[en] The distal forelimb (autopodium) of quadrupedal mammals is a key morphological unit involved in locomotion, body support, and interaction with the substrate. The manus of the tapir (Perissodactyla: Tapirus) is unique within modern perissodactyls, as it retains the plesiomorphic tetradactyl (four-toed) condition also exhibited by basal equids and rhinoceroses. Tapirs are known to exhibit anatomical mesaxonic symmetry in the manus, although interspecific differences and biomechanical mesaxony have yet to be rigorously tested. Here, we investigate variation in the manus morphology of four modern tapir species (Tapirus indicus, Tapirus bairdii, Tapirus pinchaque, and Tapirus terrestris) using a geometric morphometric approach. Autopodial bones were laser scanned to capture surface shape and morphology was quantified using 3D-landmark analysis. Landmarks were aligned using Generalised Procrustes Analysis, with discriminant function and partial least square analyses performed on aligned coordinate data to identify features that significantly separate tapir species. Overall, our results support the previously held hypothesis that T. indicus is morphologically separate from neotropical tapirs; however, previous conclusions regarding function from morphological differences are shown to require reassessment. We find evidence indicating that T. bairdii exhibits reduced reliance on the lateral fifth digit compared to other tapirs. Morphometric assessment of the metacarpophalangeal joint and the morphology of the distal facets of the lunate lend evidence toward high loading on the lateral digits of both the large T. indicus (large body mass) and the small, long limbed T. pinchaque (ground impact). Our results support other recent studies on T. pinchaque, suggesting subtle but important adaptations to a compliant but inclined habitat. In conclusion, we demonstrate further evidence that the modern tapir forelimb is a variable locomotor unit with a range of interspecific features tailored to habitual and biomechanical needs of each species.
Disciplines :
Zoology
Author, co-author :
Maclaren, James ; Université de Liège - ULiège > Département de géologie > Evolution and diversity dynamics lab
Nauwelaerts, Sandra
Language :
English
Title :
Interspecific variation in the tetradactyl manus of modern tapirs (Perissodactyla: Tapirus) exposed using geometric morphometrics
Publication date :
July 2017
Journal title :
Journal of Morphology
ISSN :
0362-2525
eISSN :
1097-4687
Publisher :
John Wiley & Sons, Hoboken, United States - New York
Volume :
278
Issue :
1
Pages :
1517-1535
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen
Funding number :
Fonds Wetenschappelijk Onderzoek. Grant Number: 11Y7615N
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Bibliography
Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the “revolution. Italian Journal of Zoology, 71(1), 5–16.
Bressou, C. (1961). La myologie du tapir (Tapirus indicus L.). Mammalia, 25(3), 358–400.
Brown, J. C., & Yalden, D. W. (1973). The description of mammals – 2 Limbs and locomotion of terrestrial mammals. Mammal Review, 3(4), 107–134.
Budras, K.-D., Sack, W. O., & Rock, S. (2003). Thoracic limb. In K.-D. Budras, W. O. Sack, & S. Rock (Eds.), Anatomy of the horse (pp. 2–13). Stuttgart: Schlutersche.
Campbell, B. (1936). The comparative myology of the forelimb of the hippopotamus, pig and tapir. Americal Journal of Anatomy, 59(2), 201–247.
Cignoni, P., Callieri, M., Corsini, M., Dellapiane, M., Ganovelli, F., & Ranzuglia, G. (2008). MeshLab: an open-source mesh processing tool. In V. Scarano, R. De Chiara, & U. Erra (Eds.), Eurographics Italian Chapter Conference (pp. 1–8). Salerno.
Clayton, H. M., Chateau, H., & Back, W. (2013). Forelimb function. In W. Back & H. M. Clayton (Eds.), Equine locomotion (pp. 99–125). London: Saunders Elsevier.
Colbert, M. W. (2005). The facial skeleton of the early Oligocene Colodon (Perissodactyla, Tapiroidea). Palaeontologia Electronica, 8(1), 1–27.
Constantinescu, G. M., Habel, R. E., Hillebrand, A., Sack, W. O., Schaller, O., Simoens, P., & de Vos, N. R. (2012). Illustrated Veterinary Anatomical Nomenclature Third. In G. M. Constantinescu & O. Schaller (Eds.), (pp. 10–62) Stuttgart: 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.
Downer, C. C. (1996). The mountain tapir, endangered “flagship” species of the high Andes. Oryx, 30(1), 45–58.
Earle, C. (1893). Some points in the comparative osteology of the tapir. Science 21(526), 118.
Earle, C. (1896). Tapirs past and present. American Journal of Science, 4(104), 934–935.
Easton, K. L., & Kawcak, C. E. (2007). Evaluation of increased subchondral bone density in areas of contact in the metacarpophalangeal joint during joint loading in horses. American Journal of Veterinary Research, 68(8), 816–821.
Fadda, C., & Corti, M. (2001). Three-dimensional geometric morphometrics of Arvicanthis: Implications for systematics and taxonomy. Journal of Zoological Systematics and Evolutionary Research, 39(4), 235–245.
Gould, F. D. H. (2014). To 3D or not to 3D, that is the question: Do 3D surface analyses improve the ecomorphological power of the distal femur in placental mammals? PLoS One, 9(3), e91719.
Gregory, W. K. (1929). Mechanics of locomotion in the evolution of limb structure as bearing on the form and habits of the titanotheres and the related odd-toed ungulates. In H. F. Osborn (Ed.), The titanotheres of ancient Wyoming, Dakota and Nebraska (pp. 727–756). Washington, DC: United States Government Printing Office.
Hawkins, P. L. (2011). Variation in the modified first metatarsal of a large sample of Tapirus polkensis, and the functional implication for Ceratomorphs. East Tennessee State University.
Hellmund, M. (2005). A three-dimensional skeletal reconstruction of the Middle Eocene Propalaeotherium hassiacum Haupt 1925 (Equidae, Perissodactyla, Mammalia) and a modern synoptic painting of some individuals within their habitat. Current Research in Vertebrate Palaeontolgy 3rd Annual Meeting of the European Association of Vertebrate Palaeontologists (EAVP; p. 15). Hessisches Landesmuseum Darmstadt.
Hershkovitz, P. (1954). Mammals of Northern Colombia, Preliminary Report No. 7: Tapirs (genus Tapirus) with a systematic review of American species. Proceedings of the United States National Museum, 103, 465–496.
Hildebrand, M. (1985). Walking and running. In M. Hildebrand, et al., (Eds.), Functional vertebrate morphology, (pp. 38–57). Cambridge: Harvard University Press
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.
Holbrook, L. (2001). Comparative osteology of early Tertiary tapiromorphs (Mammalia, Perissodactyla). Zoological Journal of the Linnean Society, 132(1), 1–54.
Holbrook, L. T. (1999). The phylogeny and classification of tapiromorph perissodactyls (Mammalia). Cladistics, 15(3), 331–350.
Holbrook, L. T. (2009). Osteology of Lophiodon Cuvier, 1822 (Mammalia, Perissodactyla) and its phylogenetic implications. Journal of Vertebrate Paleontology, 29(1), 212–230.
Hulbert, R. C. (1995). The giant tapir, Tapirus haysii, from Leisey Shell Pit 1A and other Florida Irvingtonian localities. Bulletin of the Florida Museum of Natural History, 37(16), 515–551.
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.
Hulbert, R. C., Wallace, S. C., Klippel, W. E., & Parmalee, P. W. (2009). Cranial morphology and systematics of an extraordinary sample of the Late Neogene dwarf tapir, Tapirus polkensis (Olsen). Journal of Paleontology, 83(2), 238–262.
IBM Corp. (2013). IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM Corp.
Janis, C. (1984). Tapirs as living fossils. In N. Eldredge & S. M. Stanley (Eds.), Living fossils. Casebooks in earth sciences (pp. 80–86). New York, NY: Springer New York.
Janis, C. M. (1989). A climatic explanation for patterns of evolutionary diversity in ungulate mammals. Palaeontology, 32(3), 463–481.
Klaits, B. G. (1972). The moving mesaxonic manus—A comparison of tapirs and rhinoceroses. Mammalia, 36(1), 126–145.
Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11(4), 405–421.
Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357.
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 (pp. 145–214). Stuttgart: Schlutersche.
Lockley, M. G. (2009). New perspectives on morphological variation in tridactyl foot prints : Clues to widespread convergence in developmental dynamics. Geological Quarterly, 53(4), 415–432.
MacFadden, B. J. (1992). Fossil horses: Systematics, paleobiology and evolution of the family equidae. Cambridge: Cambridge University Press.
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.
Murie, J. (1871). The Malayan tapir. Journal of Anatomy and Physiology, 6(1), 131–512.
Nauwelaerts, S., Vangeel, K., & Aerts, P. (2016). Loading distribution over the four fingers of the tapir during locomotion. 11th International Congress of Vertebrate Morphology, Washington, DC.
Norman, J. E., & Ashley, M. V. (2000). Phylogenetics of Perissodactyla and tests of the molecular clock. Journal of Molecular Evolution, 50(1), 11–21.
Osborn, H. F. (1929). Theories as to the origin, ancestry, and adaptive radiation of the titanotheres and other odd-toed ungulates. In H. F. Osborn (Ed.), The titanotheres of ancient Wyoming, Dakota and Nebraska (pp. 757–804). Washington, DC: United States Government Printing Office.
Padilla, M., Dowler, R. C., & Downer, C. C. (2010). Tapirus pinchaque (Perissodactyla: Tapiridae). Mammalian Species, 42(1), 166–182.
Pereira, S. G. (2013). Anatomia ossea, muscular e consideracoes adaptativas do membro toracico de Tapirus terrestris (Perissodactyla, Tapiridae). (pp. 1–76). Universidade Federal de Uberlandia (thesis). Minas Gerais, Brazil.
Prothero, D. R. (2005). Postcranial osteology. In The evolution of North American Rhinoceroses (pp. 146–181). Cambridge: Cambridge University Press.
R Core Development Team. (2008). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Radinsky, L. B. (1965). Evolution of the tapiroid skeleton from Heptodon to Tapirus. Bulletin of the Museum of Comparative Zoology, 134, 69–106.
Rajkumar, H. S., & Klein, H. (2014). First perissodactyl footprints from Flysch deposits of the Barail Group (Lower Oligocene) of Manipur, India. Proceedings of the Indian Academy of Sciences. Earth and Planetary Sciences, 123(2), 413–420.
Reghem, E., Byron, C., Bels, V., & Pouydebat, E. (2012). Hand posture in the grey mouse lemur during arboreal locomotion on narrow branches. Journal of Zoology, 288(1), 76–81.
Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49(4), 740–753.
Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39(1), 40–59.
Ruiz-García, M., Vásquez, C., Pinedo-Castro, M., Sandoval, S., Castellanos, A., Kaston, F., de Thoisy, B., Shostell, J. (2012). Phylogeography of the mountain tapir (Tapirus pinchaque) and the Central American tapir (Tapirus bairdii) and the origins of the three Latin-American tapirs by means of mtCyt-B sequences. In K. Anamthawat-Jnsson (Ed.), Current topics in phylogenetics and phylogeography of terrestrial and aquatic systems (pp. 83–116). InTech. Retrieved from https://www.intechopen.com/books/
Ruiz-García, M., Castellanos, A., Bernal, L. A., Pinedo-Castro, M., Kaston, F., & Shostell, J. M. (2016). Mitogenomics of the mountain tapir (Tapirus pinchaque, Tapiridae, Perissodactyla, Mammalia) in Colombia and Ecuador: Phylogeography and insights into the origin and systematics of the South American tapirs. Mammalian Biology - Zeitschrift Für Säugetierkunde, 81(2), 163–175.
Schoch, R. M. (1989). A review of the tapiroids. In D. R. Prothero & R. M. Schoch (Eds.), The evolution of perissodactyls (pp. 299–320). New York: Oxford University Press.
Simpson, G. G. (1945). Notes on Pleistocene and recent tapirs. Bulletin of the American Museum of Natural History, 86(2), 33–82.
Steiner, C. C., & Ryder, O. A. (2011). Molecular phylogeny and evolution of the Perissodactyla. Zoological Journal of the Linnean Society, 163(4), 1289–1303.
de Thoisy, B., Pukazhenthi, B., Janssen, D. L., Torres, I. L., May Jr., J. A., Medici, P. … Quse, V. (2014). Tapir Veterinary Manual (2nd ed.). In V. Quse & R. C. Fernandes-Santos (Eds.), IUCN/SSC Tapir Specialist Group.
Thomason, J. J. (1985). Estimation of locomotory forces and stresses in the limb bones of recent and extinct equids. Paleobiology, 11(2), 209–220.
Tougard, C., Delefosse, T., Hänni, C., & Montgelard, C. (2001). Phylogenetic relationships of the five extant Rhinoceros species (Rhinocerotidae, Perissodactyla) based on mitochondrial cytochrome b and 12S rRNA genes. Molecular Phylogenetics and Evolution, 19(1), 34–44.
Wiley, D. F., Amenta, N., Alcantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., … O'Neill, R. (2005). Evolutionary morphing. In: IEEE Visualization. VIS 05. Minneapolis, MN, USA. 431–438.
Wood, A. R. et al. (2010). Postcranial functional morphology of Hyracotherium (Equidae, Perissodactyla) and locomotion in the earliest horses. Journal of Mammalian Evolution, 18(1), 1–32.
Yalden, D. W. (1971). The functional morphology of the carpus in ungulate mammals. Cells Tissues Organs, 78(4), 461–487.
Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer. New York: Academic Press.
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