The Morphology of the Bovid Calcaneus: Function, Phylogenetic Signal, and Allometric Scaling

  • W. Andrew Barr
Original Paper


Despite its clear functional role in hock (ankle) plantarflexion, the bovid calcaneus has been understudied with respect to the functional constraints imposed by locomotion in differing habitats, the allometric influence of inter-specific body size differences, and phylogenetic signal. This study uses a comparative sample of extant bovid species to shed light on the evolution of bovid calcaneal morphology. I measured eight linear measurements on 204 calcaneus specimens representing 41 extant bovid species. Using a morphological body size proxy validated against published species-mean body mass estimates, I performed Ordinary Least Squares regression to examine the allometric relationships of each measurement with body size. I classified each bovid species to a preferred habitat type based on published literature, and performed Phylogenetic Generalized Least Squares (PGLS) to test for differences in morphology between bovid taxa with different preferred habitats while considering evolutionary relatedness. I visualized morphological differences between taxa using Principal Components Analysis plotted in a phylomorphospace. Results demonstrate that several measurements of the bovid calcaneus have an allometric relationship to body size. The functional length of the calcaneus scales with negative allometry, which likely maintains a comparable safety factor within the calcaneal tuber at larger body sizes. While open-habitat bovids have relatively shorter calcaneal tubers, this difference is not significant when controlling for the influence of body size and phylogenetic signal using PGLS. Among bovid tribes that have a deep evolutionary history of adaptation to open habitats, Antilopini have relatively longer calcaneal tubers than Alcelaphini or Hippotragini, which may reflect the unique importance of stotting behavior in predator avoidance among antelopins. Overall, the morphology of the bovid calcaneus has been shaped by a complex interaction of phylogenetic and body-size constraints as well as adaptation to modes of predator avoidance mediated by preferred habitat.


Bovidae Ecomorphology Functional morphology Antelope Functional traits 



I am grateful to Eileen Westwig of the American Museum of Natural History for making the trek out to Brooklyn to supervise my research at the AMNH remote storage facility. Thanks to John Kappelman, Liza Shapiro, Denné Reed, and Gabrielle Russo for helping me think through the functional anatomy of bovid hock joints. This work was partially supported by a Wenner-Gren Foundation Dissertation Research Grant (grant number 8557).

Supplementary material

10914_2018_9446_MOESM1_ESM.csv (24 kb)
ESM 1 (CSV 24 kb)


  1. Alexander RM, Bennett MB (1987) Some principles of ligament function, with examples from the tarsal joints of the sheep (Ovis aries). J Zool 211:487–504CrossRefGoogle Scholar
  2. Barr WA (2014) Functional morphology of the bovid astragalus in relation to habitat: controlling phylogenetic signal in ecomorphology. J Morphol 275:1201–1216CrossRefPubMedGoogle Scholar
  3. Barr WA (2015) Paleoenvironments of the Shungura Formation (Plio-Pleistocene: Ethiopia) based on ecomorphology of the bovid astragalus. J Hum Evol 88:97–107CrossRefPubMedGoogle Scholar
  4. Behrensmeyer AK (1975) The taphonomy and paleoecology of Plio-Pleistocene vertebrate assemblages east of Lake Rudolf, Kenya Bull Mus Comp Zool 146:473–578Google Scholar
  5. Bibi F, Souron A, Bocherens H, Uno K, Boisserie, JR (2013) Ecological change in the lower Omo Valley around 2.8 Ma Biol Lett 9:20120890CrossRefPubMedGoogle Scholar
  6. Biewener A (1989) Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45–48CrossRefPubMedGoogle Scholar
  7. Biewener A (1990) Biomechanics of mammalian terrestrial locomotion. Science 250:1097–1103CrossRefPubMedGoogle Scholar
  8. Carrier DR, Heglund NC, Earls KD (1994) Variable gearing during locomotion in the human musculoskeletal system. Science 265: 651–653CrossRefPubMedGoogle Scholar
  9. Cerling TE, Andanje, SA, Blumenthal SA, Brown FH, Chritz KL, Harris JM, Hart JA, Kirera FM, Kaleme P, Leakey LN, Leakey MG, Levin NE, Manthi FK, Passey BH, Uno KT (2015) Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 ma. Proc Natl Acad Sci U S A 112:11467–11472CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cerling TE, Harris J, Leakey M (2003) Isotope paleoecology of the Nawata and Nachukui formations at Lothagam, Turkana Basin, Kenya. In: Leakey M, Harris J (eds) Lothagam: The Dawn of Humanity in Eastern Africa. Columbia University Press, New York, pp 605–624Google Scholar
  11. Curran SC (2012) Expanding ecomorphological methods: geometric morphometric analysis of Cervidae post-crania. J Archaeol Sci 39:1172–1182CrossRefGoogle Scholar
  12. Curran SC (2015). Exploring Eucladoceros ecomorphology using geometric morphometrics. Anat Rec 298:291–313CrossRefGoogle Scholar
  13. DeGusta D, Vrba E (2003) A method for inferring paleohabitats from the functional morphology of bovid astragali. J Archaeol Sci 30:1009–1022CrossRefGoogle Scholar
  14. DeGusta D, Vrba E (2005) Methods for inferring paleohabitats from the functional morphology of bovid phalanges. J Archaeol Sci 32:1099–1113CrossRefGoogle Scholar
  15. Estes RD (1992) The Behavior Guide to African Mammals: Including Hoofed Mammals, Carnivores, Primates. University of California Press, BerkeleyGoogle Scholar
  16. Gálvez-López E, Casinos A (2012) Scaling and mechanics of the felid calcaneus: geometric similarity without differential allometric scaling. J Anat 220:555–563CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gambaryan PP (1974) How Animals Run: Anatomical Adaptations. Wiley, New YorkGoogle Scholar
  18. Gregory WK (1912) Notes on the principles of quadrupedal locomotion and on the mechanism of the limbs in hoofed animals. Ann N Y Acad Sci 22:267–294CrossRefGoogle Scholar
  19. Hernández Fernández M, Vrba ES (2005) A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol Rev Camb Philos Soc 80:269–302CrossRefPubMedGoogle Scholar
  20. Hildebrand M (1962) Walking, running, and jumping. Am Zool 2:151–155CrossRefGoogle Scholar
  21. Hildebrand M (1987) The mechanics of horse legs. Am Sci 75:594–601Google Scholar
  22. Jarman PJ (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267CrossRefGoogle Scholar
  23. Jones KE, Bielby J, Cardillo M, Fritz SA, O’Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster CA, Price SA, Rigby EA, Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A, Michener WK (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648CrossRefGoogle Scholar
  24. Jungers WL, Falsetti AB, Wall CE (1995). Shape, relative size, and size-adjustments in morphometrics. Yearb Phys Anthropol 38:137–161CrossRefGoogle Scholar
  25. Kappelman JW (1988) Morphology and locomotor adaptations of the bovid femur in relation to habitat. J Morphol 198:119–130CrossRefPubMedGoogle Scholar
  26. Kappelman JW (1991) The paleoenvironment of Kenyapithecus at Fort Ternan. J Hum Evol 20:95–129CrossRefGoogle Scholar
  27. Kappelman JW, Plummer TW, Bishop L, Duncan A, Appleton S (1997) Bovids as indicators of Plio-Pleistocene paleoenvironments in East Africa. J Hum Evol 32:229–256CrossRefPubMedGoogle Scholar
  28. Kingdon J (1974) East African Mammals (Vol. II). University of Chicago Press, ChicagoGoogle Scholar
  29. Kovarovic K (2004) Bovids as palaeoenvironmental indicators: an ecomorphological analysis of bovid post-cranial remains from Laetoli, Tanzania. Dissertation, University College, LondonGoogle Scholar
  30. Kovarovic K, Andrews P (2007) Bovid postcranial ecomorphological survey of the Laetoli paleoenvironment. J Hum Evol 52:663–680CrossRefPubMedGoogle Scholar
  31. Leuthold W (1978) On social organization and behaviour of the gerenuk Litocranius walleri (Brooke 1878). Z Tierpsychol, 47:194–216.CrossRefPubMedGoogle Scholar
  32. Louys J, Montanari S, Plummer TW, Hertel F, Bishop LC (2012) Evolutionary divergence and convergence in shape and size within African antelope proximal phalanges. J Mammal Evol 20: 239–248CrossRefGoogle Scholar
  33. Maynard Smith J, Savage RJG (1956) Some locomotory adaptations in mammals. Zool J Linn Soc 42:603–622CrossRefGoogle Scholar
  34. McMahon TA (1975) Using body size to understand the structural design of animals: quadrupedal locomotion. J Appl Physiol 39:619–627CrossRefPubMedGoogle Scholar
  35. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N (2011) caper: comparative analyses of phylogenetics and evolution in R.
  36. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884CrossRefPubMedGoogle Scholar
  37. Plummer TW, Bishop LC (1994) Hominid paleoecology at Olduvai Gorge, Tanzania as indicated by antelope remains. J Hum Evol 27:47–75CrossRefGoogle Scholar
  38. Plummer TW, Bishop LC, Hertel F (2008) Habitat preference of extant African bovids based on astragalus morphology: operationalizing ecomorphology for palaeoenvironmental reconstruction. J Archaeol Sci 35:3016–3027CrossRefGoogle Scholar
  39. Plummer TW, Ferraro JV, Louys J, Hertel F, Alemseged Z, Bobe R, Bishop LC (2015) Bovid ecomorphology and hominin paleoenvironments of the Shungura Formation, lower Omo River valley, Ethiopia. J Hum Evol 88:108–126CrossRefPubMedGoogle Scholar
  40. R Development Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  41. Revell LJ (2012) Phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223Google Scholar
  42. Rose KD (1982) Skeleton of Diacodexis, oldest known artiodactyl. Science 216:621–623CrossRefPubMedGoogle Scholar
  43. Schaeffer B (1947) Notes on the origin and function of the artiodactyl tarsus. Am Mus Novitates 1356: 1–24Google Scholar
  44. Schaeffer B (1948) The origin of a mammalian ordinal character. Evolution 2:164–175CrossRefGoogle Scholar
  45. Schmidt-Nielsen K (1984) Scaling, Why Is Animal Size So Important? Cambridge University Press, CambridgeCrossRefGoogle Scholar
  46. Scott KM (1979) Adaptation and allometry in bovid postcranial proportions. Dissertation, Yale University, New HavenGoogle Scholar
  47. Scott KM (1985) Allometric trends and locomotor adaptations in the Bovidae. Bull Am Mus Nat Hist 179:197–288.Google Scholar
  48. Scott R (2004) The comparative paleoecology of late Miocene Eurasian hominoids. Dissertation, The University of Texas, AustinGoogle Scholar
  49. Scott RS, Barr WA (2014) Ecomorphology and phylogenetic risk: implications for habitat reconstruction using fossil bovids. J Hum Evol 73:47–57CrossRefPubMedGoogle Scholar
  50. Skinner JD, Chimimba CT (2006) The Mammals of the Southern African Sub-Region. Cambridge University Press, CambridgeGoogle Scholar
  51. Vrba ES (1980) The significance of bovid remains as indicators of environment and predation patterns. In: Behrensmeyer AK, Hill A (eds) Fossils in the Making: Vertebrate Taphonomy and Paleoecology. Chicago University Press, Chicago pp 247–272Google Scholar
  52. Wilson DC, Reeder DM (2005) Mammal Species of the World: A Taxonomic and Geographic Reference. Johns Hopkins University Press, BaltimoreGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Center for the Advanced Study of Human PaleobiologyThe George Washington UniversityWashingtonUSA

Personalised recommendations