Advertisement

Journal of Mammalian Evolution

, Volume 23, Issue 3, pp 237–249 | Cite as

In the Pursuit of the Predatory Behavior of Borophagines (Mammalia, Carnivora, Canidae): Inferences from Forelimb Morphology

  • Alberto Martín-Serra
  • Borja Figueirido
  • Paul Palmqvist
Original Paper

Abstract

Here, we perform an ecomorphological study on the major bones (humerus, radius, and ulna) of the carnivoran forelimb using three-dimensional geometric morphometrics. More specifically, we test the association between forelimb morphology and predatory behavior. Our results suggest that the main morphological adaptions of carnivorans to different predatory behaviors relate to: (i) the capacity to perform long and efficient runs as in pounce/pursuit and pursuit predators; (ii) the ability to maneuver as in occasional predators; and (iii) the capacity to exert and resist large loads as in ambushing predators. We used borophagine canids as a case study, given the controversy on the predatory behavior of this extinct subfamily. Our results indicate that borophagines displayed a limited set of adaptions towards efficient running, including reduced joint mobility in both the elbow and the wrist, aspects in which they resemble the living canids. Furthermore, they had forelimbs as powerful as those of the extant ambushing carnivorans (i.e., most felids). This combination of traits suggests that the predatory behavior of borophagines was unique among carnivorans, as it was not fully equivalent to any of the living species.

Keywords

Ecomorphology Forelimb Predatory behavior Carnivora Borophaginae 

Notes

Acknowledgments

We are grateful to F. J. Serrano, J. A. Pérez Claros, and C. M. Janis and two anonymous reviewers for their helpful suggestions during the elaboration of the paper. We thank also S. Almécija for providing us the bone scanning surfaces and R. Portela (NHM, London), E. Westwig and Judith Galkin (AMNH, New York) for kindly providing us access to the specimens under their care. This study was supported by a PhD Research Fellowship (FPU) to AM-S from the “Ministerio de Educación y Ciencia” and CGL2012-37866 grant to BF from the “Ministerio de Economía y Competitividad”. The authors declare that there are not conflicts of interests.

Supplementary material

10914_2016_9321_MOESM1_ESM.pdf (1.5 mb)
ESM 1 (PDF 1.49 mb)

References

  1. Andersson K (2005) Were there pack-hunting canids in the Tertiary, and how can we know? Paleobiology 31:56–72CrossRefGoogle Scholar
  2. Andersson K, Werdelin L (2003) The evolution of cursorial carnivores in the Tertiary: implications of elbow-joint morphology. Proc R Soc Lond B 270:S163-S165CrossRefGoogle Scholar
  3. Anton M, Salesa MJ, Pastor JF, Sanchez IM, Fraile S, Morales J (2004) Implications of the mastoid anatomy of larger extant felids for the evolution and predatory behaviour of sabretoothed cats (Mammalia, Carnivora, Felidae). Zool J Linn Soc 140:207–221CrossRefGoogle Scholar
  4. Anyonge W (1996) Locomotor behaviour in Plio-Pleistocene sabre-tooth cats: a biomechanical analysis. J Zool 238:395–413CrossRefGoogle Scholar
  5. Argot C (2001) Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J Morphol 247:51–79CrossRefPubMedGoogle Scholar
  6. Argot C (2003) Functional adaptations of the postcranial skeleton of two Miocene borhyaenoids (Mammalia, Metatheria), Borhyaena and Prothylacinus, from South America. Palaeontology 46:1213–1267CrossRefGoogle Scholar
  7. Argot C (2004) Functional-adaptive analysis of the postcranial skeleton of a Laventan borhyaenoid, Lycopsis longirostris (Marsupialia, Mammalia). J Vertebr Paleontol 24:689–708CrossRefGoogle Scholar
  8. Beisiegel BD, Zuercher GL (2005) Speothos venaticus. Mammal Spec 783:1–6CrossRefGoogle Scholar
  9. Deutsch LA (1983) An encounter between bush dog (Speothos venaticus) and paca (Agouti paca). J Mammal 64:532–533CrossRefGoogle Scholar
  10. Dryden IL, Mardia K (1998) Statistical Analysis of Shape. Wiley, ChichesterGoogle Scholar
  11. Ercoli MD, Prevosti FJ, Álvarez A (2012) Form and function within a phylogenetic framework: locomotory habits of extant predators and some Miocene Sparassodonta (Metatheria). Zool J Linn Soc 165:224–251CrossRefGoogle Scholar
  12. Fabre AC, Cornette R, Slater G, Argot C, Peigné S, Goswami A, Pouydebat E (2013) Getting a grip on the evolution of grasping in musteloid carnivorans: a three-dimensional analysis of forelimb shape. J Evol Biol 26:1521–1535CrossRefPubMedGoogle Scholar
  13. Figueirido B, Janis CM (2011) The predatory behaviour of the thylacine: Tasmanian tiger or marsupial wolf? Biol Lett 7:937–940CrossRefPubMedPubMedCentralGoogle Scholar
  14. Figueirido B, Martín-Serra A, Tseng ZJ, Janis CM (2015) Habitat changes and changing predatory habits in North American fossil canids. Nat Comm 6:7976CrossRefGoogle Scholar
  15. Garland TJ, Janis CM (1993) Does metatarsal/femur ratio predict maximal running speed in cursorial mammals? J Zool 229:133–151CrossRefGoogle Scholar
  16. Harris MA, Steudel K (1997) Ecological correlates of hind-limb length in the Carnivora. J Zool 241:381–408CrossRefGoogle Scholar
  17. Heglund NC, Taylor CR, McMahon TA (1974) Scaling stride frequency and gait to animal size: mice to horses. Science 186:1112–1113CrossRefPubMedGoogle Scholar
  18. Iwaniuk AN, Pellis SM, Whishaw IQ (1999) The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora). Can J Zool 77:1064–1074CrossRefGoogle Scholar
  19. Janis CM, Figueirido B (2014) Forelimb anatomy and the discrimination of the predatory behavior of carnivorous mammals: the thylacine as a case study. J Morphol 275:1321–1338CrossRefPubMedGoogle Scholar
  20. Janis CM, Shoshitaishvili B, Kambic R, Figueirido B (2012) On their knees: distal femur asymmetry in ungulates and its relationship to body size and locomotion. J Vertebr Paleontol 32:433–445CrossRefGoogle Scholar
  21. Janis CM, Wilhelm PB (1993) Were there mammalian pursuit predators in the Tertiary? Dances with wolf avatars. J Mammal Evol 1:103–125CrossRefGoogle Scholar
  22. Kemp TJ, Bachus KN, Nairn JA, Carrier DR (2005) Functional trade-offs in the limb bones of dogs selected for running versus fighting. J Exp Biol 208:3475–3482CrossRefPubMedGoogle Scholar
  23. Kleiman DG (1972) Social behavior of the maned wolf (Chrysocyon brachyurus) and bush dog (Speothos venaticus): a study in contrast. J Mammal 53:791–806CrossRefGoogle Scholar
  24. Klingenberg CP (2011) MorphoJ. Faculty of Life Sciences, University of Manchester, Manchester. Mol Ecol Resour 11:353–357CrossRefPubMedGoogle Scholar
  25. Lewis ME, Lague MR (2010) Interpreting sabertooth cat (Carnivora; Felidae; Machairodontinae) postcranial morphology in light of scaling patterns in felids. In: Goswami A, Friscia A (eds) Carnivoran Evolution: New Views on Phylogeny, Form and Function. Cambridge University Press, Cambridge, pp 411–465Google Scholar
  26. MacLeod N, Rose KD (1993) Inferring locomotor behavior in Paleogene mammals via eigenshape analysis. Am J Sci 293:300–355CrossRefGoogle Scholar
  27. Martín-Serra A, Figueirido B, Palmqvist P (2014a) A three-dimensional analysis of morphological evolution and locomotor performance of the carnivoran forelimb. PloS ONE 9:e85574CrossRefPubMedPubMedCentralGoogle Scholar
  28. Martín-Serra A, Figueirido B, Palmqvist P (2014b) A three-dimensional analysis of the morphological evolution and locomotor behaviour of the carnivoran hind limb. BMC Evol Biol 14:129CrossRefPubMedPubMedCentralGoogle Scholar
  29. Martín-Serra A, Figueirido B, Pérez-Claros JA, Palmqvist P (2015) Patterns of morphological integration in the appendicular skeleton of mammalian carnivores. Evolution 69:321–340CrossRefPubMedGoogle Scholar
  30. Maynard-Smith J, Savage RJ (1955) Some locomotory adaptations in mammals. J Linn Soc Lond Zool 42:603–622CrossRefGoogle Scholar
  31. Meachen-Samuels JA (2012) Morphological convergence of the prey-killing arsenal of sabertooth predators. Paleobiology 38:715–728CrossRefGoogle Scholar
  32. Meachen-Samuels JA, Van Valkenburgh B (2009) Forelimb indicators of prey-size preference in the Felidae. J Morphol 270:729–744CrossRefPubMedGoogle Scholar
  33. Meloro C (2011) Locomotor adaptations in Plio-Pleistocene large carnivores from the Italian Peninsula: palaeoecological implications. Curr Zool 57:269–283CrossRefGoogle Scholar
  34. Mendoza M, Janis CM, Palmqvist P (2005) Ecological patterns in the trophic-size structure of large mammal communities: a ‘taxon-free’ characterization. Evol Ecol Res 7:505–530Google Scholar
  35. Mitteroecker P, Bookstein F (2011) Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 38:100–114CrossRefGoogle Scholar
  36. Munthe K (1989) The skeleton of the Borophaginae (Carnivora, Canidae). morphology and function. Univ Calif Publ Geol Sci 133:1–115Google Scholar
  37. Palmqvist P, Gröcke DR, Arribas A, Fariña RA (2003) Paleoecological reconstruction of a lower Pleistocene large mammal community using biogeochemical (δ13C, δ15N, δ18O, Sr: Zn) and ecomorphological approaches. Paleobiology 29:205–229CrossRefGoogle Scholar
  38. Pasi BM, Carrier DR (2003) Functional trade-offs in the limb muscles of dogs selected for running versus fighting. J Evol Biol 16:324–332CrossRefPubMedGoogle Scholar
  39. Polly PD (2010) Tiptoeing through the trophics: geographic variation in carnivoran locomotor ecomorphology in relation to environment. In: Goswami A, Friscia A (eds) Carnivoran Evolution: New Views on Phylogeny, Form and Function. Cambridge University Press, Cambridge, pp 347–410Google Scholar
  40. Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, CambridgeGoogle Scholar
  41. Rohlf FJ, Marcus LF (1993) A revolution morphometrics. Trends Ecol Evol 8:129–132CrossRefGoogle Scholar
  42. Salton JA, Sargis EJ (2008) Evolutionary morphology of the Tenrecoidea (Mammalia) forelimb skeleton. In: Sargis EJ, Dagosto M (eds) Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay. Springer, Dordrecht, pp 51–71Google Scholar
  43. Salton JA, Sargis EJ (2009) Evolutionary morphology of the Tenrecoidea (Mammalia) hindlimb skeleton. J Morphol 270:367–387CrossRefPubMedGoogle Scholar
  44. Samuels JX, Van Valkenburgh B (2008) Skeletal indicators of locomotor adaptations in living and extinct rodents. J Morphol 269:1387–1411CrossRefPubMedGoogle Scholar
  45. Samuels JX, Meachen JA, Sakay SA (2013) Postcranial morphology and the locomotor habits of living and extinct carnivorans. J Morphol 274:121–146CrossRefPubMedGoogle Scholar
  46. Schutz H, Guralnick RP (2007) Postcranial element shape and function: assessing locomotor mode in extant and extinct mustelid carnivorans. Zool J Linn Soc 150:895–914CrossRefGoogle Scholar
  47. Spoor CF, Badoux DM (1986) Descriptive and functional myology of the neck and forelimb of the striped hyena (Hyaena hyaena, L. 1758). Anat Anz 161:375–387PubMedGoogle Scholar
  48. Strang KT, Steudel K (1990) Explaining the scaling of transport costs: the role of stride frequency and stride length. J Zool 221:343–358CrossRefGoogle Scholar
  49. Taylor ME (1974) The functional anatomy of the forelimb of some African Viverridae (Carnivora). J Morphol 143:307–335CrossRefPubMedGoogle Scholar
  50. Taylor ME (1976) The functional anatomy of the hindlimb of some African Viverridae (Carnivora). J Morphol 148:227–253CrossRefPubMedGoogle Scholar
  51. Taylor ME (1989) Locomotor adaptations by carnivores. In: Gittleman JL (ed) Carnivore Behavior, Ecology, and Evolution. Cornell University Press, Ithaca, pp 382–409Google Scholar
  52. Tseng ZJ, Wang X (2010) Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). J Morphol 271:1386–1398CrossRefPubMedGoogle Scholar
  53. Van Valkenburgh B (1985) Locomotor diversity within past and present guilds of large predatory mammals. Paleobiology 11:406–428CrossRefGoogle Scholar
  54. Van Valkenburgh B (1987) Skeletal indicators of locomotor behavior in living and extinct carnivores. J Vertebr Paleontol 7:162–182CrossRefGoogle Scholar
  55. Van Valkenburgh B. (1999). Major patterns in the history of carnivorous mammals. Annu Rev Earth Planet Sci 27:463–493CrossRefGoogle Scholar
  56. Van Valkenburgh B, Sacco T, Wang X (2003) Chapter 7: pack hunting in Miocene borophagine dogs: evidence from craniodental morphology and body size. Bull Am Mus Nat Hist 279:147–162CrossRefGoogle Scholar
  57. Walmsley A, Elton S, Louys J, Bishop LC, Meloro C (2012) Humeral epiphyseal shape in the Felidae: the influence of phylogeny, allometry, and locomotion. J Morphol 273:1424–1438CrossRefPubMedGoogle Scholar
  58. Wang X, Tedford RH, Taylor BE (1999) Phylogenetic systematics of the Borophaginae (Carnivora, Canidae). Bull Am Mus Nat Hist 243: 1–391Google Scholar
  59. Werdelin L (1989) Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387–401CrossRefGoogle Scholar
  60. Wiley DF, Amenta N, Alcantara DA, Ghosh D, Kil YJ, Delson E, Harcourt-Smith W, Rohlf FJ, St. John K, Hamann B (2005) Evolutionary morphing. In: Proceedings of IEEE Visualization 2005 (VIS’05), pp 431–438Google Scholar
  61. Wilson DE, Mittermeier RA (2009) Handbook of the Mammals of the World. Vol. 1. Carnivores. Lynx Edicions, BarcelonaGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Departamento de Ecología y Geología, Facultad de CienciasUniversidad de MálagaMálagaSpain

Personalised recommendations