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Cranial Biometrics of the Iberian Myotis myotis/Myotis blythii Complex: New Data for Studying the Fossil Record

  • Julia Galán
  • Carmen Núñez-Lahuerta
  • Víctor Sauqué
  • Gloria Cuenca-Bescós
  • Juan Manuel López-García
Original Paper

Abstract

The Myotis myotis/M. blythii species complex, spread across the Western Palearctic, is a problematic group for which the taxonomy of the species is not yet satisfactorily resolved. The Iberian Peninsula played a key role in its evolutionary history as a Pleistocene refuge and as the starting point for the eastward expansion of M. myotis in the early Holocene, while M. blythii reached the Iberian Peninsula only during the middle Holocene. The study of Iberian populations and particularly of the Iberian fossil record is of high interest in this regard. However, there are few data available on the biometry of the skulls and teeth of Iberian populations (which differ somewhat in size from those of other regions of Europe and Asia) or tools for the identification of fragmentary cranial remains. Much of the Quaternary Iberian record of large Myotis remains unassigned. Here, we contribute to the task of determining fragmentary cranial remains by providing new cranial and dental biometric data from extant Iberian populations, predictive models for isolated upper molar identification, and a set of indices that allow quantitative evaluation of the differences in anatomical traits (in skull and molars) between the two species.

Keywords

Sibling species Large mouse-eared bats Iberian Peninsula Classic morphometry 

Notes

Acknowledgements

We are very grateful to the curators of the Collection of the Estación Biológica de Doñana (EBD-CSIC) and the specialists in Chiroptera C. Ibáñez and J. Juste. We would like to acknowledge our colleague J. Esteve for his advice on data processing during the first stages of the study, and E. Ángel for his help with statistics. R. Glasgow corrected the English of the manuscript. The two anonymous referees have greatly improved the quality of the work with their comments. The projects MICICINN CGL2012-38434-C03-01, CGL2012-38434-C03-03, CGL2012-38358, CGL2015-65387-C3-2-P (MINECO/FEDER), and the institutions Junta de Castilla y León, Fundación Atapuerca and Grupos Consolidados del Gobierno de Aragón made this work possible. J. Galán and C. Núñez-Lahuerta are recipients of PhD grants from the Diputación General de Aragón (DGA), co-financed by the European Social Fund (FSE) of the European Union.

Supplementary material

10914_2018_9427_MOESM1_ESM.docx (28 kb)
List of specimens analyzed. MCNZ: Museo de Ciencias Naturales de Zaragoza; MCNM: Museo de Ciencias Naturales de Madrid; EDB-CSIC: Estación Biológica de Doñana-Consejo Superior de Investigaciones Científicas; N-Sp: Northern Spain; S-Sp: Southern Spain; C-Sp: Central Spain; Med-Sp: Mediterranean Spain; M: male; F: female. (DOCX 28 kb)

References

  1. Afonso E, Goydadin A-C, Giraudoux P, Farny G (2017) Investigating hybridization between the two sibling bat species Myotis myotis and M. blythii from guano in a natural mixed maternity colony. PLoS One 12(2):e0170534Google Scholar
  2. Arlettaz R (1995) Ecology of the sibling species Myotis myotis and Myotis blythii. Dissertation, University of LausanneGoogle Scholar
  3. Arlettaz R (1996) Feeding behaviour and foraging strategy of free-living mouse-eared bats, Myotis myotis and Myotis blythii. Anim Behav 51(1):1–11Google Scholar
  4. Arlettaz R (1999) Habitat selection as a major resource partitioning mechanism between the two sympatric sibling bat species Myotis myotis and Myotis blythii. J Anim Ecol 68(3):460–471Google Scholar
  5. Arlettaz R, Ruedi M, Ibáñez C, Palmeirim J, Hausser J (1997) A new perspective on the zoogeography of the sibling mouse-eared bat species Myotis myotis and Myotis blythii: morphological, genetical and ecological evidence. J Zool 242(1):45–62Google Scholar
  6. Bachanek J, Postawa T (2010) Morphological evidence for hybridization in the sister species Myotis myotis and Myotis oxygnathus (Chiroptera: Vespertilionidae) in the Carpathian Basin. Acta Chiropterol 12(2):439–448Google Scholar
  7. Benda P (1996) To the suitability of some cranial criteria for the determination of mouse-eared bats (Myotis myotis and Myotis blythii). Lynx 27:5–12Google Scholar
  8. Benda P, Horáček I (1995a) Biometrics of Myotis myotis and Myotis blythi. Myotis 32(33):45–55Google Scholar
  9. Benda P, Horáček I (1995b) Geographic variation in three species of Myotis (Mammalia: Chiroptera) in south of the western Palearctics. Acta Soc Zool Bohem 59(1–2):17–39Google Scholar
  10. Berthier P, Excoffier L, Ruedi M (2006) Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc R Soc Lond B Biol Sci 273(1605):3101–3123Google Scholar
  11. Bogan MA, Setzer HW, Findley JS, Wilson DE (1978) Phenetics of Myotis blythii in Morocco. In: Proceedings of the Fourth International Bat Research Conference, Nairobi, pp. 217–230Google Scholar
  12. Bogdanowicz W, Van Den Bussche RA, Gajewska M, Postawa T, Harutyunyan M (2009) Ancient and contemporary DNA sheds light on the history of mouse-eared bats in Europe and the Caucasus. Acta Chiropterol 11(2):289–305Google Scholar
  13. Castella V, Ruedi M, Excoffier L, Ibáñez C, Arlettaz R, Hausser J (2000) Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Mol Ecol 9(11):1761–1772Google Scholar
  14. Corbet GB (1978) The mammals of the Palaearctic region: a taxonomic review. British Museum (Natural History), LondonGoogle Scholar
  15. Cuenca-Bescós G, Straus LG, García-Pimienta JC, Morales MG, López-García JM (2010) Late Quaternary small mammal turnover in the Cantabrian region: the extinction of Pliomys lenki (Rodentia, Mammalia). Quaternary Internatl 212(2):129–136Google Scholar
  16. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J Roy Stat Soc Ser B (Meth) 39(1):1–38Google Scholar
  17. Dietz C, von Helversen O, Nill D (2009) L’encyclopédie des chauves-souris d’Europe et d’Afrique du Nord: biologie, caractéristiques, protection. Delachaux et Niestlé, ParisGoogle Scholar
  18. Dupuis I (1986) Les Chiropteres du Quaternaire en France. Mémoire de Maîtrise de l’Université de Paris I, ParisGoogle Scholar
  19. Dzeverin II, Strelkov PP (2008) Taxonomic status of Myotis blythii (Chiroptera, Vespertilionidae) from the Altai. Zool Zh 87:973–982Google Scholar
  20. Evin A, Baylac M, Ruedi M, Mucedda M, Pons J (2008) Taxonomy, skull diversity and evolution in a species complex of Myotis (Chiroptera: Vespertilionidae): a geometric morphometric appraisal. Biol J Linn Soc 95(3):529–538Google Scholar
  21. Felten H, Spitzenberger F, Storch G (1977) Zur Kleinsäugerfauna West-Anatoliens. Teil IIIa. Senckenberg Biol 58:1–44Google Scholar
  22. Freeman PW (1981) Correspondence of food habits and morphology in insectivorous bats. J Mammal 62(1):164–166Google Scholar
  23. Freeman PW (2000) Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evol Ecol Res 2(3):317–335Google Scholar
  24. Furman A, Coraman E, Celik YE, Postawa T, Bachanek J, Ruedi M (2014) Cytonuclear discordance and the species status of Myotis myotis and Myotis blythii (Chiroptera). Zool Scripta 43(6):549–561Google Scholar
  25. Galán J, Cuenca-Bescós G, López-García JM (2016a) The fossil bat assemblage of Sima del Elefante lower red unit (Atapuerca, Spain): first results and contribution to the palaeoenvironmental approach to the site. C R Palevol 15(6):647–657Google Scholar
  26. Galán J, Cuenca-Bescós G, López-García JM, Sauqué V, Núnez-Lahuerta C (2016b) Fossil bats from the late Pleistocene site of the Aguilón P7 cave (Zaragoza, Spain). C R Palevol 15(5):501–514Google Scholar
  27. Ghazali M (2009) Identification of Myotis blythii and M. myotis (Chiroptera, Vespertilionidae) from Eastern Europe based on the measurements of lower teeth. Vestnik zoologii 43(5):403–408Google Scholar
  28. Ghazali M, Dzeverin I (2013) Correlations between hardness of food and craniodental traits in nine Myotis species (Chiroptera, Vespertilionidae). Vestnik zoologii 47(1):67–76.Google Scholar
  29. Gulia G (1913) Uno Sguardo alla Zoologia delle Isole Maltesi. In: IX International Congress of Zoology, March 1913, Monaco, pp 545–555Google Scholar
  30. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9Google Scholar
  31. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276Google Scholar
  32. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112Google Scholar
  33. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913Google Scholar
  34. Jenrich J, Löhr P-W, Müller F, Vierhaus H (2012) Fledermäuse. Bildbestimmungsschlüssel anhand von Schädelmerkmalen. Imhof Verlag, FuldaGoogle Scholar
  35. Kowalski K, Ruprecht A (1981) Order bats-Chiroptera. In: Pucek Z (ed) Keys to Vertebrates of Poland. Polish Scienlilic Publishers, Warsaw, pp 101–154Google Scholar
  36. Lanza B (1959) Chiroptera Blumenbach, 1774. In: Toschi A, Lanza B (ed) Fauna d’Italia, Vol. IV, Mammalia, generalità, Insectivora, Chiroptera. Ed. Calderini, Bologna, pp 187–473Google Scholar
  37. López-García JM (2011) Los micromamíferos del Pleistoceno superior de la Península Ibérica. Evolución de la diversidad taxonómica y cambios paleoambientales y paleoclimaticos. Editorial Académica Española, SaarbrückenGoogle Scholar
  38. Mein P (1975) Les Chiroptères (Mammalia) du gisement Pléistocène moyen des Abimes de la Fage à Noailles (Corrèze). Nouvelle Archives du Musée d’Histoire naturelle de Lyon 13:57–67Google Scholar
  39. Menu H, Popelard J-B (1987) Utilisation des caractères dentaires pour la détermination des Vespertilionines de l’Ouest Européen. Le Rhinolophe 4:1–88Google Scholar
  40. Mitchell-Jones T (2017) Mammal mapping, European-mammals.org. https://www.european-mammals.org/php/mapmaker.php
  41. Palomo LJ, Gisbert J, Blanco JC (2007) Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, MadridGoogle Scholar
  42. Paz O de, Benzal J (1991) Los refugios importantes y su valoración ecológica para los murciélagos españoles. Los murciélagos de España y Portugal 1(1):3–140Google Scholar
  43. Ruedi M, Castella V (2003) Genetic consequences of the ice ages on nurseries of the bat Myotis myotis: A mitochondrial and nuclear survey. Mol Ecol 12(6):1527–1540Google Scholar
  44. Ruedi M, Mayer F (2001) Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggest deterministic ecomorphological convergences. Mol Phylogenet Evol 21:436–448Google Scholar
  45. Sauqué V, Cuenca-Bescós G (2013) The Iberian peninsula, the last European refugium of Panthera pardus Linnaeus 1758 during the upper Pleistocene. Quaternaire 24(1):35–48Google Scholar
  46. Sevilla P (1988) Estudio Paleontológico de los Quirópteros del Cuaternario español. Paleontologia i Evolució 22:113–233Google Scholar
  47. Sevilla P (1989) Quaternary Fauna of bats in Spain: Paleoecologie and biogeographic interest. In: Hanak V, Horáček I, Gaisler J (ed) European Bat Research 1987. Charles University Press, Praga, pp 349–355Google Scholar
  48. Simmons NB (2005) Order Chiroptera. In: Wilson DE, Reeder DM (Ed) Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edition. Johns Hopkins University Press, Baltimore, pp 312–529Google Scholar
  49. Strelkov PP (1972) Myotis blythii (tomes, 1857): Distribution, geographical variability and differences from Myotis myotis (Borkhausen, 1797). Acta Theriol 17:355–380Google Scholar
  50. Topál G, Ruedi M (2001) Myotis blythii (tomes, 1857) – Kleines Mausohr. In: Krapp F (ed) Handbuch der Säugetiere Europas Bd 4/I (Fledertiere). AULAVerlag, GmbH, Wiebelsheim, pp 209–255Google Scholar
  51. Topál G, Tusnádi G (1963) Data for the craniometric investigation of Myotis myotis Borkh. and Myotis oxygnathus Montic. in Hungary (Mammalia). In: Annales historico-naturales Musei nationalis hungarici (Vol. 55). Gondolat Kiadó, Budapest, pp 543–549Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Earth Science, Area of PalaeontologyUniversity of ZaragozaZaragozaSpain
  2. 2.Aragosaurus-IUCAUniversity of ZaragozaZaragozaSpain
  3. 3.IPHESUniversity of Rovira i VirgilTarragonaSpain

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