Were ancient foxes far more carnivorous than recent ones?—Carnassial morphological evidence

Autoři: Elwira Szuma aff001;  Mietje Germonpré aff002
Působiště autorů: Mammal Research Institute Polish Academy of Sciences, Białowieża, Poland aff001;  Operational Direction “Earth and History of Life”, Royal Belgian Institute of Natural Sciences, Brussels, Belgium aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227001


Crown shape variation of the first lower molar in the arctic (Vulpes lagopus) and red foxes (Vulpes vulpes) was analyzed using five groups of morphotypes. Carnassial morphologies were compared between the species and between spatially and temporally distant populations: one Late Pleistocene (n = 45) and seven modern populations of the arctic fox (n = 259), and one Late Pleistocene (n = 35) and eight modern populations of the red fox (n = 606). The dentition of Holocene red foxes had larger morphotype variability than that of arctic foxes. The lower carnassials of the red fox kept have some primitive characters (additional cusps and stylids, complex shape of transverse cristid), whereas the first lower molars of the arctic fox have undergone crown shape simplification, with the occlusal part of the tooth undergoing a more pronounced adaptation to a more carnivorous diet. From the Late Pleistocene of Belgium to the present days, the arctic fox’s crown shape has been simplified and some primitive characters have disappeared. In the red fox chronological changes in the morphology of the lower carnassials were not clearly identified. The phyletic tree based on morphotype carnassial characteristics indicated the distinctiveness of both foxes: in the arctic fox line, the ancient population from Belgium and recent Greenland made separate branches, whereas in the red foxes the ancient population from Belgium was most similar to modern red foxes from Belgium and Italy.

Klíčová slova:

Belgium – Dentition – Foxes – Mammals – Molars – Paleobiology – Pleistocene epoch – Teeth


1. Binder WJ, Van Valkenburgh B. Development of bite strength and feeding behavior in juvenile spotted hyenas (Crocuta crocuta). J Zool Lond. 2000;252:273–283.

2. Evans AR, Sanson GD. The tooth of perfection: functional and spatial constraints on mammalian tooth shape. Biol J Linn Soc. 2003;78:173–191.

3. Meloro C, Raia P, Piras P, Barbera C, O’Higgins P. The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zool J Linn Soc. 2008;154:832–845.

4. Polly D. Development and phenotypic correlations: the evolution of tooth shape in Sorex araneus. Evol Dev. 2005;7:29–41. doi: 10.1111/j.1525-142X.2005.05004.x 15642087

5. White J. Geometric morphometric investigation of molar shape diversity in modern lemurs and lorises. Anat Rec. 2009;292:701–719.

6. Smits PD, Evans AR. Functional constraints on tooth morphology in carnivorous mammals. BMC Evol Biol. 2012;12:146. doi: 10.1186/1471-2148-12-146 22899809

7. Tarquini SD, Chemisquy MA, Prevosti FJ. Evolution of carnassial in living mammalian Carnivores (Carnivora, Didelphimorphia, Dasyuromorphia): diet, phylogeny, and allometry. J Mamm Evol. 2018, Aug 23. doi: 10.1007/s10914-018-9448-7

8. Nadachowski A. Late Quaternary rodents of Poland, with special reference to morphotype dentition analysis of voles. Warszawa: Państwowe Wydawnictwo Naukowe; 1982.

9. Pozdnyakov AA. Morphotypic variation in molar masticatory surface pattern in gray voles of the “maximowiczi” group (Rodentia, Arvicolidae): Experience in quantitative statistical analysis. Zool Zh. 1993;72:114–125.

10. Markova EA. Assessment of tooth complexity in Arvicolines (Rodentia). A morphotype ranking approach. Biol Bull. 2014;41:589–600.

11. Szuma E. Dental polymorphism in a population of the red fox (Vulpes vulpes) from Poland. J Zool, Lond. 2002;256:243–253.

12. Szuma E. Evolutionary implications of morphological variation in the lower carnassial of red fox Vulpes vulpes. Acta Theriol. 2004;49:433–447.

13. Szuma E. Geography of dental polymorphism in the red fox Vulpes vulpes and its evolutionary implications. J Zool, Lond. 2007;90:61–84.

14. Gimranov DO. Species diagnostics of the corsac (Vulpes corsac), fox (Vulpes vulpes) and arctic fox (Vulpes lagopus, Carnivora, Canidae) using the upper teeth. Zool Zh. 2017;96:684–697.

15. Gimranov DO, Kosintsev PA, Gasilin VV. Species diagnostic of corsac (Vulpes corsac), fox (Vulpes vulpes), and arctic fox (Vulpes lagopus) according to ontological characteristics of mandible teeth. Zool Zh. 2015;94:1338–1350.

16. Szuma E. Ecological and evolutionary determinants of dental polymorphism in the arctic fox Vulpes (Alopex) lagopus. Ann Zool Fenn. 2011;48:191–213.

17. Korablev NP, Szuma E, Korablev PN, Zinoviev AV. Dental polymorphism of the raccoon dog in indigenous and invasive populations: internal and external causation. Mamm Res. 2017;62:163–177. doi: 10.1007/s13364-016-0293-x

18. Wolsan M. Dental polymorphism in the genus Martes (Carnivora: Mustelidae) and its evolutionary significance. Acta Theriol. 1989;34:545–593.

19. Gimranov DO, Kosintsev PA. Differentiation of three Martes species (M. martes, M. zibellina, M. foina) by tooth morphotypes. CR Palevol. 2015;14:647–656.

20. Baryshnikov GF, Potapova OR. Variability of the dental system in badgers (Meles, Carnivora) of the USSR fauna. Zool Zh. 1990;69:84–97. Russian.

21. Szuma E. Quasi-continuous variation of the first premolars in the Polish population of the badger Meles meles. Acta Theriol. 1994;39:201–208.

22. Gimranov DO. Morphotypic characteristics of the fourth premolars of the brown (Ursus arctos) and polar (Ursus maritimus) bears (Carnivora, Ursidae). Zool Zh. 2018;97:205–223.

23. Serdyuk VA. Variability of teeth structure in Citellus parryi rich. and possible ways of migration of this species in the north-east of USSR. Zool Zh. 1979;58:1692–1702.

24. Suchentrunk F. Epigenetic dental asymmetry of Israeli hares: Developmental stability along an environmental gradient. Isr J Zool. 2000;46:103–118.

25. Suchentrunk F. Phylogenetic relationships between Indian and Burmese hares (Lepus nigricollis and L. peguensis) inferred from epigenetic dental characters. Mamm Biol. 2004;69:28–45.

26. Suchentrunk F, Flux JEC. Minor dental traits in East African cape hares and savanna hares (Lepus capensis and Lepus victoriae): A study of intra- and interspecific variability. J Zool, Lond. 1996;238:495–511.

27. Suchentrunk F, Willing R, Hartl GB. Nonmetrical polymorphism of the first lower premolar (P-3) in Austrian brown hares (Lepus europaeus)–a study on regional differentiation. J Zool, Lond. 1994;232:79–91.

28. Maleeva AG. Evolutsiya gryzunov i istoriya formirovaniya ikh sovremennoy fauny. In: Sbornik nauchnykh trudov, Leningrad 1976:48–57. Russian.

29. Markova EA, Borodin AV, Gileva EA. Odontological features in Microtus arvalis s.str. and M. rossiaemeridionalis from the Ural region and their taxonomic value. Zool Zh. 2003;82:1086–1094.

30. Markova EA, Malygin V, Montuire S, Nadachowski A, Quéré J-P, Ochman K. Dental Variation in sibling species Microtus arvalis and M. rossiaemeridionalis (Arvicolinae, Rodentia): Between-species comparisons and geography of morphotype dental patterns. J Mam Evol. 2010;17:121–139.

31. Nadachowski A. Systematic, geographic variation and evolution of snow voles (Chionomys) based on dental characters. Acta Theriol. 1991;36:1–45.

32. Pozdnyakov AA. The structure of morphological variability of common voles (Microtus: Rodentia, Arvicolidae) in the light of epigenetic theory of evolution. Usp sovrem biol. 2007;127:416–424.

33. Berthaume MA, Schroer K. Extant ape dental topography and its implications for reconstructing the emergence of early Homo. J Hum Evol. 2017;112:15–29. doi: 10.1016/j.jhevol.2017.09.001 29037413

34. Ercoli MD, Candela AM, Rasia LL, Ramírez MA. Dental shape variation of Neogene Pachyrukhinae (Mammalia, Notoungulata, Hegetotheriidae): systematics and evolutionary implications for the late Miocene Paedotherium species. J Syst Paleontol. 2018;16:1073–1095.

35. Gomez Cano AR, Kimura Y, Blanco F, Menéndez I, Álvarez-Sierra MA, Fernández MH. Ecomorphological characterization of murines and non-arvicoline cricetids (Rodentia) from south-western Europe since the latest Middle Miocene to the Mio-Pliocene boundary (MN 7/8_MN13). PeerJ 2017;5:e3646. doi: 10.7717/peerj.3646 28966888

36. Zazhigin VS, Voyta LL. A new middle Miocene crocidosoricine shrew from the Mongolian Shargain Gobi Desert. Acta Palaeontol Pol. 2018;63:171–187.

37. Szuma E. Microevolutionary trends in the dentition of the red fox (Vulpes vulpes). J Zool Syst Evol Res. 2003;41:47–56.

38. Kay RF. Molar structure and diet in extant Cercopithecidae. In: Butler PM, Joysey KA (eds) Development, function and evolution of teeth. New York: Academic Press; 1978.

39. Strait SG. Molar morphology and food texture among small-bodied insectivorous mammals. J Mammal. 1993;74:391–402.

40. Yom-Tov Y, Yom-Tov S, Baagøe HJ. Increase of skull size in the red fox (Vulpes vulpes) and Eurasian badger (Meles meles) in Denmark during the 20th century: an effect of improved diet? Evol Ecol Res. 2003;5:1037–1048.

41. Yom-Tov Y, Yom-Tov S, Zachos FE. Temporal and geographical variation in skull size of the red fox (Vulpes vulpes) and the Eurasian badger (Meles meles) in Austria. J Linn Soc, Lond. 2013;108:579–585.

42. Otte M, Baden-Powell D. Le Magdalénien du Trou de Chaleux (Hulsonniaux-Belgique). ERAUL 1994;60:241–253.

43. Dupont E. L’homme pendant les âges de la pierre dans les environs de Dinant-sur-Meuse. 2nd ed. Bruxelles: C Muquardt; 1873.

44. Germonpré M, Sablin MV. Systematics and osteometry of Late Glacial foxes from Belgium. Bull Inst r sci nat Belg. 2004;74:175–188.

45. Germonpré M. A reconstruction of the spatial distribution of the faunal remains from Goyet, Belgium. Notae praehistoricae. 2001;21:57–65.

46. Posth C, Renaud G, Mittnik A, Drucker D, Rougier H, Cupillard Ch, et al. Pleistocene mitochondrial genomes suggest a single major dispersal of Non-Africans and Late Glacial Population turnover in Europe. Curr Biol. 2016;26:827–833. doi: 10.1016/j.cub.2016.01.037 26853362

47. Rougier H, Crevecoeur I, Beauval C, Posth C, Flas D, Wiẞing Ch, et al. Neandertal canibalism and Neandertal bones used as tools in Northern Europe. Sci Rep. 2016;6:29005. doi: 10.1038/srep29005 27381450

48. Germonpré M. Preliminary results on the mammals of the Magdalenian upper horizon of Goyet (Belgium). Notae Praehistoricae. 1996;16:75–85.

49. Charles R. Late Magdalenian chronology and faunal exploitation in the North-Western Ardennes. In: BAR Int Ser. 1998;737:1–246.

50. Germonpré M, Sablin MV, Stevens RE, Hedges REM, Hofreiter M, Stiller M, et al. Fossil dogs and wolves from Paleolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J Archaeol Sci. 2009;36:473–490.

51. Otte M. Le paléolithique supérieur ancien en Belgique. Monographies d’Archéologie Nationale 5. Bruxelles: Musées Royaux d’art et d’histoire; 1979.

52. Jimenez E-L. Palaeoecology and subsistence strategies in Belgium and Northwestern Europe during the MIS 3 through the reassessment of forgotten collections: A methodological approach. PIA 2016;26(1):Art.3. doi: 10.5334/pia-486

53. Jimenez E-L, Smolderen A, Jadin I, Germonpré M. Exhumation de la collection faunique d’Édouard Dupont provenant du Trou Magrite (Pont-à-Lesse) Quelles données et quelles perspectives pour une collection do XIXe siècle? Notae Praehistoricae 2016;36:167–190. Franch.

54. Jimenez E-L. Modalités d’occupation du territoire et relations humains-grands carnivores durant le Pléistocène supérieur. Approche archéozoologique, taphonomique et paléoécologique du Bassin mosan belge dans son contexte nord-ouest européen. [dissertation], Histoire de l’art et Archéologie, Université Libre de Bruxelles; 2017. Franch.

55. Szuma E. Geographic variation of tooth and skull sizes in the arctic fox Vulpes (Alopex) lagopus. Ann Zool Fenn. 2008;45:185–199.

56. Szuma E. Evolutionary and climatic factors affecting tooth size in the red fox Vulpes vulpes in the Holarctic. Acta Theriol. 2008;53:289–332.

57. Szuma E. Variation and correlation patterns in the dentition of the red fox from Poland. Ann Zool Fenn. 2000;37:113–127.

58. Gilbert N. Biometrical interpretation. Making sense of statistics in Biology. 2nd ed. Oxford, New York: Oxford University Press; 1989.

59. Bonis de L, Peigné S, Likius A, Mackaye HT, Vignaud P, Brunet M. The oldest African fox (Vulpes riffautae n. sp., Canidae, Carnivora) recovered in the late Miocene deposits of the Djurab desert, Chad. Naturwissenschaften. 2007;94:575–580. doi: 10.1007/s00114-007-0230-6 17361401

60. Wang X, Tseng ZJ, Li Q, Takeuchi GT, Xie G. From ‘third pole’ to north pole: a Himalayan origin for the arctic fox. Proc Royal Soc. B 2014, Jul 22. 281(1787). doi: 10.1098/rspb.2014.0893 24920475

61. Deng T, Wang X, Wu F, Wang Y, Li Q, Wang S, et al. Review: implications of vertebrate fossils for paleo-elevations of the Tibetan Plateau. Glob Planet Change. 2019;174:58–69.

62. Szuma E, Germonpré M. Size of the lower carnassial in the arctic and the red fox from Late Pleistocene in Belgium compared to other ancient and extant populations. Mammal Res. doi: 10.1007/s13364-019-00459-w

63. Deng T, Wang XM, Fortelius M, Li Q, Wang Y, Tseng ZJ, et al. Out of Tibet: Pliocene woolly rhino suggests highplateau origin of Ice Age megaherbivores. Science. 2011;333:1285–1288. doi: 10.1126/science.1206594 21885780

64. Elmhagen B, Rushton SP. Trophic control of mesopredators in terrestrial ecosystems: top-down or bottom-up? Ecol Lett. 2007;10:197–206. doi: 10.1111/j.1461-0248.2006.01010.x 17305803

65. Selås V, Vik JO. Possible impact of snow depth and ungulate carcasses on red fox (Vulpes vulpes) populations in Norway, 1897–1976. J Zool. 2006;268:299–308.

66. Hersteinsson P, Macdonald DW. Interspecific competition and the geographical-distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus. Oikos. 1990;64:505–515.

67. Roff DA, Stirling G, Fairbairn DJ. The evolution of threshold traits: A quantitative genetic analysis of the physiological and life-history correlates of wing dimorphism in the sand cricket. Evolution. 1997;51:1910–1919. doi: 10.1111/j.1558-5646.1997.tb05113.x 28565097

68. Wang X, Tedford RH. Dogs. Their fossil relatives abd evolutionary history. New York: Columbia University Press; 2010.

69. Qiu Z, Tedford RH. A Pliocene species of Vulpes from Yushe, Shanxi. Vertebrat PalAsiatic. 1990;10:245–258.

70. Szuma E. Microevolutionary trends in the dentition of the Red fox (Vulpes vulpes). J Zool Syst Evol Res. 2002,40:1–10.

71. Dalén L, Nyström V, Valdiosera C, Germonpré M, Sablin M, Turner E, et al. Ancient DNA reveals lack of postglacial habitat tracking in the arctic fox. PNAS. 2007;104:6726–6729. doi: 10.1073/pnas.0701341104 17420452

72. Flower LDH. New body mass estimates of British Pleistocene wolves: Palaeoenvironmental implications and competitive interactions. Quat Sci Rev. 2016;149:230–247

73. Meiri S, Dayan T, Simberloff D. Carnivores, biases and Bergmann’s rule. Biol J Linn Soc. 2004;81:579–588.

Článek vyšel v časopise


2020 Číslo 1