Published October 13, 2023 | Version v1

Descriptive study of the intrinsic muscles of the shoulder and brachium in kinkajou (Potos flavus) and an evolutionary analysis within the suborder Caniformia

  • 1. Universidad del Tolima, Ibagué, Colombia|Universidade de São Paulo, São Paulo, Brazil
  • 2. Universidad del Tolima, Ibagué, Colombia
  • 3. King Fahd University of Petroleum and Minerals, Dhahran, Saudi Arabia|University of São Paulo, São Paulo, Brazil

Description

Abstract

The kinkajou (Potos flavus) is a carnivoran of the suborder Caniformia and the family Procyonidae, inhabiting regions throughout Central and South America. Potos flavus has arboreal preferences and exhibits unique anatomical adaptations that facilitate movement within trees. Its pelvic limbs enable hindfoot reversal, while its thoracic limbs possess remarkable prehensile capabilities. Previous anatomical studies in Potos flavus have presented discrepancies in the description of the intrinsic shoulder and brachial muscles. Therefore, this study aims to provide a comprehensive anatomical description of these muscles in five specimens. The findings are compared with descriptions reported for other caniforms. The application of the Density-Based Spatial Clustering of Application with Noise (DBSCAN) algorithm aids in identifying relationships among caniforms based on the presence or absence of specific muscles. Our analysis reveals several key differences, including the presence of a biceps brachii with two capita (longum and breve), two coracobrachiales muscles (longus and brevis), a tensor fasciae antebrachii with two distinct parts (cranialis and caudalis), and an anconeus medialis. The caput breve of the biceps brachii and coracobrachialis longus muscles are absent in some individuals, with prevalence rates of 10% and 20%, respectively. One specimen exhibited an accessory caput laterale of the m. triceps brachii bilaterally. The comparative analysis suggests that the shoulder and brachial muscles of Potos flavus share more similarities with those of Ailurus fulgens and ursids of the genera Ursus and Tremarctos. These findings suggest the retention of muscles that may have been present in the common ancestor of the infraorder Arctoidea.

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References

  • Allen H (1882) The muscles of the limbs of the raccoon (Procyon lotor). Proceedings of the Academy of Natural Sciences Philadelphia 34: 115–144.
  • Annie VR, Jamuna KV, Arun A, Prasad RV, Girish-Kumar V, Shruti O, Chunkkath R, Patil S, Manjunath K, Kumar B (2017) Architecture of shoulder muscles of sloth bear (Melursus ursinus). Indian Journal of Applied Research 7: 295–297.
  • Annie VR, Jamuna KV, Arun AS, Prasad. RV, Girish-Kumar V, Shruti O (2019) Architecture of arm muscles of sloth bear (Melursus ursinus). Journal of Entomology and Zoology Studies 7: 1511–1515.
  • Barone R (2020) Anatomie Comparée des Mammifères domestiques. Tome 2: Arthrologie et Myologie. 4th ed. Association Centrale D'Entraide Vétérinaire, Paris, 1021 pp.
  • Beddard FE (1900) On the anatomy of Bassaricyon alleni. Proceedings of the Zoological Society of London 69: 661–675. https://doi.org/10.1111/j.1096-3642.1890.tb01730.x
  • Beswick-Perrin J (1871) On the myology of the limbs of the kinkajou (Cercoleptes caudivolvulus). Proceedings of Zoological Society of London 1871: 547–559.
  • Böhmer C, Theil J-C, Fabre A-C, Herrel A (2020) Atlas of Terrestrial Mammal Limbs Atlas of Terrestrial Mammal Limbs. CRC Press, Boca Raton, FL. https://doi.org/10.1201/b22115
  • Böhmer C, Fabre AC, Herbin M, Peigné S, Herrel A (2018) Anatomical basis of differences in locomotor behavior in martens: A comparison of the forelimb musculature between two sympatric species of Martes. Anatomical Record 301: 449–472. https://doi.org/10.1002/ar.23742
  • Böhmer C, Fabre AC, Taverne M, Herbin M, Peigné S, Herrel A (2019) Functional relationship between myology and ecology in carnivores: Do forelimb muscles reflect adaptations to prehension? Biological Journal of the Linnean Society 127: 661–680. https://doi.org/10.1093/biolinnean/blz036
  • Carlsson A (1925) Über Ailurus fulgens. Acta Zoologica 6: 269–305. https://doi.org/10.1111/j.1463-6395.1925.tb00268.x
  • Davis DD (1949) The shoulder architecture of bears and other carnivores. Chicago Natural History Museum 31: 285–305. https://doi.org/10.5962/bhl.title.1291
  • Davis DD (1964) The giant panda: A morphological study of evolutionary mechanisms. Fieldiana 3: 1–339. Available from: http://marefateadyan.nashriyat.ir/node/150.
  • Diogo R, Abdala V (2010) Muscles of Vertebrates: Comparative Anatomy, Evolution, Homologies and Development. CRC Press, Enfield, 470 pp.
  • Diogo R, Wood B (2012) Comparative Anatomy and Phylogeny of Primate Muscles and Human Evolution. CRC Press, Enfield, 1020 pp.
  • Diogo R, Bello-Hellegouarch G, Kohlsdorf T, Esteve-Altava B, Molnar JL (2016) Comparative Myology and evolution of marsupials and other vertebrates, with notes on complexity, bauplan, and "scala naturae". Anatomical Record 299: 1224–1255. https://doi.org/10.1002/ar.23390
  • Enciso-García LM, Vélez-García JF (2022) Origin and distribution of the brachial plexus in kinkajou (Potos flavus – Schreber, 1774). Anatomia, Histologia, Embryologia 51: 221–235. https://doi.org/10.1111/ahe.12781
  • Ercoli MD, Álvarez A, Stefanini MI, Busker F, Morales MM (2015) Muscular anatomy of the forelimbs of the lesser grison (Galictis cuja), and a functional and phylogenetic overview of Mustelidae and other Caniformia. Journal of Mammalian Evolution 22: 57–91. https://doi.org/10.1007/s10914-014-9257-6
  • Ester M, Kriegel HP, Sander J, Xu X (1996) A density-based algorithm for discovering clusters in large spatial databases with noise. In: Simoudis E, Han J, Fayyad U (Eds) Proceedings of the Second International Conference on Knowledge Discovery and Data Mining. Association for the Advancement of Artificial Intelligence, Portland, OR, 226–231.
  • Feeney S (1999) Comparative osteology, myology, and locomotor specializations of the fore and hind limbs of the North American foxes Vulpes vulpes and Urocyon cinereoargenteus. Doctoral Dissertation, University of Massachussets, Amherst, MA.
  • Fisher RE, Adrian B, Barton M, Holmgren J, Tang SY (2009) The phylogeny of the red panda (Ailurus fulgens): Evidence from the forelimb. Journal of Anatomy 215: 611–635. https://doi.org/10.1111/j.1469-7580.2009.01156.x
  • Gambaryan PP, Kuznetsov AN, Gerasimov S V., Panyutina AA (2015) Shoulder girdle and forelimb myology of extant Monotremata. Russian Journal of Theriology/Русский териологический журнал 14: 1–56.
  • Hall ER (1926) The muscular anatomy of three mustelid mammals, Mephilis, Spilogale, and Martes. University of California Publications in Zoology 30: 7–38.
  • Hassanin A, Veron G, Ropiquet A, Jansen van Vuuren B, Lécu A, Goodman SM, Haider J, Nguyen TT (2021) Evolutionary history of Carnivora (Mammalia, Laurasiatheria) inferred from mitochondrial genomes. PLoS ONE 16: e0240770. https://doi.org/10.1371/journal.pone.0240770
  • Haughton S (1864) On the muscular anatomy of the otter (Lutra vulgaris). Proceedings of the Royal Irish Academy 9: 511–515.
  • Helgen K, Kays R, Schipper J (2016) Potos flavus. The IUCN Red List of Threatened Species 2016: e.T41679A45215631. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T41679A45215631.en
  • Hermanson JW (2020) The muscular system. In: Hermanson JW, Evans H, De Lahunta A (Eds) Miller's Anatomy of the Dog. Elsevier, St. Louis, MO, 444–658.
  • Hermanson JW, Evans H, De Lahunta A (2020) Miller and Evan's Anatomy of the Dog. 5th ed. Elsevier, St. Louis, MO, 2119 pp.
  • Howard LD (1973) Muscular anatomy of the fore-limb of the sea otter (Enhydra lutris). Proceedings of the California Academy of Sciences 39: 411–500.
  • International Committee on Veterinary Gross Anatomical Nomenclature (2017) Nomina Anatómica Veterinaria. 6th ed. World Association of Veterinary Anatomists, Hannover, 160 pp.
  • Jiangzuo Q, Flynn JJ (2020) The earliest ursine bear demonstrates the origin of plant-dominated omnivory in Carnivora. iScience 23: 101235. https://doi.org/10.1016/j.isci.2020.101235
  • Julitz C (1909) Osteologie und Myologie der Extremitäten und des Wickelschwanzes vom Wickelbären, Cercoleptes caudivolvulus, mit besonderer Berücksichtigung der Anpassungserscheinungen an das Baumleben. Archiv für Naturgeschichte 75: 143–188.
  • Kardong KV (2012) Vertebrates: Comparative Anatomy, Function, Evolution. 6th ed. McGraw Hill, New York, NY, 794 pp.
  • Kelley E (1888) Notes on the myology of Ursus maritimus. Proceedings of the Academy of Natural Sciences Philadelphia 40: 141–154.
  • Kluyver T, Ragan-Kelley B, Pérez F, Granger BE, Bussonnier M, Frederic J, Kelley K, Hamrick J, Grout J, Corlay S, Ivanov P, Avila D, Abdalla S, Willing C (2016) Jupyter Notebooks – a publishing format for reproducible computational workflows. In: Loizides F, Schmidt B (Eds) Positioning and Power in Academic Publishing: Players, Agents and Agendas. IOS Press, Amsterdam, 87–90. https://doi.org/10.3233/978-1-61499-649-1-87
  • Kotu V, Deshpande B (2019) Data Science: Concepts and Practice. 2nd ed. Morgan Kauffman Publishers, Cambridge, 548 pp.
  • Lambert JE, Fellner V, McKenney E, Hartstone-Rose A (2014) Binturong (Arctictis binturong) and kinkajou (Potos flavus) digestive strategy: Implications for Interpreting frugivory in carnivora and primates. PLoS ONE 9: e105415. https://doi.org/10.1371/journal.pone.0105415
  • Leach D (1977) The forelimb musculature of marten (Martes americana Turton) and fishes (Martes pennanti Erxleben). Canadian Journal of Zoology 55: 31–41. https://doi.org/10.1139/z77-003
  • Liebich HG, Maierl J, König HE (2020) Forelimbs or thoracic limbs (membra thoracica). In: König HE, Liebich HG (Eds) Veterinary Anatomy of Domestic Animals. Textbook and Colour Atlas. Georg Thieme Verlag, Stuttgart, 171–242.
  • Macalister A (1873a) On the anatomy of Aonyx. Proceedings of the Royal Irish Academy (Science) 1: 539–547.
  • Macalister A (1873b) The muscular anatomy of the civet and tayra. Proceedings of the Royal Irish Academy (Science) 1: 506–513.
  • Mackintosh HW (1875) Notes on the myology of the Coati-Mondi (Nasua narica and N. fusca) and common martin (Martes foina). Proceedings of the Royal Irish Academy (Science) 2: 48–55.
  • Marsh SF, Manfredi K, Smith HF (2021) Myological and osteological correlates of hindfoot reversal in the kinkajou (Potos flavus). Journal of Mammalian Evolution 28: 813–830. https://doi.org/10.1007/s10914-020-09533-6
  • McClearn D (1992) Locomotion, posture, and feeding behavior of kinkajous, coatis, and raccoons. Journal of Mammalogy 73: 245–261.
  • Meloro C, de Oliveira AM (2019) Elbow Joint geometry in bears (Ursidae, Carnivora): A tool to infer paleobiology and functional adaptations of quaternary fossils. Journal of Mammalian Evolution 26: 133–146. https://doi.org/10.1007/s10914-017-9413-x
  • Monroy-Cendales MJ, Vélez-García JF, Castañeda-Herrera FE (2020) Gross anatomy of the shoulder and arm intrinsic muscles in the white-footed tamarin (Saguinus leucopus – Günther, 1876): Inter- and intraspecific anatomical variations. Journal of Medical Primatology 49: 123–135. https://doi.org/10.1111/jmp.12465
  • Monroy-Cendales MJ, Vélez-García JF, Castañeda-Serrano RD, Miglino MA (2023) Gross anatomical description of the extrinsic and intrinsic scapular and brachial muscles of Sapajus apella (Linnaeus, 1758). Journal of Medical Primatology 52: 3–16. https://doi.org/10.1111/jmp.12619
  • Monterrubio-Rico TC, Charre-Medellín JF, Villanueva-Hernández AI, León-Paniagua L (2013) Nuevos registros de la martucha (Potos flavus) para Michoacán, México, que establecen su límite de distribución al norte por el Pacífico. Revista Mexicana de Biodiversidad 84: 1002–1006. https://doi.org/10.7550/rmb.34419
  • Moore AL, Budny JE, Russell AP, Butcher MT (2013) Architectural specialization of the intrinsic thoracic limb musculature of the American badger (Taxidea taxus). Journal of Morphology 274: 35–48. https://doi.org/10.1002/jmor.20074
  • Müller AC, Guido S (2017) Introduction to Machine Learning with Python: A Guide for Data Scientists. 2nd ed. O'Reilly Media, Beijing, 384 pp.
  • Nascimento FF, Oliveira-Silva M, Veron G, Salazar-Bravo J, Gonçalves PR, Langguth A, Silva CR, Bonvicino CR (2017) The evolutionary history and genetic diversity of kinkajous, Potos flavus (Carnivora, Procyonidae). Journal of Mammalian Evolution 24: 439–451. https://doi.org/10.1007/s10914-016-9354-9
  • Nyakatura K, Bininda-Emonds OR (2012) Updating the evolutionary history of Carnivora (Mammalia): A new species-level supertree complete with divergence time estimates. BMC Biology 10: 12. https://doi.org/10.1186/1741-7007-10-12
  • Perdomo-Cárdenas V, Patiño-Holguín C, Vélez-García JF (2021) Evolutionary and terminological analysis of the flexor digitorum superficialis, interflexorii and palmaris longus muscles in kinkajou (Potos flavus) and crab-eating racoon (Procyon cancrivorus). Anatomia Histologia Embryologia 50: 520–533. https://doi.org/10.1111/ahe.12656
  • Pereira KF, Pereira F, Lima V (2010) Estudo morfológico dos músculos do braço de mão pelada (Procyon cancrivorus Cuvier 1798). Veterinary Notes 16: 23–28.
  • Richards HL, Adams JW, Evans AR (2023) Hanging on and digging deep: Comparative forelimb myology of the koala (Phascolarctos cinereus) and common wombat (Vombatus ursinus). Zoological Journal of the Linnean Society 199: 60–92. https://doi.org/10.1093/zoolinnean/zlad018
  • Rousseeuw PJ (1987) Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. Journal of Computational and Applied Mathematics 20: 53–65. https://doi.org/10.1016/0377-0427(87)90125-7
  • Santos AC, Bertassoli B, Oliveira VC, Carvalho AF, Rosa RA, Mançanares CA (2010a) Morfologia dos músculos do ombro, braço e antebraço do quati (Nasua nasua Linnaeus, 1758). Biotemas 23: 167–173.
  • Santos AC, Bertassoli B, Rosa RA, Cravalho AF, Mançanares CA (2010b) Miologia comparada do membro torácico do mão-pelada (Procyon cancrivorus, Cuvier, 1798). Revista de FZVA 17: 262–275.
  • Shepherd F (1883) Short notes on the myology of the american black bear (Ursus americanus). Journal of Anatomy and Physiology 18: 103–117. https://doi.org/10.1007/bf00203353
  • Smith HF, Adrian B, Koshy R, Alwiel R, Grossman A (2020) Adaptations to cursoriality and digit reduction in the forelimb of the African wild dog (Lycaon pictus). PeerJ 8: 1–34. https://doi.org/10.7717/peerj.9866
  • Souza-Junior P, Santos LMRP dos, Viotto-Souza W, de Carvalho N da C, Souza EC, Kasper CB, Abidu-Figueiredo M, Santos ALQ (2018) Functional myology of the thoracic limb in Pampas fox (Lycalopex gymnocercus): A descriptive and comparative analysis. Journal of Anatomy 233: 783–806. https://doi.org/10.1111/joa.12892
  • Souza Junior P, Viotto-Souza W, Mendes VP, Bernardes FCS, Anjos BL, Abidu-Figueiredo M, Santos ALQ (2020) Clavicle in carnivorans: A forgotten bone. Anatomical Record 303: 1831–1841. https://doi.org/10.1002/ar.24294
  • Standring S (2020) Gray's Anatomy. The Anatomical Basis of Clinical Practice. 42nd ed. Elsevier, Philadelphia, PA, 1606 pp.
  • Tarquini J, Mosto MC, Ercoli MD (2023) Functional and phylogenetic interpretation of the forelimb myology of two South American carnivorans, the ring-tailed coati (Nasua nasua) and crab-eating raccoon (Procyon cancrivorus). Journal of Morphology 284: e21587. https://doi.org/10.1002/jmor.21587
  • Tarquini J, Morgan CC, Toledo N, Soibelzon LH (2019) Comparative osteology and functional morphology of the forelimb of Cyonasua (Mammalia, Procyonidae), the first South American carnivoran. Journal of Morphology 280: 446–470. https://doi.org/10.1002/jmor.20956
  • Taverne M, Fabre A-C, Herbin M, Herrel A, Peigné S, Lacroux C, Lowie A, Pagès F, Theil J-C, Böhmer C (2018) Convergence in the functional properties of forelimb muscles in carnivorans: Adaptations to an arboreal lifestyle? Biological Journal of the Linnean Society 125: 250–263. https://doi.org/10.1093/biolinnean/bly123
  • Taylor BK (1978) The anatomy of the forelimb in the anteater (Tamandua) and its functional implications. Journal of Morphology 157: 347–367. https://doi.org/10.1002/jmor.1051570307
  • Taylor ME (1982) The functional anatomy of the forelimb of Some African Viverridae (Carnivora). Journal of Morphology 143: 307–336.
  • Vélez-García JF, Miglino MA (2023) Evolutionary comparative analysis of the extrinsic thoracic limb muscles in three procyonids (Procyon cancrivorus Cuvier, 1798, Nasua nasua Linnaeus, 1766, and Potos flavus Schreber, 1774) based on their attachments and innervation. Anatomical Science International 98: 273–292. https://doi.org/10.1007/s12565-022-00696-1
  • Vélez-García JF, Patiño-Holguín C, Duque-Parra JE (2018a) Anatomical variations of the caudomedial antebrachial muscles in the crab-eating fox (Cerdocyon thous). International Journal of Morphology 36: 1193–1196. https://doi.org/10.4067/S0717-95022018000401193
  • Vélez-García JF, Ramírez-Arias JC, Duque-Parra JE (2018b) Gross anatomy of the intrinsic muscles of the scapular and humeral joint regions in crab-eating fox (Cerdocyon thous, Linnaeus 1776). Acta Scientiarum (Biological Sciences) 40: 37861. https://doi.org/10.4025/actascibiolsci.v40i1.37861
  • 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). Anatomia Histologia Embryologia 49: 203–215. https://doi.org/10.1111/ahe.12514
  • Vélez-García JF, Marín-González L, Monroy-Cendales MJ, Miglino MA (2022) Craniolateral forearm muscles of the crab-eating raccoon (Procyon cancrivorus) and a comparative review with other carnivorans. Iheringia (Série Zoologia) 112: e2022012. https://doi.org/10.1590/1678-4766e2022012
  • Vélez-García JF, Arbeláez-Quiñones AC, Montealegre-Hurtado KD (2021) Evolutionary adaptations in the flexor digitorum profundus muscle in Tamandua mexicana (Xenarthra, Myrmecophagidae). Anatomical Record 304: 758–770. https://doi.org/10.1002/ar.24502
  • Vélez-García JF, Chunganá-Caicedo D, Saavedra-Montealegre S (2022) Gross anatomy of the craniolateral antebrachial muscles in kinkajou (Potos flavus, Carnivora): Intra- and interspecific variants within the family Procyonidae. Anatomia, Histologia, Embryologia 51: 308–313. https://doi.org/10.1111/ahe.12772
  • Vélez García JF, de Carvalho Barros RA, Miglino MA (2023) Origin and distribution of the brachial plexus in two procyonids (Procyon cancrivorus and Nasua nasua, Carnivora). Animals 13: 210. https://doi.org/10.3390/ani13020210
  • Vélez J, Ramírez J, Aristizábal O (2018) An anatomic description of intrinsic brachial muscles in the crab-eating fox (Cerdocyon thous, Linnaeus 1776) and report of a variant arterial distribution. Anatomia, Histologia, Embryologia 47: 180–183. https://doi.org/10.1111/ahe.12330
  • Williams SM (2016) Observations on the mating behavior of the eastern lowland olingo Bassaricyon alleni (Carnivora: Procyonidae) in the Peruvian Amazon. Zoologia (Curitiba) 33. https://doi.org/10.1590/S1984-4689zool-20160027
  • Windle B (1888) Notes on the limb myology of Procyon cancrivorus and of the Ursidae. Journal of Anatomy and Physiology 23: 81–89.
  • Windle B, Parsons F (1897) Myology of the terrestrial carnivora. Part I. Muscles of the head, neck, and fore-limb. Proceedings of the Zoological Society of London 65: 370–409.
  • Yousefi MH, Rasouli B, Ghodrati S, Adibi MA, Taherdoost M, Omidbakhsh S, Behnam G (2018) Anatomical study of extrinsic and some intrinsic muscles of the thoracic limb in Iranian pine marten (Martes martes): A case report. Iranian Journal of Veterinary Medicine 12: 273–282. https://doi.org/10.22059/ijvm.2018.252150.1004876