Advertisement

Journal of Mammalian Evolution

, Volume 24, Issue 4, pp 495–503 | Cite as

Variations in Microtus arvalis and Microtus agrestis (Arvicolinae, Rodentia) Dental Morphologies in an Archaeological Context: the Case of Teixoneres Cave (Late Pleistocene, North-Eastern Iberia)

  • Elisa LuziEmail author
  • Juan Manuel López-García
  • Ruth Blasco
  • Florent Rivals
  • Jordi Rosell
Original Paper

Abstract

Morphological and morphometric variations in the first lower molars of Microtus arvalis and Microtus agrestis from the late Pleistocene site of Teixoneres Cave (Barcelona, Spain) have been investigated in order to understand the modifications in dental patterns occurring in these two species in a peripheral region of their distribution area. It was possible to identify along the sequence differences in size and frequencies of morphotypes within the two populations, corresponding to environmental and climatic oscillations. Hypotheses to explain these intraspecific changes are discussed, and the variations are ascribed primarily to small-scale intraregional movements of these two rodent populations.

Keywords

Microtus arvalis Microtus agrestis Morphology Intraspecific Variation Late Pleistocene 

Notes

Acknowledgments

The authors want to thank Rupert Glasgow for the revision of the English and the reviewers for their valuable comments. E. Luzi is a beneficiary of a PhD scholarship funded under the Erasmus Mundus Program – International Doctorate in Quaternary and Prehistory. The research at Toll-Teixoneres Caves is supported by projects 2014/100573 and 2014 SGR 900 from the Generalitat de Catalunya; project 19434/PI/14 from the SéNeCa Foundation; and projects HAR2013-48784-C3-1-P, CGL2012-38434-C03-03, CGLBOS-2012-34717 and HAR2010-18952-C02-01 from the Spanish Ministry of Economy and Competitiveness (MINECO).

References

  1. Berto C, Bertè D, Luzi E, Lopez-Garcia JM, Pereswiet-Soltan A, Arzarello M (2016) Small and large mammals from Ciota Ciara cave (Borgosesia, Vercelli, Italy): an Isotope Stage 5 assemblage. Palevol 15:669–680CrossRefGoogle Scholar
  2. Borodin AV, Markova EA (2015) Keys to identify modern and Pleistocene arvicolines (Arvicolinae, Rodentia) from the Urals and western Siberia based on odontological characteristics. Biol Bull 42:652–663CrossRefGoogle Scholar
  3. Bužan EV, Kryštufek B, Hänfling B, Hutchinson WF (2008) Mitochondrial phylogeny of Arvicolinae using comprehensive taxonomic sampling yields new insights. Biol J Linn Soc 94:825–835CrossRefGoogle Scholar
  4. Chaline J (1972) Les Rongeurs du Pléistocène Moyen et Supérieur de France. CNRS, ParisGoogle Scholar
  5. Cucchi T, Barnett R, Martínková N, Renaud S, Renvoisé E, Evin A, Sheridan A, Mainland I, Wickham-Jones C, Tougard C, Quéré JP, Pascal M, Pascal M, Heckel G, O’Higgins P, Searle JB, Dobney KM (2014) The changing pace of insular life: 5000 years of microevolution in the Orkney vole (Microtus arvalis orcadensis). Evolution 68:2804–2820CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cuenca-Bescós G, Laplana C (1995) Evolución de Iberomys (Arvicolidae, Rodentia, Mammalia) durante el Cuaternario español. In: López G, Obrador A, Vicens E (eds) XI Jornadas de Paleontología. Sociedad Española de Paleontología, Tremp, Lérida, pp 69–72Google Scholar
  7. Cuenca-Bescós G, Rofes J, López-García JM, Blain HA, De Marfá R, Galindo-Pellicena MA, Bennásar-Serra ML, Melero-Rubio M, Arsuaga JL, de Castro Bermúdez JM, Carbonell E (2010) Biochronology of Spanish Quaternary small vertebrate faunas. Quaternary Internatl 212:109–119CrossRefGoogle Scholar
  8. De Jonge G (1983) Aggression and group formation in the voles Microtus agrestis, M. arvalis and Clethrionomys glareolus in relation to intra- and interspecific competition. Behaviour 84:1–73.CrossRefGoogle Scholar
  9. Dienske H (1979) The importance of social interactions and habitat in competition between Microtus agrestis and M. arvalis. Behaviour 71:1–125CrossRefGoogle Scholar
  10. Gould SJ (1975) On the scaling of tooth size in mammals. Am Zool 15:351–362.CrossRefGoogle Scholar
  11. Hammer Ø, Harper DAT (2006) Paleontological Data Analysis. Blackwell, OxfordGoogle Scholar
  12. Haynes S, Jaarola M, Searle JB (2003) Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago. Mol Ecol 12:951–956CrossRefPubMedGoogle Scholar
  13. Heller F (1936) Eine oberpliozane Wirbeltierfauna aus Rheinhessen. Neues Jb Miner Geol Paleontol 76:99–160Google Scholar
  14. Hernández Fernández M, Peláez-Campomanes P (2005) Quantitative palaeoclimatic inference based on terrestrial mammal faunas. Glob Ecol Biogeogr 14:39–56CrossRefGoogle Scholar
  15. IUCN (2015) The IUCN Red List of Threatened Species. Version 2015–4. www.iucnredlist.org
  16. Jaarola M, Martínková N, Gündüz I, Brunhoff C, Zima J, Nadachowski A, Amori G, Bulatova NS, Chondropoulos B, Fraguedakis-Tsolis S, González-Esteban J, José López-Fuster M, Kandaurov AS, Kefelioǧlu H, Da Luz Mathias M, Villate I, Searle JB (2004) Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 33:647–663CrossRefPubMedGoogle Scholar
  17. Jaarola M, Searle JB (2004) A highly divergent mitochondrial DNA lineage of Microtus agrestis in southern Europe. Heredity 92:228–234CrossRefPubMedGoogle Scholar
  18. Jaarola M, Searle JB (2008) Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol Ecol 11:2613–2621CrossRefGoogle Scholar
  19. Jernvall J (2000) Linking development with generation of novelty in mammalian teeth. Proc Natl Acad Sci U S A 97:2641–2645CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jernvall J, Thesleff I (2012) Tooth shape formation and tooth renewal: evolving with the same signals. Development 139:3487–3497CrossRefPubMedGoogle Scholar
  21. Kapischke H-J, Kraft R, Jentzsch M, Hiermeier M (2009) Variation and complexity of the enamel pattern in the first lower molar of the field vole, Microtus agrestis (L., 1761) (Mammalia: Rodentia: Arvicolinae). Vertebr Zool 59:191–195Google Scholar
  22. Kassai Y, Munne P, Hotta Y, Penttilä E, Kavanagh K, Ohbayashi N, Takada S, Thesleff I, Jernvall J, Itoh N (2005) Regulation of mammalian tooth cusp patterning by ectodin. Science 309:2067–2070CrossRefPubMedGoogle Scholar
  23. Kovalsky K (2001) Pleistocene Rodents of Europe. Polska Akademia Umiej tno ci, KrakówGoogle Scholar
  24. Laffont R, Renvoisé E, Navarro N, Alibert P, Montuire S (2009) Morphological modularity and assessment of developmental processes within the vole dental row (Microtus arvalis, Arvicolinae, Rodentia). Evol Dev 11:302–311CrossRefPubMedGoogle Scholar
  25. Ledevin R, Michaux JR, Deffontaine V, Henttonen H, Renaud S (2010a) Evolutionary history of the bank vole Myodes glareolus: a morphometric perspective. Biol J Linn Soc 100:681–694CrossRefGoogle Scholar
  26. Ledevin R, Quéré J-P, Renaud S (2010b) Morphometrics as an insight into processes beyond tooth shape variation in a bank vole population. PLoS One 5:e15470CrossRefPubMedPubMedCentralGoogle Scholar
  27. López-García JM, Blain HA, Burjachs F, Ballesteros A, Allué E, Cuevas-Ruiz GE, Rivals F, Blasco R, Morales JI, Hidalgo AR, Carbonell E, Serrat D, Rosell J (2012) A multidisciplinary approach to reconstructing the chronology and environment of southwestern European Neanderthals: the contribution of Teixoneres cave (Moià, Barcelona, Spain). Quaternary Sci Rev 43:33–44Google Scholar
  28. López-García JM, Dalla Valle C, Cremaschi M, Peresani M (2015) Reconstruction of the Neanderthal and modern human landscape and climate from the Fumane cave sequence (Verona, Italy) using small-mammal assemblages. Quaternary Sci Rev 128:1–13CrossRefGoogle Scholar
  29. Luque-Larena JJ, Mougeot F, Viñuela J, Jareño D, Arroyo L, Lambin X, Arroyo B (2013) Recent large-scale range expansion and outbreaks of the common vole (Microtus arvalis) in NW Spain. Basic Appl Ecol 14:432–441CrossRefGoogle Scholar
  30. Markova EA (2013) Assessment of tooth complexity in arvicolines (Rodentia): a morphotype-based ranking approach. Зоологический Журнал 92:968–980Google Scholar
  31. Markova EA, Malygin V, Montuire S, Nadachowski A, Quéré JP, Ochman K (2010) Dental variation in sibling species Microtus arvalis and M. rossiaemeridionalis (Arvicolinae, Rodentia): between-species comparisons and geography of morphotype dental patterns. J Mammal Evol 17:121–139CrossRefGoogle Scholar
  32. Markova EA, Smirnov NG, Kourova TP, Kropacheva YE (2013a) Ontogenetic variation in occlusal shape of evergrowing molars in voles: an intravital study in Microtus gregalis (Arvicolinae, Rodentia). Mammal Biol- Säugetierk 78:251–257Google Scholar
  33. Markova EA, Yalkovskaya LE, Zykov S V (2013b) Morphological and chromosomal variation in the common vole Microtus arvalis (pall.) at the northern boundary of its distribution area. Dokl Biol Sci 448:13–16CrossRefPubMedGoogle Scholar
  34. Nadachowski A (1982) Late Quaternary Rodents of Poland with Special Reference to Morphotype Dentition Analysis of Voles. P.W.N., Warszava - KrakowGoogle Scholar
  35. Nadachowski A (1984) Taxonomic value of anteroconid measurements of M1 in common and field voles. Acta Theriol 29:123–127CrossRefGoogle Scholar
  36. Paupério J (2012) Cryptic speciation in the field vole (Microtus agrestis): insights from genetic, karyotypic and morphometric data. PhD dissertation, Departamento de Biologia Faculdade de Ciências, Universidade do Porto, PortugalGoogle Scholar
  37. Paupério J, Herman JS, Melo-Ferreira J, Jaarola M, Alves PC, Searle JB (2012) Cryptic speciation in the field vole: a multilocus approach confirms three highly divergent lineages in Eurasia. Mol Ecol 21:6015–6032CrossRefPubMedGoogle Scholar
  38. Polly PD, Killick L, Ruddy M (2011) Using left-right asymmetry to estimate non-genetic variation in vole teeth ( Arvicolinae, Muridae, Rodentia ). Palaeontol Electron 14:41 A.Google Scholar
  39. Rekovets L, Nadachowski A (1995) Pleistocene voles (Arvicolidae) of the Ukraine. Paleontol i Evol 28–29:145–245Google Scholar
  40. Renaud S, Pantalacci S, Quéré JP, Laudet V, Auffray JC (2009) Developmental constraints revealed by co-variation within and among molar rows in two murine rodents. Evol Dev 11:590–602CrossRefPubMedGoogle Scholar
  41. Renvoisé E, Montuire S, Richard Y, Quéré JP, Gerber S, Cucchi T, Chateau-Smith C, Tougard C (2012) Microevolutionary relationships between phylogeographical history, climate change and morphological variability in the common vole (Microtus arvalis) across France. J Biogeogr 39:698–712CrossRefGoogle Scholar
  42. Robovský J, Řičánková V, Zrzavý J (2008) Phylogeny of Arvicolinae (Mammalia, Cricetidae): utility of morphological and molecular data sets in a recently radiating clade. Zool Scr 37:571–590CrossRefGoogle Scholar
  43. Rofes J, Garcia-Ibaibarriaga N, Aguirre M, Martínez-García B, Ortega L, Zuluaga MC, Bailon S, Alonso-Olazabal A, Castaños J, Murelaga X (2015) Combining small-vertebrate, marine and stable-isotope data to reconstruct past environments. Sci Rep 5:14219CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rosell J, Blasco R, Cebrià A, Chacón MG, Menéndez L, Morales JI, Rodríguez-Hidalgo A (2008) Mossegades i Levallois: les noves intervencions a la Cova de les Teixoneres (Moià, Bages). Trib d’Arqueologia 29–43Google Scholar
  45. Rosell J, Blasco R, Rivals F, Chacón MG, Arilla M, Camarós E, Rufà A, Sánchez-Hernández C, Picin A, Andrés M, Blain HA, López-García JM, Iriarte E, Cebrià A (2016) A resilient landscape at Teixoneres Cave (MIS 3; Moià, Barcelona, Spain): the Neanderthals as disrupting agent. Quataternary Internatl doi: 10.1016/j.quaint.2015.11.077 Google Scholar
  46. Rosell J, Blasco R, Rivals F, Chacón MG, Menéndez L, Morales JI, Rodríguez-Hidalgo A, Cebria A, Carbonell E, Serrat D (2010) A stop along the way: the role of Neanderthal groups at level III of Teixoneres cave (Moia, Barcelona, Spain). Quaternaire 21:139–154.CrossRefGoogle Scholar
  47. Royer A, Montuire S, Legendre S, Discamps E, Jeannet M, Lécuyer C (2016) Investigating the influence of climate changes on rodent communities at a regional scale (MIS 1-3, southwestern France). PLoS One 11:e0145600CrossRefPubMedPubMedCentralGoogle Scholar
  48. Sala B, Masini F (2007) Late Pliocene and Pleistocene small mammal chronology in the Italian peninsula. Quataternary Internatl 160:4–16. doi: 10.1016/j.quaint.2006.10.002 CrossRefGoogle Scholar
  49. Sánchez-Hernández C, Rivals F, Blasco R, Rosell J (2014) Short, but repeated Neanderthal visits to Teixoneres cave (MIS 3, Barcelona, Spain): a combined analysis of tooth microwear patterns and seasonality. J Archaeol Sci 49:317–325CrossRefGoogle Scholar
  50. Stohl G (1984) Über einige Besonderheiten „künstlicher" Feldmaus-Populationen (Microtus arvalis [ Pallas ] ) (Mammalia, Rodentia). Vertebr Hungarica XXII:51–63.Google Scholar
  51. Talamo S, Blasco R, Rivals F, Picin A, Chacón MG, Iriarte E, López-García JM, Blain H-A, Arilla M, Rufà A, Sánchez-Hernández C, Andrés M, Camarós E, Ballesteros A, Cebrià A, Rosell J, Hublin J-J (2016) The radiocarbon approach to Neanderthals in a carnivore den site: a well-defined chronology for Teixoneres cave (Moià, Barcelona, Spain). Radiocarbon 58: 247–265CrossRefGoogle Scholar
  52. Tissoux H, Falguères C, Bahain JJ, Rossel I Ardèvol J, Cebrià A, Carbonell E, Serrat D (2006) Datation par les séries de l’Uranium des occupations Moustériennes de la grotte de Teixoneres (Moia, Province de Barcellone, Espagne). Quaternaire 17:27–33.CrossRefGoogle Scholar
  53. Tiunov MP, Kartavtseva IV, Lapin AS (2013) Morphotype analysis of the sibling vole (Microtus rossiaemeridionalis) casually introduced to the Russian Far East. Acta Theriol 58:79–82CrossRefPubMedGoogle Scholar
  54. Tougard C, Brunet-Lecomte P, Fabre M, Montuire S (2008) Evolutionary history of two allopatric Terricola species (Arvicolinae, Rodentia) from molecular, morphological, and palaeontological data. Biol J Linn Soc 93:309–323CrossRefGoogle Scholar
  55. Ungar PS (2010) Mammals Teeth. Origins, Evolution and Diversity. Johns Hopkins University Press, BaltimoreGoogle Scholar
  56. Van der Meulen AJ (1973) Middle Pleistocene smaller mammals from the Monte Peglia (Orvieto, Italy) with special reference to the phylogeny of Microtus. Quaternaria 17:1–144.Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Elisa Luzi
    • 1
    • 2
    Email author
  • Juan Manuel López-García
    • 1
  • Ruth Blasco
    • 3
  • Florent Rivals
    • 1
    • 2
    • 4
  • Jordi Rosell
    • 1
    • 2
  1. 1.IPHES, Institut Catala de Paleoecologia Humana i Evolucio SocialTarragonaSpain
  2. 2.Area de PrehistoriaUniversitat Rovira i Virgili (URV)TarragonaSpain
  3. 3.Centro Nacional de Investigación Sobre la Evolución Humana (CENIEH)BurgosSpain
  4. 4.ICREA, Institució Catalana de Recerca i Estudis AvançatsBarcelonaSpain

Personalised recommendations