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Journal of Mammalian Evolution

, Volume 22, Issue 3, pp 421–434 | Cite as

The Endocranial Morphology of the Plio-Pleistocene Bone-Cracking Hyena Pliocrocuta perrieri: Behavioral Implications

  • Víctor Vinuesa
  • Joan Madurell-Malapeira
  • Josep Fortuny
  • David M. Alba
Original Paper

Abstract

The internal cranial morphology of the bone-cracking hyena Pliocrocuta perrieri (Carnivora, Hyaenidae) is described based on three crania from the late Pliocene and early Pleistocene of the Iberian Peninsula. The shape and size of the inner cranial cavities (with emphasis on encephalization and relative regional brain volumes) are compared with those of extant hyaenids with the aid of computed tomography techniques—which had not been previously used to study the brain morphology of any extinct bone-cracking hyena. Our results indicate that the frontal sinuses of P. perrieri are caudally extended and overlap the brain cavity, as in other extinct and extant bone-cracking hyaenids. In turn, the brain morphology and sulcal pattern of P. perrieri are more similar to those of Hyaena hyaena and Parahyaena brunnea than to those of Crocuta crocuta among extant bone-cracking hyaenids. Our results further indicate that Pliocrocuta is clearly less encephalized than the highly-social Crocuta, and displays an anterior cerebrum relatively smaller than in all extant bone-cracking hyenas (indicating the possession of a poorly-developed frontal cortex). These facts might suggest that P. perrieri possessed less developed cognitive abilities than Crocuta for processing the information associated with complex social behaviors.

Keywords

Carnivora Hyaenidae CT-scan Brain Frontal sinus 

Notes

Acknowledgments

We are particularly grateful to Sergio Llácer for assistance with image processing. We also thank the Mútua de Terrassa for access to CT-scanning facilities, E. Gilissen and W. Wendelen for allowing us to study comparison material under their care, S. Sakai and L. Werdelin for sending relevant literature cited in this paper, M. Pina for assistance with ANCOVA comparisons, and T. Rowe and J. Maisano (University of Texas and Digimorph website) for providing to us the CT-scans of extant hyaenids. This paper greatlly benefited from the careful reading and thoughtful comments by the Editor J. R. Wible and two anonymous reviewers on a previous version of the manuscript.

References

  1. Adolphs R (2001) The neurobiology of social cognition. Curr Opin Neurobiol 11: 231–239. doi:  10.1016/S0959-4388(00)00202-6 PubMedCrossRefGoogle Scholar
  2. Agustí J, Oms O (2001) On the age of the last hipparionine faunas in western Europe. C R Acad Sci Paris 332: 291–297. doi:  10.1016/S1251-8050(01)01523-3 Google Scholar
  3. Alba DM (2010) Cognitive inferences in fossil apes (Primates: Hominoidea): does encephalization reflect intelligence? J Anthropol Sci 88: 11–48PubMedGoogle Scholar
  4. Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7: 268–277. doi:  10.1038/nrn1884 PubMedCrossRefGoogle Scholar
  5. Anadón P, Utrilla R, Vázquez A, Martín-Rubio M, Rodriguez-Lázaro J, Robles F (2009) Paleoenviromental evolution of the Pliocene Villarroya lake, northern Spain, from stable isotopes and trace-element geochemistry of ostracods and mollusks. J Paleolimnol 39: 339–419. doi:  10.1007/s10933-007-9121-2 Google Scholar
  6. Andersson J (2005) Were there pack-hunting canids in the Tertiary, and how can we know? Paleobiology 31: 56–72CrossRefGoogle Scholar
  7. Antón M, Turner A, Salesa MJ, Morales J (2006) A complete skull of Chasmaporthetes lunensis (Carnivora, Hyaenidae) from the Spanish Pliocene site of La Puebla de Valverde (Teruel). Estudios Geol 62: 375–388. doi:  10.3989/egeol.0662132 CrossRefGoogle Scholar
  8. Arribas Herrera A, Bernad García J (1994) Catálogo de mamíferos pliocenos del yacimiento de Villarroya (La Rioja), en la colección del Museo Geominero. Bol Geol Min 105: 236–248Google Scholar
  9. Arsznov BM, Lundrigan BL, Holekamp KE, Sakai ST (2010) Sex and the frontal cortex: a developmental CT study in the spotted hyena. Brain Behav Evol 76: 185–97. doi:  10.1159/000321317 PubMedCrossRefGoogle Scholar
  10. Barton RA, Dunbar RIM (1997) Evolution of the social brain. In: Whiten A, Byrne R (eds) Machiavellian Inteligence II. Cambridge Unversity Press, Cambridge, pp 240–263CrossRefGoogle Scholar
  11. Boaz NT, Ciochon RL, Xu Q, Liu J (2000) Large mammalian carnivores as a taphonomic factor in the bone accumulation at Zhoukoudian. Acta Anthropol Sinica 19: 224–234Google Scholar
  12. Byrne R, Whiten A (1988) Machiavellian Intelligence. Oxford University Press, OxfordGoogle Scholar
  13. Cooper SM, Holekamp KE, Smale L (1999) A seasonal feast: long-term analysis of feeding behavior in the spotted hyaena Crocuta crocuta (Erxbelen). Afr J Ecol 1: 178–180Google Scholar
  14. Crusafont Pairó M, Hartenberger JL, Heintz E (1964) Un nouveau gisement de Mammifères fossiles d’âge villafranchien à La Puebla de Valverde (Province de Teruel, Espagne). C R Hebd Séances Acad Sci 258: 2869–2871Google Scholar
  15. Dockner M (2006) Comparisons of Crocuta crocuta crocuta and Crocuta crocuta spelaea through computer tomography. M.S. Dissertation, University of ViennaGoogle Scholar
  16. Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6: 178–190. doi:  10.1002/(SICI)1520-6505(1998)6:5<178::AID-EVAN5>3.0.CO;2-8 CrossRefGoogle Scholar
  17. Dunbar RIM (2003) The social brain: mind, language, and society in evolutionary perspective. Annu Rev Anthropol 32: 163–181. doi:  10.1146/annurev.anthro.32.061002.093158 CrossRefGoogle Scholar
  18. Dunbar RIM, Bever J (1998) Neocortex size predicts group size in carnivores and some insectivores. Ethology 104: 695–708. doi:  10.1111/j.1439-0310.1998.tb00103.x CrossRefGoogle Scholar
  19. Dunbar RIM, Shultz S (2007a) Understanding primate brain evolution. Phil Trans R Soc B 362: 649–658. doi:  10.1098/rstb.2006.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Dunbar RIM, Shultz S (2007b) Evolution in the social brain. Science 317: 1344–1347. doi:  10.1126/science.1145463 PubMedCrossRefGoogle Scholar
  21. Eloff FC (1964) On the predatory habits of lions and hyaenas. Koedoe 7: 105–112CrossRefGoogle Scholar
  22. Finarelli JA, Flynn JJ (2009) Brain-size evolution and sociality in Carnivora. Proc Natl Acad Sci USA 106: 345–349. doi:  10.1073/pnas.0901780106 CrossRefGoogle Scholar
  23. Gaudry A (1862–1867) Animaux Fossiles du Mont Leberon. F. Savy, Paris, pp 475Google Scholar
  24. Gautier F, Heintz E (1974) Le gisement villafranchien de La Puebla de Valverde (Province de Teruel, Espagne). Bull Mus Natl Hist Nat 36: 113–133Google Scholar
  25. Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41: 587–640. doi:  10.1111/j.1469-185X.1966.tb01624.x PubMedCrossRefGoogle Scholar
  26. Gould SJ (1975) Allometry in primates, with emphasis on scaling and the evolution of the brain. Contrib Primatol 5: 244–292PubMedGoogle Scholar
  27. Holekamp KE, Sakai ST, Lundrigan BL (2007a) Social intelligence in the spotted hyena (Crocuta crocuta). Phil Trans R Soc Lond B 362: 523–538. doi:  10.1098/rstb.2006.1993 CrossRefGoogle Scholar
  28. Holekamp KE, Sakai ST, Lundrigan BL (2007b) The spotted hyena (Crocuta crocuta) as a model system for study of the evolution of intelligence. J Mammal 88: 545–554. doi:  10.1644/06-MAMM-S-361R1.1 CrossRefGoogle Scholar
  29. Howell FG, Petter G (1980) The Pachycrocuta and Hyaena lineages (Plio-Pleistocene and extant species of the Hyaenidae). Their relationships with Miocene ictitheres: Palhyaena and Hyaenictitherium. Geobios 13: 579–623. doi: 10.1016/S0016-6995(80)80004-0CrossRefGoogle Scholar
  30. Jerison HJ (1973) Evolution of the Brain and Intelligence. Academic Press, New YorkGoogle Scholar
  31. Jiménez García S, Martín de Jesús S, Jiménez Fuentes E (1999) Primeros resultados de la excavación “Villarroya 88-89”. Stvdia Geológica Salmanticensia 35: 41–56Google Scholar
  32. Joeckel RM (1998) Unique frontal sinuses in fossil and living Hyaenidae (Mammalia, Carnivora): description and interpretation. J Vertebr Paleontol 18: 627–639. doi:  10.1080/02724634.1998.10011089 CrossRefGoogle Scholar
  33. Klingenberg CP (1998) Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73: 79–123. doi:  10.1111/j.1469-185X.1997.tb00026.x PubMedCrossRefGoogle Scholar
  34. Kruuk H (1972) The Spotted Hyena: Study of Predation and Social Behavior. Chicago University Press, ChicagoGoogle Scholar
  35. Kruuk H (1976) Feeding and social behavior of the striped hyaena (Hyaena hyaena Desmarest). E Afr Wildl J 4: 91–111CrossRefGoogle Scholar
  36. Kurtén B (1968) Pleistocene Mammals of Europe. Weidenfeld and Nicolson, LondonGoogle Scholar
  37. Martin RD, Barbour AD (1989) Aspects of line-fitting in bivariate allometric analyses. Folia Primatol 53: 65–41. doi:  10.1159/000156409 PubMedCrossRefGoogle Scholar
  38. Mills MGL (1990) Kalahari Hyaenas: The Comparative Behavioral Ecology of Two Species. Unwin Hyman, LondonGoogle Scholar
  39. Palmqvist P, Martínez-Navarro B, Pérez-Claros JA, Torregrosa V, Figueirido B (2011) The giant hyena Pachycrocuta brevirostris: modelling the bone-cracking behavior of an extinct carnivore. Quaternary Internatl 243: 61–79. doi:  10.1016/j.quaint.2010.12.035 CrossRefGoogle Scholar
  40. Paulli S (1900) Über die Pneumaticität des Schädels bei den Säugethieren. III. Über die Morphologie des Siebbeins und die der Pneumaticität bei den Insectivoren, Hyracoideen, Chiroptera, Carnivoren, Pinnipedien, Edentaten, Prosimiern und Primaten. Gegenbaurs Morphol Jahrb 28: 483–564Google Scholar
  41. Pérez-Barbería FJ, Shultz S, Dunbar RIM (2007) Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61: 2811–2821. doi:  10.1111/j.1558-5646.2007.00229.x PubMedCrossRefGoogle Scholar
  42. Pilgrim GE (1932) The fossil Carnivora of India. Paleontol Indica 18: 1–232Google Scholar
  43. Radinsky L (1971) An example of parallelism in carnivore brain evolution. Evolution 25: 518–522CrossRefGoogle Scholar
  44. Radinsky L (1975) Evolution of the felid brain. Brain Behav Evol 11: 214–253. doi:  10.1159/000123636 PubMedCrossRefGoogle Scholar
  45. Radinsky L (1977) Brains of early carnivores. Paleobiology 3: 333–349Google Scholar
  46. Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011) Brain size and social complexity: a computed tomography study in Hyaenidae. Brain Behav Evol 77: 91–104. doi:  10.1159/000323849 PubMedCrossRefGoogle Scholar
  47. Schlosser M (1890) Die Aven, Lemuren, Chiropteren, Insectivoren, Marsupialier, Creodonten und Carnivoren des europäischen Tertiärs. III. Beitr Paläontol Geol Osterr Ung 8: 1–107Google Scholar
  48. Shultz S, Dunbar R (2010) Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc Natl Acad Sci USA 107: 21582–21586. doi:  10.1073/pnas.1005246107 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Sinusía C, Pueyo EL, Azanza B, Pocoví A (2004) Datación magnetoestratigráfica del yacimiento paleontológico de Puebla de Valverde (Teruel). GeoTemas 6: 339–342Google Scholar
  50. Smith RJ (1984) Determination of relative size: the “criterion of subtraction” problem in allometry. J Theor Biol 108: 131–142. doi:  10.1016/S0022-5193(84)80174-5 PubMedCrossRefGoogle Scholar
  51. Swanson EM, Holekamp KE, Lundrigan BL, Arsznov BM, Sakai ST (2012) Multiple determinants of whole and regional brain volume among terrestrial carnivorans. PLoS ONE 7: e38447. doi:  10.1371/journal.pone.0038447 PubMedCentralPubMedCrossRefGoogle Scholar
  52. Tanner JB, Dumont ER, Sakai ST, Lundrigan BL, Holejamp KE (2008) Of arcs and vaults: the biomechanics of bone-cracking in spotted hyenas (Crocuta crocuta). Biol J Linn Soc 95: 246–255. doi:  10.1111/j.1095-8312.2008.01052.x CrossRefGoogle Scholar
  53. Thenius E (1966) Zur Stammegeschichte der Hyänen (Carnivora, Mammalia). Z Säugetierk 31: 293–300Google Scholar
  54. Tilson RL, Henschel JR (1986) Spatial arrangement of spotted hyaena groups in a desert envoiroment, Namibia. Afr J Ecol 4: 173–180CrossRefGoogle Scholar
  55. Tseng ZJ, Antón M, Salesa MJ (2011) The evolution of the bone-cracking model in carnivorans: cranial functional morphology of the Plio-Pleistocene cursorial hyaenid Chasmaporthetes lunensis (Mammalia: Carnivora). Paleobiology 37: 140–156. doi:  10.1666/09045.1 CrossRefGoogle Scholar
  56. Turner A, Antón M (1996) The giant hyaena Pachycrocuta brevirostris (Mammalia, Carnivora, Hyaenidae). Geobios 29: 455–468. doi:  10.1016/S0016-6995(96)80005-2 CrossRefGoogle Scholar
  57. Turner A, Antón M, Werdelin L (2008) Taxonomy and evolutionary patterns in the fossil Hyaenidae of Europe. Geobios 41: 677–687. doi:  10.1016/j.geobios.2008.01.001 CrossRefGoogle Scholar
  58. Van Valkenburgh B (1990) Skeletal and dental prefictors of body mass in carnivores. In: Damuth J, MacFadden B (eds) Body Size in Mammalian Paleobiology: Estimation and Biological Implications. Cambridge University Press, Cambridge, pp 181–205Google Scholar
  59. Van Valkenburgh B, Sacco T, Wang X (2003) Pack hunting in Miocene borophagine dogs: evidence from craniodental morphology and body size. Bull Am Mus Nat His 13: 147–162Google Scholar
  60. Vinuesa V, Madurell-Malapeira J, Ansón M, Alba DM (2014) New cranial remains of Pliocrocuta perrieri (Carnivora, Hyaenidae) from the Villafranchian of the Iberian Peninsula. Boll Soc Paleont Ital 53: 39–47Google Scholar
  61. Wagner AP (2006) Behavioral ecology of the striped hyaena (Hyaena hyaena). Ph.D. Dissertation, Montana State UniversityGoogle Scholar
  62. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81: 259–291. doi:  10.1017/S1464793106007007 PubMedCrossRefGoogle Scholar
  63. Werdelin L (1989) Constraint and adaption in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15: 387–401Google Scholar
  64. Werdelin L, Solounias N (1991) The Hyaenidae: taxonomy, systematics and evolution. Fossils Strata 30: 1–104Google Scholar
  65. Werdelin L, Solounias N (1996) The evolutionary history of hyenas in Europe and western Asia during the Miocene. In: Bernor RL, Fahlbusch R, Mittmann HW (eds) The Evolution of Western Eurasian Neogene Mammal Faunas. Columbia University Press, New York, pp 290–306Google Scholar
  66. Werdelin L, Turner A (1996a) The fossil and living Hyaenidae of Africa: present status. In: Stewart KM, Seymour KL (eds) Palaeoecology and Palaeoenvironments of Late Cenozoic Mammals. University of Toronto Press, Toronto, pp 637–659Google Scholar
  67. Werdelin L, Turner A (1996b) Turnover in the guild of larger carnivores in Eurasia across the Miocene–Pliocene boundary. Acta Zool Crac 39: 585–592Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Víctor Vinuesa
    • 1
  • Joan Madurell-Malapeira
    • 1
    • 2
  • Josep Fortuny
    • 1
  • David M. Alba
    • 1
  1. 1.Institut Català de Paleontologia Miquel CrusafontUniversitat Autònoma de BarcelonaBarcelonaSpain
  2. 2.Dipartimento di Scienze della TerraSapienza Università di RomaRomaItaly

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