[en] The musculoskeletal anatomy of the shoulder of many ungulates has been inferred from veterinary model taxa, with uniformity in muscle arrangements and attachment sites often assumed. In this study, I investigated the muscular and osteological anatomy of tapirs and their relatives (Perissodactyla: Tapiroidea), using a combination of gross dissection and digital imaging (photography and laser surface scanning). Dissections of three modern tapir species revealed that the m. infraspinatus originates from both supraspinous and infraspinous fossae for all species, lying on both sides of the distal scapular spine. The epimysial border between the m. supraspinatus and m. infraspinatus origin sites are marked in all species by an ossified ridge, sometimes extending the length of the scapular spine. This "supraspinous ridge" is clearly visible on the scapular surface of both modern and extinct Tapirus scapulae; however, the ridge does not appear present in any non-Tapirus tapiroids examined (e.g., Helaletes, Nexuotapirus), nor in other perissodactyls or artiodactyls. Moreover, the ridge exhibits a clearly distinct morphology in Tapirus indicus compared to all other Tapirus species examined. Combined, these findings indicate that the presence and position of the "supraspinous ridge" may represent a robust phylogenetic character for reconstructing relationships within tapiroids. Unfortunately, any functional locomotor outcomes or benefits of the m. infraspinatus straddling the scapular spine remains elusive. This study represents a firm reminder for anatomists, veterinarians, and paleontologists to (where possible) look beyond veterinary model systems when inferring musculoskeletal form or function in non-model organisms.
Disciplines :
Zoology
Author, co-author :
Maclaren, James ; Université de Liège - ULiège > Département de géologie > Evolution and diversity dynamics lab ; Department of Biology, Universiteit Antwerpen, Wilrijk, Antwerp, Belgium
Language :
English
Title :
Looking back over the shoulder: New insights on the unique scapular anatomy of the tapir (Perissodactyla: Tapiridae).
Publication date :
15 November 2023
Journal title :
Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology
ISSN :
1932-8486
eISSN :
1932-8494
Publisher :
John Wiley and Sons Inc, United States
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
COB - Company of Biologists FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen
Funding text :
I would like to thank the following for their provision of specimens and workspace for this study: Sandra Nauwelaerts, Ellen Goosenaerts, Denise Vogel, Chris Van Ginneken (UAntwerpen); Chris Conroy (MVZ); Christiane Funk (ZMB); Eleanor Hoeger (AMNH); Pepijn Kamminga (RMNH); Josephine Lesur (MNHN); Luc Tyteca (MEO); Frank Zachos (NHMW); Richard Hulbert, Jeanette Pirlo, Rachel Narducci (FLMNH); Chris Widga, Steve Wallace (ETMNH); John Demboski, Andie Carrillo, Kristen MacKenzie, Garth Spellman (DMNS); Mason Kirkland (LSU); Liza Dadone and the staff of Cheyenne Mountain Zoo; Francis Vercammen and the staff of Antwerp Zoo (KMDA); Alex Larsson, Bim Boijsen, Linda Berggren and the staff of Kolmården Wildlife Park. I would also like to specifically thank Martha MacMillan, Eleesha Annear, and Brianna McHorse for their hands‐on assistance during dissections, and both Peter Aerts and Federico Banfi for their assistance in translating foreign texts. Extended thanks to Christine Böhmer (Editor) and both Eloy Gálvez‐López and Cyril Etienne (reviewers) for their constructive comments during review. This study was financially supported by doctoral (11Y7615N) and post‐doctoral (12V8422N) fellowships from the FWO (Fonds Wetenschappelijk Onderzoek), an FWO Short‐Stay Travel Grant (Denver, 2022; K207322N), and a Company of Biologists Travel Grant (Kolmården, 2023).
Bai, B., Meng, J., Mao, F. Y., Zhang, Z. Q., & Wang, Y. Q. (2019). A new early Eocene deperetellid tapiroid illuminates the origin of Deperetellidae and the pattern of premolar molarization in Perissodactyla. PLoS One, 14(11), 1–26. https://doi.org/10.1371/journal.pone.0225045
Bai, B., Wang, Y.-Q., Mao, F. Y., & Meng, J. (2017). New material of Eocene Helaletidae (Perissodactyla, Tapiroidea) from the Irdin Manha formation of the Erlian Basin, Inner Mongolia, China and comments on related localities of the Huheboerhe area. American Museum Novitates, 3878, 1–44. https://doi.org/10.1206/3878.1
Bapst, D. W. (2012). Paleotree: An R package for paleontological and phylogenetic analyses of evolution. Methods in Ecology and Evolution, 3(5), 803–807. https://doi.org/10.1111/j.2041-210X.2012.00223.x
Berta, A., Sumich, J. L., Kovacs, K. M., Folkens, P. A., & Adam, P. J. (2015). Pinniped evolution and systematics. In A. Berta, J. L. Sumich, K. M. Kovacs, P. A. Folkens, & P. J. Adam (Eds.), Marine mammals: Evolutionary biology (3rd ed., pp. 35–61). Academic Press. https://doi.org/10.1016/b978-0-12-397002-2.00003-x
Berta, A., & Wyss, A. R. (1994). Pinniped phylogeny. Proceedings of the San Diego Society of Natural History, 29, 33–56.
Böhmer, C., Theil, J.-C., Fabre, A.-C., & Herrel, A. (2020). In C. Böhmer, J.-C. Theil, A.-C. Fabre, & A. Herrel (Eds.), Atlas of terrestrial mammal limbs (1st ed.). CRC Press. https://doi.org/10.1201/b22115
Bressou, C. (1961). La myologie du tapir (Tapirus indicus L.). Mammalia, 25(3), 358–400. https://doi.org/10.1515/mamm.1961.25.3.358
Budras, K.-D., Sack, W. O., & Rock, S. (2012). Thoracic limb. In K.-D. Budras, W. O. Sack, & S. Rock (Eds.), Anatomy of the horse (6th ed., pp. 4–14). Schlutersche.
Campbell, B. (1936). The comparative myology of the forelimb of the hippopotamus, pig and tapir. American Journal of Anatomy, 59(2), 201–247.
Constantinescu, G. M., Habel, R. E., Hillebrand, A., Sack, W. O., Schaller, O., Simoens, P., & de Vos, N. R. (2012). Osteologia. In G. M. Constantinescu & O. Schaller (Eds.), Illustrated veterinary anatomical nomenclature (3rd ed., pp. 10–62). Enke.
Cozzuol, M. A., Clozato, C. L., Holanda, E. C., Rodrigues, F. H. G., Nienow, S., de Thoisy, B., Redondo, R. A. F., & Santos, F. R. (2013). A new species of tapir from the Amazon. Journal of Mammalogy, 94(6), 1331–1345. https://doi.org/10.1644/12-MAMM-A-169.1
Cuff, A. R., Sparkes, E. L., Randau, M., Pierce, S. E., Kitchener, A. C., Goswami, A., & Hutchinson, J. R. (2016). The scaling of postcranial muscles in cats (Felidae) I: Forelimb, cervical, and thoracic muscles. Journal of Anatomy, 229(1), 128–141. https://doi.org/10.1111/joa.12477
Deutsch, A. R., Dickinson, E., Leonard, K. C., Pastor, F., Muchlinski, M. N., & Hartstone-Rose, A. (2020). Scaling of anatomically derived maximal bite force in primates. Anatomical Record, 303(7), 2026–2035. https://doi.org/10.1002/ar.24284
Diedrich, C. G. (2012). Late Pleistocene Crocuta crocuta spelaea (Goldfuss 1823) populations from the Emscher River terrace open air hyena den near Bottrop and other sites in NW Germany: Their bone accumulations along rivers in lowland mammoth steppe environments and scavenging activities on woolly rhinoceros. Quaternary International, 276–277, 93–119. https://doi.org/10.1016/j.quaint.2011.07.046
Diniz, J. A. R. A., Falcão, B. M. R., Rocha, E. F., de Souza, J. G., da Nobrega Carreiro, A., Medeiros, G. X., & de Menezes, D. J. A. (2018). Anatomical description of the forelimb muscles of the brown-throated sloth (Bradypus variegatus). Acta Scientiae Veterinariae, 46(1601), 1-10. https://doi.org/10.22456/1679-9216.85986
English, A. W. M. (1976). Functional anatomy of the hands of fur seals and sea lions. American Journal of Anatomy, 147(1), 1–17. https://doi.org/10.1002/aja.1001470102
English, A. W. M. (1977). Structural correlates of forelimb function in fur seals and sea lions. Journal of Morphology, 151(3), 325–352. https://doi.org/10.1002/jmor.1051510303
Etienne, C., Houssaye, A., & Hutchinson, J. R. (2021). Limb myology and muscle architecture of the Indian rhinoceros Rhinoceros unicornis and the white rhinoceros Ceratotherium simum (Mammalia: Rhinocerotidae). PeerJ, 9, e11314. https://doi.org/10.7717/peerj.11314
Fabre, A. C., Perry, J. M. G., Hartstone-Rose, A., Lowie, A., Boens, A., & Dumont, M. (2018). Do muscles constrain skull shape evolution in Strepsirrhines? Anatomical Record, 301(2), 291–310. https://doi.org/10.1002/ar.23712
Falconi-Briones, F. A., Naranjo, E. J., Reyna-Hurtado, R., Spínola, M., Enríquez-Rocha, P., & Medellín, R. A. (2022). Habitat use and activity patterns of ungulates in a tropical rainforest of southern México. Therya, 13(2), 171–182. https://doi.org/10.12933/therya-22-1167
Flinn, E. B., Strickland, B. K., Demarais, S., & Christiansen, D. (2013). Age and gender affect epiphyseal closure in white-tailed deer. Southeastern Naturalist, 12(2), 297–306. https://doi.org/10.1656/058.012.0205
Franzen, J. L. (2010). Pseudo horses and relatives of horses. In The rise of horses: 55 million years of evolution (pp. 145–164). Johns Hopkins University Press.
Gardiner, J. D., Behnsen, J., & Brassey, C. A. (2018). Alpha shapes: Determining 3D shape complexity across morphologically diverse structures. BMC Evolutionary Biology, 18(1), 184. https://doi.org/10.1186/s12862-018-1305-z
Grandi, F., del Valle, H., Cáceres, I., Rodríguez-Salgado, P., Oms, O., Fernández-Jalvo, Y., García, F., Campeny, G., & Gómez de Soler, B. (2023). Exceptional preservation of large fossil vertebrates in a volcanic setting (camp dels Ninots, Spain). Historical Biology, 35(7), 1234–1249. https://doi.org/10.1080/08912963.2022.2085570
Graziotti, G. H., Chamizo, V. E., Ríos, C., Acevedo, L. M., Rodríguez-Menéndez, J. M., Victorica, C., & Rivero, J. L. L. (2012). Adaptive functional specialisation of architectural design and fibre type characteristics in agonist shoulder flexor muscles of the llama, Lama glama. Journal of Anatomy, 221(2), 151–163. https://doi.org/10.1111/j.1469-7580.2012.01520.x
Großmann, M., Sánchez-Villagra, M. R., & Maier, W. (2002). On the development of the shoulder girdle in Crocidura russula (Soricidae) and other placental mammals: Evolutionary and functional aspects. Journal of Anatomy, 201(5), 371–381. https://doi.org/10.1046/j.0021-8782.2002.00105.x
Groves, C., & Grubb, P. (2011). Tapiridae. In C. Groves & P. Grubb (Eds.), Ungulate taxonomy (1st ed., Issue 9, pp. 18–20). Johns Hopkins University Press. https://doi.org/10.5860/choice.49-5062
Handa, N., Izuho, M., Takahashi, K., Iizuka, F., Tsogtbaatar, B., Gunchinsuren, B., Odosuren, D., & Ishitseren, L. (2022). The woolly rhinoceros (Coelodonta antiquitatis) from Ondorkhaan, eastern Mongolia. Boreas, 51(3), 584–605. https://doi.org/10.1111/bor.12582
Hartstone-Rose, A., Dickinson, E., Deutsch, A. R., Worden, N., & Hirschkorn, G. A. (2022). Masticatory muscle architectural correlates of dietary diversity in Canidae, Ursidae, and across the order Carnivora. Anatomical Record, 305(2), 477–497. https://doi.org/10.1002/ar.24748
Hartstone-Rose, A., Perry, J. M. G., & Morrow, C. J. (2012). Bite force estimation and the fiber architecture of felid masticatory muscles. Anatomical Record, 295(8), 1336–1351. https://doi.org/10.1002/ar.22518
Holanda, E. C., Ferigolo, J., & Ribeiro, A. M. (2011). New Tapirus species (Mammalia: Perissodactyla: Tapiridae) from the upper Pleistocene of Amazonia, Brazil. Journal of Mammalogy, 92(1), 111–120. https://doi.org/10.1644/10-MAMM-A-144.1
Holanda, E. C., & Ferrero, B. S. (2013). Reappraisal of the genus Tapirus (Perissodactyla, Tapiridae): Systematics and phylogenetic affinities of the south American tapirs. Journal of Mammalian Evolution, 20(1), 33–44. https://doi.org/10.1007/s10914-012-9196-z
Holanda, E. C., Ribeiro, A. M., & Ferigolo, J. (2012). New material of Tapirus (Perissodactyla: Tapiridae) from the Pleistocene of southern Brazil. Revista Mexicana de Ciencias Geologicas, 29(2), 308–318.
Hulbert, R. C. (2005). Late Miocene Tapirus (Mammalia, Perissodactyla) from Florida, with description of a new species, Tapirus webbi. Bulletin of the Florida Museum of Natural History, 45(4), 465–494.
Hulbert, R. C. (2010). A new early Pleistocene tapir (Mammalia: Perissodactyla) from Florida, with a review of Blancan tapirs from the state. Bulletin of the Florida Museum of Natural History, 49(3), 67–126.
Kavanagh, K. D., Bailey, C. S., & Sears, K. E. (2020). Evidence of five digits in embryonic horses and developmental stabilization of tetrapod digit number. Proceedings of the Royal Society B: Biological Sciences, 287(1920), 20192756. https://doi.org/10.1098/rspb.2019.2756
King, J. E. (1983). Seals of the world (2nd ed.). British Museum of Natural History.
Law, C. J., Blackwell, E. A., Curtis, A. A., Dickinson, E., Hartstone-Rose, A., & Santana, S. E. (2022). Decoupled evolution of the cranium and mandible in carnivoran mammals. Evolution, 76(12), 2959–2974. https://doi.org/10.1111/evo.14578
Liebich, H.-G., & König, H. E. (2020). Veterinary anatomy of domestic animals. In H.-G. Liebich & H. E. König (Eds.), Veterinary anatomy of domestic animals (7th ed.). Elsevier. https://doi.org/10.1055/b-007-167437
Liebich, H.-G., Konig, H. E., & Maierl, J. (2007). Forelimb or thoracic limb (membra thoracica). In H. E. Konig & H.-G. Liebich (Eds.), Veterinary anatomy of domestic animals: Textbook and colour atlas (3rd ed., pp. 145–214). Schlutersche.
MacLaren, J. A., Hulbert, R. C., Wallace, S. C., & Nauwelaerts, S. (2018). A morphometric analysis of the forelimb in the genus Tapirus (Perissodactyla: Tapiridae) reveals influences of habitat, phylogeny and size through time and across geographical space. Zoological Journal of the Linnean Society, 184(2), 499–515.
MacLaren, J. A., & McHorse, B. K. (2020). Comparative forelimb myology and muscular architecture of a juvenile Malayan tapir (Tapirus indicus). Journal of Anatomy, 236(1), 85–97. https://doi.org/10.1111/joa.13087
MacLaren, J. A., & Nauwelaerts, S. (2016). A three-dimensional morphometric analysis of upper forelimb morphology in the enigmatic tapir (Perissodactyla: Tapirus) hints at subtle variations in locomotor ecology. Journal of Morphology, 277(11), 1469–1485.
MacLaren, J. A., & Nauwelaerts, S. (2020). Modern tapirs as Morphofunctional analogues for locomotion in endemic Eocene European Perissodactyls. Journal of Mammalian Evolution, 27(2), 245–263. https://doi.org/10.1007/s10914-019-09460-1
Marchi, D., Leischner, C. L., Pastor, F., & Hartstone-Rose, A. (2018). Leg muscle architecture in primates and its correlation with locomotion patterns. Anatomical Record, 301(3), 515–527. https://doi.org/10.1002/ar.23745
Martini, P., Schmid, P., & Costeur, L. (2018). Comparative morphometry of Bactrian camel and dromedary. Journal of Mammalian Evolution, 25(2), 407–425. https://doi.org/10.1007/S10914-017-9386-9
Maynard Smith, J., & Savage, R. J. G. (1956). Some locomotory adaptations in mammals. Journal of the Linnean Society of London, Zoology, 42(288), 603–622. https://doi.org/10.1111/j.1096-3642.1956.tb02220.x
Murie, J. (1872). On the Malayan tapir, Rhinochoerus sumatranus (gray). Journal of Anatomy and Physiology, 6, 131–169.
Nyakatura, J. A., & Fischer, M. S. (2011). Functional morphology of the muscular sling at the pectoral girdle in tree sloths: Convergent morphological solutions to new functional demands? Journal of Anatomy, 219(3), 360–374. https://doi.org/10.1111/j.1469-7580.2011.01394.x
Nyakatura, J. A., Melo, K., Horvat, T., Karakasiliotis, K., Allen, V. R., Andikfar, A., Andrada, E., Arnold, P., Lauströer, J., Hutchinson, J. R., Fischer, M. S., & Ijspeert, A. J. (2019). Reverse-engineering the locomotion of a stem amniote. Nature, 565(7739), 351–355. https://doi.org/10.1038/s41586-018-0851-2
Olsen, S. J. (1960). Age and faunal relationship of Tapiravus remains from Florida. Journal of Paleontology, 34(1), 164–167. https://www.jstor.org/stable/1300997
Olson, R. A., Glenn, Z. D., Cliffe, R. N., & Butcher, M. T. (2018). Architectural properties of sloth forelimb muscles (Pilosa: Bradypodidae). Journal of Mammalian Evolution, 25(4), 573–588. https://doi.org/10.1007/s10914-017-9411-z
Onwuama, K. T., Salami, S. O., Kigir, E. S., & Jaji, A. Z. (2021). Gross anatomical studies on the hind limb of the west African giraffe (Giraffa camelopardalis peralta). Veterinary Medicine International, 2021, 8818525. https://doi.org/10.1155/2021/8818525
Padilla, M., Dowler, R. C., & Downer, C. C. (2010). Tapirus pinchaque (Perissodactyla: Tapiridae). Mammalian Species, 42(1), 166–182.
Pampush, J. D., Winchester, J. M., Morse, P. E., Vining, A. Q., Boyer, D. M., & Kay, R. F. (2016). Introducing molaR: A new R package for quantitative topographic analysis of teeth (and other topographic surfaces). Journal of Mammalian Evolution, 23(4), 397–412. https://doi.org/10.1007/s10914-016-9326-0
Pereira, S. G., Santos, A. L. Q., Borges, D. C. S., de Souza, R. R., & Quaioz, P. R. (2015). Anatomia óssea e muscular do cíngulo escapular e braço de Tapirus terrestris (Perissodactyla: Tapiridae). Ciencia Animal Brasileira, 16(2), 268–278. https://doi.org/10.1590/1089-6891v16i228130
Pereira, S. G., Santos, A. L. Q., Borges, D. C. S., Ribeiro, P. R. Q., & Rodrigues de Souza, R. (2017). Bone and muscular anatomy of the forearm and hand in Tapirus terrestris (Perissodactyla, Tapiridae). Biotemas, 30(2), 35–41.
Qiu, Z., Yan, D., & Sun, B. (1991). A new genus of Tapiridae from Shanwang, Shandong. Vertebrata Palasiatica, 29(2), 119–135.
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
RC Epic Games Slovakia. (2023). Reality capture (1.2.1.116300). Epic Games Slovakia.
Regnault, S., & Pierce, S. E. (2018). Pectoral girdle and forelimb musculoskeletal function in the echidna (Tachyglossus aculeatus): Insights into mammalian locomotor evolution. Royal Society Open Science, 5(11), 181400. https://doi.org/10.1098/rsos.181400
Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rogers, C. W., Gee, E. K., & Dittmer, K. E. (2021). Growth and bone development in the horse: When is a horse skeletally mature? Animals, 11(12), 3402. https://doi.org/10.3390/ani11123402
RStudio Team. (2020). RStudio: Integrated Development for R. RStudio, PBC.
Smith, H. F., 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, e9866. https://doi.org/10.7717/peerj.9866
Spradley, J. P., Pampush, J. D., Morse, P. E., & Kay, R. F. (2017). Smooth operator: The effects of different 3D mesh retriangulation protocols on the computation of Dirichlet normal energy. American Journal of Physical Anthropology, 163(1), 94–109. https://doi.org/10.1002/ajpa.23188
Toledo, N., Bargo, M. S., & Vizcaíno, S. F. (2013). Muscular reconstruction and functional morphology of the forelimb of early Miocene sloths (Xenarthra, Folivora) of Patagonia. The Anatomical Record, 296(2), 305–325. https://doi.org/10.1002/ar.22627
Tong, H. W., & Wang, X. M. (2014). Juvenile skulls and other postcranial bones of Coelodonta nihowanensis from Shanshenmiaozui, Nihewan Basin, China. Journal of Vertebrate Paleontology, 34(3), 710–724. https://doi.org/10.1080/02724634.2013.814661
van der Made, J., & Stefanovic, I. (2006). A small tapir from the Turolian of Kreka (Bosnia) and a discussion on the biogeography and stratigraphy of the Neogene tapirs. Neues Jahrbuch Fur Geologie Und Palaontologie—Abhandlungen, 240(2), 207–240. https://doi.org/10.1127/njgpa/240/2006/207
van Houtven, K., & MacLaren, J. A. (2019). Shoulder-blade runners: Utility of the scapula fossa ratio to investigate locomotor evolution in equids (Mammalia: Perissodactyla). Journal of Morphology, 280(S1), S232.
Vélez-García, J. F., Ramírez-Arias, J. C., & Duque-Parra, J. E. (2018). 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(1), 1–7. https://doi.org/10.4025/actascibiolsci.v40i1.37861
Waldman, E., Gonzalez, Y., Flynn, J. J., & Tseng, Z. J. (2023). Dental topographic proxies for ecological characteristics in carnivoran mammals. Journal of Anatomy, 242(4), 627–641. https://doi.org/10.1111/joa.13806
Wareing, K., Tickle, P. G., Stokkan, K. A., Codd, J. R., & Sellers, W. I. (2011). The musculoskeletal anatomy of the reindeer (Rangifer tarandus): Fore- and hindlimb. Polar Biology, 34(10), 1571–1578. https://doi.org/10.1007/s00300-011-1017-y
Witmer, L. M. (1995). The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In J. J. Thomason (Ed.), Functional morphology in vertebrate paleontology (pp. 19–33). Cambridge University Press.
Wood, A. R., Bebej, R. M., Manz, C. L., Begun, D. L., & Gingerich, P. D. (2011). Postcranial functional morphology of Hyracotherium (Equidae, Perissodactyla) and locomotion in the earliest horses. Journal of Mammalian Evolution, 18(1), 1–32. https://doi.org/10.1007/s10914-010-9145-7