xenarthra. The thoracic limbs of Tamandua have anatomical adaptations that widely differ from other mammals, and there are frequently specimens in wildlife care centers with traumas in their limbs. However, there are few studies describing the radiographic and morphometric anatomy of the humerus in Tamandua, or describing partially the bone reliefs. Thus, the main objective of this study was to describe the characteristics of the humerus of Tamandua mexicana based on gross dissections, radiographies and measurements comparing with other studies in the three Vermilingua genera, and establishing more suitable terminology. Twelve thoracic limbs of six death specimens of Tamandua mexicana were analyzed. The bone reliefs, ligaments, muscles and neurovascular structures related to the humerus were identified, and the suitable terminology to the humerus of Tamandua was established. Morphometric measurements of each bone relief were taken, and the data were statistically analyzed with the Wilcoxon non-parametric test for functional proposes. The humerus of Tamandua has anatomical characteristics mainly to offer greater areas to the muscles that act on the shoulder flexion and hand movements. Even the articular reliefs are lesser than the adjacent non-articular reliefs, the muscles and ligaments are the anatomical structures that give more stabilization to the shoulder and elbow joints. The deltosupracondylar ligament can be partially ossified in older adult specimens, and neurovascular structures pass through the supracondylar foramen. These anatomical characteristics must be accounted for in the radiological diagnosis and surgical approaches.

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References

  • Aguilar RF, Superina M (2015) Xenarthra. In: Miller E, Fowler M (eds) Fowler’s zoo and wild animal medicine, vol 8. Saunders Elsevier, St. Louis, pp 355–369

    Google Scholar 

  • Ankel-Simons F (2007) Primate anatomy: an introduction, 3d edn. Elsevier Academic, Amsterdam

    Google Scholar 

  • Arguedas R, López E, Ovares L (2019) Bone fractures in roadkill Northern Tamandua Tamandua mexicana (Mammalia: Pilosa: Myrmecophagidae) in Costa Rica. J Threat Taxa 11:14802–14807

    Google Scholar 

  • Baljit S (2017) Dyce, Sack, and Wensing’s textbook of veterinary anatomy, 5th edn. Saunders Elsevier, St. Louis

    Google Scholar 

  • Bargo MS, Toledo N, Vizcaíno SF (2012) Paleobiology of the Santacrucia sloths and anteaters (Xenarthra, Pilosa). Early miocene paleobiology in patagonia: high-latitude paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 216–242

    Google Scholar 

  • Brown D (2011) Fruit-eating by an obligate insectivore: palm fruit consumpti in wild northern tamanduas (Tamandua mexicana) in Panamá. Edentata 12:63–66

    Google Scholar 

  • Cotts L, Amaral RV, Laeta M, Cunha-Filho CA, Moratelli R (2019) Pathology in the appendicular bones of southern tamandua, Tamandua tetradactyla (Xenarthra, Pilosa): injuries to the locomotor system and first case report of osteomyelitis in anteaters. BMC Vet Res 15:1–16

    Google Scholar 

  • Cuesta RE, Valencia MJ, Ortega A (2007) Aprovechamiento de los vertebrados terrestres por una comunidad humana en bosque tropicales (Tutunendo, Chocó, Colombia). Rev Inst Univ Tecnol Chocó 26:37–43

    Google Scholar 

  • Duque PJ, Vélez GJ (2014) Descripción anatómica y funcional del húmero del tití gris (Saguinus leucopus). Int J Morphol 32:147–150

    Google Scholar 

  • Evans HE, Lahunta A (2013) Miller’s anatomy of the dog. Saunders Elsevier, St. Louis

    Google Scholar 

  • Federative International Committee on Anatomical Terminologies (1998) Terminologia anatomica: international anatomical terminology. Thieme, New York

    Google Scholar 

  • Fleagle JG, Stern JT, Jungers WL, Susman RL, Vangor AK, Wells JP (1981) Climbing: a biomechanical link with brachiation and with bipedalism. Symp Zool Soc Lond 48:359–375

    Google Scholar 

  • Galton JC (1869) The myology of Cyclothurus didactylus. Ann Mag Nat Hist 4:244–264

    Google Scholar 

  • Garcia CP, Pulido JAR, Soto CMS (2019) Estudio morfofuncional del miembro torácico de Myrmecophaga tridactyla (hormiguero gigante) de la Orinoquia colombiana. Braz J Dev 5:21507–21530

    Google Scholar 

  • Gaudin T, Croft DA (2015) Paleogene xenarthra and the evolution of South American mammals. J Mamm 96:622–634

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Humphry J (1869) The myology of the limbs of the unau, the aï, the twotoed anteater, and the pangolin. J Anat Physiol 3:2–78

    Google Scholar 

  • Ibáñez GP, Galtés I, Jordana X, Fiorin E, Manyosa J, Malgosa A (2013) Entheseal changes and functional implications of the humeral medial epicondyle. Int J Osteoarchaeol 23:211–220

    Google Scholar 

  • International Committee on Veterinary Gross Anatomical Nomenclature (2017) Nomina Anatomica Veterinaria (ed) Committee, Hannover

  • Isler K (2005) 3D-kinematics of vertical climbing in hominoids. Am J Phys Anthropol 126:66–81

    PubMed  Google Scholar 

  • Li H, Jiang LS, Dai LY (2007) Hormones and growth factors in the pathogenesis of spinal ligament ossification. Eur Spine J 16:1075–1084

    PubMed  PubMed Central  Google Scholar 

  • Liebich HG, Maierl J, König HE (2020). In: König HE, Liebich HG (eds) Veterinary anatomy of domestic mammals: text book and colour atlas. Thieme, New York, pp 171–242

    Google Scholar 

  • Lima IG, Biihrer DA, Guimarães GC, Moreira KC, de Britto Rosa MC, Birck AJ, de Oliveira Guimarães CS (2013) Morfologia dos ossos do membro torácico do tamanduá-bandeira. Biotemas 26:141–151

    Google Scholar 

  • Lins FL, Branco É, Giese EG, da Silva LM, de Lima AR (2019) Anátomo-radiografia dos ossos longos do membro torácico do Tamandua tetradactyla. Rev Bras Cienc Vet 26:57–63

    Google Scholar 

  • Lozada-Gallegos AR, Muñoz-García CI, Villanueva-García C, Rocha-Martínez N, Ovando-Fuentes D, Trejo-Salas MB, Rendón-Franco E (2020) Radiographic anatomy of the forelimb in the northern tamandua (Tamandua mexicana). J Zoo Wildl Med 51:265–274

    PubMed  Google Scholar 

  • Macalister A (1875) Report on the anatomy of insectivorous edentates. Trans R Ir Acad 25:491–508

    Google Scholar 

  • Makungu M, Groenewald HB, Du Plessis WM, Barrows M, Koeppel KN (2015) Thoracic limb morphology of the ring-tailed lemur (Lemur catta) evidenced by gross osteology and radiography. Anat Hist Embryol 44:288–298. https://doi.org/10.1111/ahe.12139

    Article  CAS  Google Scholar 

  • McDonald HG, Vizcaíno S, 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 

  • McDowell LJ, Wells D, Hepper PG (2018) Lateralization of spontaneous behaviors in the domestic cat, Felis silvestris. Anim Behav 135:37–43

    Google Scholar 

  • Minto BW, Magalhães TV, Lucena DVF, Soriano IM, Barranco GHF, Dias LGG, Werther K (2021) Humeral fracture repair using a robust fixation in an adult Giant Anteater (Myrmecophaga tridactyla): case report. Arquiv Bras Med Vet Zootec 73:647–652

    Google Scholar 

  • Moraes N, Arteaga M (2015) Genetic diversity in Xenarthra and its relevance to patterns of neotropical biodiversity. J Mamm 96:690–702

    Google Scholar 

  • Moore KL, Persaud T (1998) The developmental human. Clinically oriented embryology, 6th edn. WB Saunders Company, Philadelphia

    Google Scholar 

  • Navarrete D, Ortega J (2011) Tamandua mexicana (Pilosa: Myrmecophagidae). Mamm Species 43:56–63

    Google Scholar 

  • Ortega RJ, Tirira DG, Arteaga M, Miranda F (2014) Tamandua mexicana. The IUCN Red List of Threatened Species 2014: T21349A47442649.

  • Oishi M, Ogihara N, Endo H, Ichihara N, Asari M (2009) Dimensions of forelimb muscles in orangutans and chimpanzees. J Anat 215:373–382

    PubMed  PubMed Central  Google Scholar 

  • Pan J, Xiao W, Zhao Q (2011) Hand preference by black-and-white snub-nosed monkeys (Rhinopithecus bieti) in captivity: influence of tasks and sexes. Laterality 16:656–672

    PubMed  Google Scholar 

  • Pereira KF, de Souza PR, Cardoso JR, Cruz VS, Mendonça AC, Araújo EG (2021) Aspectos da anatomia dos músculos do ombro e braço do Myrmecophaga tridactyla. Arquiv Mudi 25:100–115

    Google Scholar 

  • Polania-Guzmán PV, Vélez-García JF (2019) Gross anatomical adaptations of the craniolateral forearm muscles in Tamandua mexicana (Xenarthra: Myrmecophagidae): development of accessory muscles and rete mirabile for its arterial supply. Heliyon 5:e02179

    PubMed  PubMed Central  Google Scholar 

  • R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rojano C, Padilla H, Almentero E (2013) Percepciones y usos de los Xenarthra e implicaciones para su conservación en Pedraza, Magdalena, Colombia. Edentata 14:58–64

    Google Scholar 

  • Rojano C, Chacón J, Polo A (2016) El oso melero (Tamandua mexicana) en el caribe colombiano: aportes sobre su ecología y amenazas. Edentata 17:17–24

    Google Scholar 

  • Ruiz-García M, Pinilla-Beltrán D, Murillo-García OE, Pinto CM, Brito J, Shostell JM (2021) Comparative mitogenome phylogeography of two anteater genera (Tamandua and Myrmecophaga; Myrmecophagidae, Xenarthra): evidence of discrepant evolutionary traits. Zool Res 42:525–547

    PubMed  PubMed Central  Google Scholar 

  • Sánchez HL, Silva LB, Rafasquino ME, Mateo AG, Zuccolilli GO, Portiansky EL, Alonso CR (2013) Anatomical study of the forearm and hand nerves of the domestic cat (Felis catus), puma (Puma concolor) and jaguar (Panthera onca). Anat Histol Embryol 42:99–104

    PubMed  Google Scholar 

  • Sesoko N, Canevese S, Bortolini Z, Pasini L, Vulcano L, Ozanan F (2015) Skeletal morphology of the forelimb of Myrmecophaga tridactyla. J Zoo Wildl Med 46:713–722

    PubMed  Google Scholar 

  • Sesoko N, Canevese S, Bortolini Z, Bertelis N, Teixeira C (2016) Gross anatomy and surgical approach to the humeral shaft in giant anteater (Myrmecophaga tridactyla). J Zoo Wildl Med 47:790–796

    PubMed  Google Scholar 

  • Silva T, Cuenca S (2012) Anatomia radiográfica de Tamanduá mirim. In: Miranda A (ed) Manutenção de Tamanduás em cativeiro. Editora Cubo, São Carlos, pp 212–239

    Google Scholar 

  • Silva DB, Moreira PC, Cruz VS, Santana EP, Mendonça AC, Cardoso JR (2021) Anatomical aspects of the forearm muscles of Myrmecophaga tridactyla. Acta Vet Bras 15:60–65

    Google Scholar 

  • Spaulding KA, Voges AK (2015) Radiographic anatomy of the appendicular skeleton. In: Thrall DE (ed) Textbook of veterinary diagnostic radiology, 7th edn. Elsevier Science Health Science Division, St. Louis, pp 306–333

    Google Scholar 

  • Superina M, Miranda F, Abba A (2010) The 2010 anteater red list assessment. Edentata 11:96–115

    Google Scholar 

  • Taylor B (1978) The anatomy of the forelimb in the anteater (Tamandua) and its functional implications. J Morphol 157:347–367

    PubMed  Google Scholar 

  • Taylor BK (1985) Functional anatomy of the forelimb in vermilinguas (anteaters). In: Montgomery BB (ed) The evolution and ecology of armadillos sloths, and vermilinguas. Smithsonian Institution, Washington, pp 163–171

    Google Scholar 

  • Thewissen JGM, Badoux DM (1986) The descriptive and functional myology of the fore-limb of the aardvark (Orycteropus afer, Pallas 1766). Anat Anz 162:109–123

    CAS  PubMed  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 Mamm 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 

  • Toledo N, Cassini GH, Vizcaíno SF, Bargo M (2014) Mass estimation Santacrucian sloths from the early Miocene Santa Cruz formation of Patagonia, Argentina. Acta Palaeontol Pol 59:267–281

    Google Scholar 

  • Vélez-García JF, Torres-Suárez SV, Echeverry-Bonilla DF (2020) Anatomical and radiographic study of the scapula in juveniles and adults of Tamandua mexicana (Xenarthra: Myrmecophagidae). Anat Histol Embryol 49:203–215

    PubMed  Google Scholar 

  • Vélez-García JF, Arbeláez-Quiñones AC, Montealegre-Hurtado KD (2021) Evolutionary adaptations in the flexor digitorum profundus muscle in Tamandua mexicana (Xenarthra, Myrmecophagidae). Anat Rec 304:758–770

    Google Scholar 

  • Wislocki GB, Straus WL (1932) On the blood vascular bundles in the limbs of certain edentates and lemurs. Bull Mus Comp Zool 74:1–15

    Google Scholar 

  • Yayama T, Uchida K, Kobayashi S (2007) Thoracic ossification of the human ligamentum flavum: histopathological and immunohistochemical findings around the ossified lesion. J Neurosurg Spine 7:184–193

    PubMed  Google Scholar 

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

    Google Scholar 

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Acknowledgements

We want to thanks to Tolima University for financially supporting this research and special thanks to CORTOLIMA by borrowed the cadavers. We also thank to the Veterinary Hospital of the University of Tolima for facilitating the radiographic studies.

Funding

This research was funded by grants from the Central Research Office of the University of Tolima to Juan Fernando Vélez García (Project No. 390116).

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Authors and Affiliations

  1. Research Group of Medicine and Surgery in Small Animals, Departamento de Sanidad Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad del Tolima, Calle 42 1b-1 Altos de Santa Helena, 730006299, Ibagué, Colombia

    Guerly Johana Heredia-Díaz, Juan Fernando Vélez-García & Diego Fernando Echeverry-Bonilla

  2. Programa de Pós-Graduação em Anatomia dos Animais Domésticos e Silvestres, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, Brazil

    Juan Fernando Vélez-García

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  1. Guerly Johana Heredia-Díaz
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  2. Juan Fernando Vélez-García
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  3. Diego Fernando Echeverry-Bonilla
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis of the humerus were performed by GJHD and JFVG. The radiographic study of the humeri by DFEB and JFVG. The first draft of the manuscript was written by GJHD and all authors commented on posterior versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Juan Fernando Vélez-García.

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Heredia-Díaz, G.J., Vélez-García, J.F. & Echeverry-Bonilla, D.F. Anatomical, morphometric and radiographic study of the humerus in lesser anteater (Tamandua mexicana Saussure, 1860): terminological and functional analyses. Anat Sci Int 97, 170–187 (2022). https://doi.org/10.1007/s12565-021-00639-2

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