Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Andersson K (2005) Were there pack-hunting canids in the Tertiary, and how can we know? Paleobiology 31:56–72

    Article  Google Scholar 

  • 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-S165

    Article  Google Scholar 

  • 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 140:207–221

    Article  Google Scholar 

  • Anyonge W (1996) Locomotor behaviour in Plio-Pleistocene sabre-tooth cats: a biomechanical analysis. J Zool 238:395–413

    Article  Google Scholar 

  • 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 247:51–79

    Article  CAS  PubMed  Google Scholar 

  • Argot C (2003) Functional adaptations of the postcranial skeleton of two Miocene borhyaenoids (Mammalia, Metatheria), Borhyaena and Prothylacinus, from South America. Palaeontology 46:1213–1267

    Article  Google Scholar 

  • Argot C (2004) Functional-adaptive analysis of the postcranial skeleton of a Laventan borhyaenoid, Lycopsis longirostris (Marsupialia, Mammalia). J Vertebr Paleontol 24:689–708

    Article  Google Scholar 

  • Beisiegel BD, Zuercher GL (2005) Speothos venaticus. Mammal Spec 783:1–6

    Article  Google Scholar 

  • Deutsch LA (1983) An encounter between bush dog (Speothos venaticus) and paca (Agouti paca). J Mammal 64:532–533

    Article  Google Scholar 

  • Dryden IL, Mardia K (1998) Statistical Analysis of Shape. Wiley, Chichester

    Google Scholar 

  • 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 165:224–251

    Article  Google Scholar 

  • 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 26:1521–1535

    Article  PubMed  Google Scholar 

  • Figueirido B, Janis CM (2011) The predatory behaviour of the thylacine: Tasmanian tiger or marsupial wolf? Biol Lett 7:937–940

    Article  PubMed  PubMed Central  Google Scholar 

  • Figueirido B, Martín-Serra A, Tseng ZJ, Janis CM (2015) Habitat changes and changing predatory habits in North American fossil canids. Nat Comm 6:7976

    Article  CAS  Google Scholar 

  • Garland TJ, Janis CM (1993) Does metatarsal/femur ratio predict maximal running speed in cursorial mammals? J Zool 229:133–151

    Article  Google Scholar 

  • Harris MA, Steudel K (1997) Ecological correlates of hind-limb length in the Carnivora. J Zool 241:381–408

    Article  Google Scholar 

  • Heglund NC, Taylor CR, McMahon TA (1974) Scaling stride frequency and gait to animal size: mice to horses. Science 186:1112–1113

    Article  CAS  PubMed  Google Scholar 

  • Iwaniuk AN, Pellis SM, Whishaw IQ (1999) The relationship between forelimb morphology and behaviour in North American carnivores (Carnivora). Can J Zool 77:1064–1074

    Article  Google Scholar 

  • 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 275:1321–1338

    Article  PubMed  Google Scholar 

  • 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 32:433–445

    Article  Google Scholar 

  • Janis CM, Wilhelm PB (1993) Were there mammalian pursuit predators in the Tertiary? Dances with wolf avatars. J Mammal Evol 1:103–125

    Article  Google Scholar 

  • 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 208:3475–3482

    Article  CAS  PubMed  Google Scholar 

  • Kleiman DG (1972) Social behavior of the maned wolf (Chrysocyon brachyurus) and bush dog (Speothos venaticus): a study in contrast. J Mammal 53:791–806

    Article  Google Scholar 

  • Klingenberg CP (2011) MorphoJ. Faculty of Life Sciences, University of Manchester, Manchester. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • 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 411–465

  • MacLeod N, Rose KD (1993) Inferring locomotor behavior in Paleogene mammals via eigenshape analysis. Am J Sci 293:300–355

    Article  Google Scholar 

  • 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:e85574

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 14:129

    Article  PubMed  PubMed Central  Google Scholar 

  • Martín-Serra A, Figueirido B, Pérez-Claros JA, Palmqvist P (2015) Patterns of morphological integration in the appendicular skeleton of mammalian carnivores. Evolution 69:321–340

    Article  PubMed  Google Scholar 

  • Maynard-Smith J, Savage RJ (1955) Some locomotory adaptations in mammals. J Linn Soc Lond Zool 42:603–622

    Article  Google Scholar 

  • Meachen-Samuels JA (2012) Morphological convergence of the prey-killing arsenal of sabertooth predators. Paleobiology 38:715–728

    Article  Google Scholar 

  • Meachen-Samuels JA, Van Valkenburgh B (2009) Forelimb indicators of prey-size preference in the Felidae. J Morphol 270:729–744

    Article  PubMed  Google Scholar 

  • Meloro C (2011) Locomotor adaptations in Plio-Pleistocene large carnivores from the Italian Peninsula: palaeoecological implications. Curr Zool 57:269–283

    Article  Google Scholar 

  • 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 7:505–530

    Google Scholar 

  • Mitteroecker P, Bookstein F (2011) Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 38:100–114

    Article  Google Scholar 

  • Munthe K (1989) The skeleton of the Borophaginae (Carnivora, Canidae). morphology and function. Univ Calif Publ Geol Sci 133:1–115

    Google Scholar 

  • 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 29:205–229

    Article  Google Scholar 

  • Pasi BM, Carrier DR (2003) Functional trade-offs in the limb muscles of dogs selected for running versus fighting. J Evol Biol 16:324–332

    Article  CAS  PubMed  Google Scholar 

  • 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 347–410

  • Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge

  • Rohlf FJ, Marcus LF (1993) A revolution morphometrics. Trends Ecol Evol 8:129–132

    Article  Google Scholar 

  • 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 51–71

  • Salton JA, Sargis EJ (2009) Evolutionary morphology of the Tenrecoidea (Mammalia) hindlimb skeleton. J Morphol 270:367–387

    Article  PubMed  Google Scholar 

  • Samuels JX, Van Valkenburgh B (2008) Skeletal indicators of locomotor adaptations in living and extinct rodents. J Morphol 269:1387–1411

    Article  PubMed  Google Scholar 

  • Samuels JX, Meachen JA, Sakay SA (2013) Postcranial morphology and the locomotor habits of living and extinct carnivorans. J Morphol 274:121–146

    Article  PubMed  Google Scholar 

  • Schutz H, Guralnick RP (2007) Postcranial element shape and function: assessing locomotor mode in extant and extinct mustelid carnivorans. Zool J Linn Soc 150:895–914

    Article  Google Scholar 

  • Spoor CF, Badoux DM (1986) Descriptive and functional myology of the neck and forelimb of the striped hyena (Hyaena hyaena, L. 1758). Anat Anz 161:375–387

    CAS  PubMed  Google Scholar 

  • Strang KT, Steudel K (1990) Explaining the scaling of transport costs: the role of stride frequency and stride length. J Zool 221:343–358

    Article  Google Scholar 

  • Taylor ME (1974) The functional anatomy of the forelimb of some African Viverridae (Carnivora). J Morphol 143:307–335

    Article  CAS  PubMed  Google Scholar 

  • Taylor ME (1976) The functional anatomy of the hindlimb of some African Viverridae (Carnivora). J Morphol 148:227–253

    Article  CAS  PubMed  Google Scholar 

  • Taylor ME (1989) Locomotor adaptations by carnivores. In: Gittleman JL (ed) Carnivore Behavior, Ecology, and Evolution. Cornell University Press, Ithaca, pp 382–409

  • Tseng ZJ, Wang X (2010) Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). J Morphol 271:1386–1398

    Article  PubMed  Google Scholar 

  • Van Valkenburgh B (1985) Locomotor diversity within past and present guilds of large predatory mammals. Paleobiology 11:406–428

    Article  Google Scholar 

  • Van Valkenburgh B (1987) Skeletal indicators of locomotor behavior in living and extinct carnivores. J Vertebr Paleontol 7:162–182

    Article  Google Scholar 

  • Van Valkenburgh B. (1999). Major patterns in the history of carnivorous mammals. Annu Rev Earth Planet Sci 27:463–493

    Article  Google Scholar 

  • 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 279:147–162

    Article  Google Scholar 

  • 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 273:1424–1438

    Article  PubMed  Google Scholar 

  • Wang X, Tedford RH, Taylor BE (1999) Phylogenetic systematics of the Borophaginae (Carnivora, Canidae). Bull Am Mus Nat Hist 243: 1–391

    Google Scholar 

  • Werdelin L (1989) Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387–401

    Article  Google Scholar 

  • 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 431–438

  • Wilson DE, Mittermeier RA (2009) Handbook of the Mammals of the World. Vol. 1. Carnivores. Lynx Edicions, Barcelona

Download references

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.

Author information

Authors and Affiliations

  1. Departamento de Ecología y Geología, Facultad de Ciencias, Universidad de Málaga, Campus de Teatinos s/n, 20971, Málaga, Spain

    Alberto Martín-Serra, Borja Figueirido & Paul Palmqvist

Authors
  1. Alberto Martín-Serra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Borja Figueirido
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul Palmqvist
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alberto Martín-Serra.

Electronic supplementary material

ESM 1

(PDF 1.49 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martín-Serra, A., Figueirido, B. & Palmqvist, P. In the Pursuit of the Predatory Behavior of Borophagines (Mammalia, Carnivora, Canidae): Inferences from Forelimb Morphology. J Mammal Evol 23, 237–249 (2016). https://doi.org/10.1007/s10914-016-9321-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-016-9321-5

Keywords

Search

Navigation