Jump to ContentJump to Main Navigation
Show Summary Details


Editor-in-Chief: Denys, Christiane

6 Issues per year

IMPACT FACTOR 2015: 0.538
5-year IMPACT FACTOR: 0.786

SCImago Journal Rank (SJR) 2015: 0.482
Source Normalized Impact per Paper (SNIP) 2015: 0.555
Impact per Publication (IPP) 2015: 0.723

See all formats and pricing
Volume 79, Issue 2 (May 2015)


Testing a long-standing hypothesis on the relation between the auditory bulla size and environmental conditions: a case study in two jird species (Muridae: Meriones libycus and M. crassus)

Fatemeh Tabatabaei Yazdi
  • Corresponding author
  • Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad, Azadi Square, 91735 Mashhad, Iran
  • Email:
/ Paolo Colangelo
  • Department of Biology and Biotechnologies “Charles Darwin”, University of Rome “La Sapienza”, Roma, Italy
/ Dominique Adriaens
  • Evolutionary Morphology of Vertebrates, K.L. Ledeganckstraat 35, 9000 Gent, Belgium
Published Online: 2014-07-18 | DOI: https://doi.org/10.1515/mammalia-2013-0043


Variation in mammalian auditory bulla size has been linked to environmental conditions, and has even been claimed to provide a habitat-specific survival value. Enlarged bullae are typically shared among species adapted to living in arid habitats. Previous studies suggest that jirds also exhibit this adaptive enlargement of the bulla. However, such claims are based on the observation on a limited number of specimens, and thus they provide no quantitative support for this hypothesis. Therefore, we tested this hypothesis using a combination of geometric morphometrics and multivariate statistical techniques on a large sample of two jird species that exhibit a wide and partially overlapping geographical (and hence climatic) range, i.e., Meriones crassus (Sundevall, 1842) and M. libycus (Lichtenstein, 1823). A total of 485 intact skulls of populations originating from Africa to the eastern Iranian Plateau were analysed. The covariation between auditory bulla shape and several geoclimatic variables was explored using the two-block partial least-squares method. To some degree, the results seem to support the hypothesis that morphological variation in the auditory bulla is, indeed, correlated with geoclimatic variation. However, this finding cannot be generalised at several levels, hence refuting the hypothesis of convergent correlations between geoclimatic conditions and bulla morphology. Species-specific differences were found at different levels, suggesting that if local responses are present, they may reflect interactions with phylogenetic constraints.

Keywords: geoclimatic variation; geometric morphometrics; rodent; skull; two-block partial least squares


  • Adriaens, D. 2007. Protocol for error testing in landmark based geometric morphometrics. <http://www.fun-morph.ugent.be/Miscel/Methodology/Morphometrics.pdf>. [Accessed February 20, 2012].

  • Agren, G. 1979. Field observations of social-behavior in a saharan gerbil – Meriones libycus. Mammalia 43: 135–146.

  • Ashton, K.G., M.C. Tracy and A. de Queiroz. 2000. Is Bergmann’s rule valid for mammals? Am. Nat. 156: 390–415. [Crossref]

  • Bronikowski, A. and C. Webb. 1996. Appendix: a critical examination of rainfall variability measures used in behavioral ecology studies. Behav. Ecol. Sociobiol. 39: 27–30. [Crossref]

  • Burda, H., V. Bruns and M. Müller. 1999. Sensory adaptations in subterranean mammals. Prog. Clin. Biol. Res. 335: 269–293.

  • Cardini, A., A.-U. Jansson and S. Elton. 2007. A geometric morphometric approach to the study of ecogeographical and clinal variation in vervet monkeys. J. Biogeogr. 34: 1663–1678. [Crossref]

  • Cardini, A., J.A.F. Diniz Filho, P.D. Polly and S. Elton. 2010. Biogeographic analysis using geometric morphometrics: clines in skull size and shape in a widespread African arboreal monkey. In: (A.M.T. Elewa, ed.) Morphometrics for nonmorphometricians, Lecture Notes in Earth Sciences 124. Springer-Verlag Publishers, Heidelberg, Germany. DOI 10.1007/978-3-540-95853-6_8. [Crossref]

  • Chaworth-Musters, J.L. and J.R. Ellerman. 1947. A revision of the genus Meriones. Proc. Zool. Soc. Lond. 117: 478–504.

  • Chevret, P. and G. Dobigny. 2005. Systematics and evolution of the subfamily Gerbillinae (Mammalia, Rodentia, Muridae). Mol. Phyl. Evol. 35: 674–688. [Crossref]

  • Colangelo, P., R. Castiglia, P. Franchini and E. Solano. 2010. Pattern of shape variation in the eastern African gerbils of the genus Gerbilliscus (Rodentia, Muridae): environmental correlations and implication for taxonomy and systematic. Mamm. Biol. 75: 302–310.

  • Darvish, J. 2009. Morphmetric comparison of fourteen species of the genus Meriones Illiger, 1811 (Gerbillinae, Rodentia) from Asia and North Africa. Iran J. Anim. Biosyst. 5: 59–77.

  • Dempster, E.R. and M.R. Perrin. 1991. Ultrasonic vocalizations of 6 taxa of Southern African gerbils (Rodentia, Gerbillinae). Ethol. 88: 1–10.

  • Dempster, E.R. and M.R. Perrin. 1994. Divergence in acoustic repertoire of sympatric and allopatric gerbil species (Rodentia, Gerbillinae). Mammalia 58: 93–104.

  • Elewa, A.M.T. Ed. 2004. Morphometrics: applications in biology and paleontology. Springer, Berlin. pp. 263.

  • Escoufier, Y. 1973. Le traitement des variables vectorielles. Biometrics 29: 751–760. [Crossref]

  • FAO. 2007. FAO World Climate Data (http://freegeographytools.com/2007/fao-world-climate-data). [Accessed July 20, 2012]

  • Goltsman, M.E., S.V. Popov, A.V. Tchabovsky and N.G. Borisova. 1994. Syndrome of sociality – comparative study of gerbils behavior. Zh. Obshch. Biol. 55: 49–69.

  • Hammer, Ø., D.A.T. Harper and P.D. Ryan. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4: 1–9.

  • Hashimoto, H., N. Moritani, S. Aoki-Komori, M. Tanaka and T.R. Saito. 2004. Comparison of ultrasonic vocalizations emitted by rodent pups. Exp. Anim. 53: 409–416.

  • Hetem, R.S., W.M. Strauss, L.G. Fick, S.K. Maloney, L.C.R. Meyer, A. Fuller, M. Shobrak and D. Mitchell. 2012. Selective brain cooling in Arabian oryx (Oryx leucoryx): a physiological mechanism for coping with aridity? J. Exp. Biol. 215: 3917–3924.

  • Hill, R.A. and R.I.M. Dunbar. 2002. Climatic determinants of diets and foraging behaviour in baboons. Evol. Ecol. 16: 579–593. [Crossref]

  • Huang, G.T., J.J. Rosowski, M.E. Ravicz and W.T. Peake. 2002. Mammalian ear specializations in arid habitats: structural and functional evidence from sand cat (Felis margarita). J. Comp. Physiol. 188: 663–681.

  • Hunt, R. M. Jr. 1974. The auditory bulla in Carnivora: an anatomical basis for reappraisal of carnivore evolution. J. Morphol. 143: 21–76.

  • Hunt, R. M. Jr. and W. K. Korth. 1980. The auditory region of Dermoptera: morphology and function relative to other living mammals. J. Morphol. 164: 167–211.

  • Klingenberg C.P. 2008. MorphoJ. Faculty of Life Sciences, University of Manchester, UK. Available from: http://www.flywings.org.uk/MorphoJ_page.htm. [Accessed September 2, 2012].

  • Lay, D.M. 1972. The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents. J. Morphol. 138: 41–120.

  • Liao, J., Z. Zhang and N. Liu. 2007. Effects of altitudinal change on the auditory bulla in Ochotona daurica (Mammalia, Lagomorpha). J. Zool. Syst. Evol. Res. 45: 151–154. [Crossref]

  • Maloney, S. K., A. Fuller, G. Mitchell and D. Mitchell. 2001. Rectal temperature measurement results in artifactual evidence of selective brain cooling. Am. J. Physiol. 281: R108–R114.

  • Mason, M.J. 2001. Middle ear structures in fossorial mammals: a comparison with non-fossorial species. J. Zool. Lond. 255: 467–486.

  • Mason, M.J. 2003. Morphology of the middle ear of golden moles (Chrysochloridae). J. Zool. Lond. 260: 391–403.

  • Meiri, S. and T. Dayan. 2003. On the validity of Bergmann’s rule. J. Biogeogr. 30: 331–351. [Crossref]

  • Misonne, X. 1959. Analyse Zoogéographique des mammifères de l’Iran. Bruxelles Mem. Inst. Roy. Sci. Nat. Belgique, 2nd Ser 59: 1–157.

  • Momenzadeh, M.,J. Darvish, F. Toutoniyan, M. Sarmad, and Sadeghi Shakib, F. 2008. Investigation of climatic effects on the shape and volume of tympanic bulla of Meriones libycus and Meriones persicus (Muridae: Rodentia) from northeastern Iran: an evolutionary approach. Iranian Journal of Animal Biosystematics 4: 63–73.

  • Monteiro, L.R., L.C. Duarte and S.F. Reis. 2003. Environmental correlates of geographical variation in the skull and mandible shape of the punaré rat, Thricomys apereoides (Rodentia: Echimyidae). J. Zool. Lond. 261: 47–57.

  • Musser, G.G. and M.D. Carleton. 2005. Superfamily Muroidea. In: (D.E. Wilson and D.M. Reeder, eds.) Mammal species of the World: a taxonomic and geographic reference, 3rd edition, Vol. 2. Johns Hopkins University Press, Baltimore, MD. pp. 894–1531.

  • Oaks, E. 1967. Structure and function of inflated middle ears of rodents. Ph.D. thesis. Yale University, New Haven, CT.

  • Osborn, D. J. and I. Helmy. 1980. The contemporary land mammals of Egypt (Including Sinai). Fieldiana Zool No 5.

  • Pavlinov, I.Y. 1979. Morphology and taxonomic significance of the middle ear ossicles in the jirds of the genus Meriones (Rodentia: Cricetidae). Zool. J. 58: 1703–1712. [In Russian].

  • Pavlinov, I.Y. 2001. Current concepts of Gerbillid phylogeny and classification, African small mammals. In: Proceedings of the 8th International Symposium on African Small Mammals, Paris. pp. 141–149.

  • Pavlinov, I.Y. 2008. A review of phylogeny and classification of Gerbillinae (Mammalia: Rodentia). Moscow Univ. Publ., Moscow, pp. 1–68.

  • Pavlinov, I.Y., A.A. Lissovsky and E.V. Obolenskaya. 2010. Geographic variation of skull traits in the Libyan jird, Meriones libycus (Rodentia: Gerbillinae), over its entire distribution area. Russ. J. Theriol. 9: 19–26.

  • Petter F. 1959. Evolution du dessin de la surface d’usure des molaires des Gerbillidés. Mammalia 23 (3): 304–315.

  • Petter, F. 1961. Répartition géographique et écologique des rongeurs désertiques (du Sahara occidental à l’Iran oriental). 25, Special, 1–222.

  • Randall, J.A., B. McCowan, K.C. Collins, S.L. Hooper and K. Rogovin. 2005. Alarm signals of the great gerbil: acoustic variation by predator context, sex, age, individual, and family group. J. Acoust. Soc. Am. 118: 2706–2714. [Crossref]

  • Reis, S.F., L.C. Duarte, L.R. Monteiro and F.J. Von Zuben. 2002a. Geographic variation in cranial morphology in Thrichomys apereoides (Rodentia: Echimyidae): I. Geometric descriptors of shape and multivariate analysis of geographic variation in shape. J. Mammal. 83: 333–344.

  • Reis, S.F., L.C. Duarte, L.R. Monteiro and F.J. Von Zuben. 2002b. Geographic variation in cranial morphology in Thrichomys apereoides (Rodentia: Echimyidae): II. Geographic units, morphological discontinuities, and sampling gaps. J. Mammal. 83: 345–353.

  • Rohlf, F.J. 2004. TpsDig, Ver. 2.12. Department of Ecology and Evolution, State University of New York at Stony Brook. <http://life.bio.sunysb.edu/morph/>. [Accessed June 20, 2012].

  • Rohlf, F.J. 2006. TpsPLS: Partial Least-Squares, Ver. 1.18. Department of Ecology and Evolution, State University of New York at Stony Brook. <http://life.bio.sunysb.edu/morph/>. [Accessed June 20, 2012].

  • Rohlf, F.J. and M. Corti. 2000. Use of two-block partial least squares to study covariation in shape. Syst. Biol. 49: 740–753. [PubMed]

  • Rychlik, L., M.G. Ramalhinho and D. Polly. 2006. Response to competition and environmental factors: skull, mandible, and tooth shape in Polish Water shrews (Neomys, Soricidae, Mammalia). J. Zool. Syst. Evol. Res. 44: 339–351. [Crossref]

  • Schleich, C.E. and A.I. Vasallo. 2003. Bullar volume in subterranean and surface-dwelling caviomorph rodents. J. Mammal. 84: 185–189. [Crossref]

  • Sheets, B.S. 1989. Cranial anatomy of Jaculus orientalis (Rodentia, Dipodoidea): new evidence for close relationship of dipodoid and muroid rodents. Undergraduate Honors Thesis, Baruch College, New York. pp. 1–37.

  • Squarcia, S.M., N.S. Sidorkewicj and E.B. Casanave. 2007. The hypertrophy of the tympanic bulla in three species of dasypodids (Mammalia, Xenarthra) from Argentina. Int. J. Morphol. 25: 597–602.

  • StatSoft, Inc. 2004. STATISTICA (data analysis software system), ver. 7. <www.statsoft.com>. [Accessed October 10, 2012].

  • Tong, H. 1989. Origine et évolution des Gerbillidae (Mammalia, Rodentia) en Afrique du Nord. Mem. Soc. Geol. France, n. ser. 155: 1–120.

  • Torigoe, Y., K. Kobayashi, and H. Riquimaroux. 2012. Categorical perception for frequency modulated sound derivative communication sound of Mongolian gerbils. Trans. Tech. Comm. Psychol. Physiol. Acoust. 42(3): 287–291.

  • Van der Straeten, E. and F. Dieterlen. 1992. Craniometrical comparison of tour populations of Praomys jacksoni captured at different heights in Eastern Zaire (Kivu). Mammalia 56: 125–131.

  • Webster, D.B. 1962. A function of the enlarged middle ear cavities of the kangaroo rat, Dipodomys. Physiol. Zool. 35: 248–255.

  • Webster, D.B. 1966. Ear structure and function in modern mammals. Am. Zool. 6: 451–466. [PubMed]

  • Webster, D.B. and M. Webster. 1984. The specialized auditory system of kangaroo rats. Contrib. Sens. Physiol. 8: 161–196.

  • Webster, D.B. and W. Plassmann. 1992. Parallel evolution of low frequency sensitivity in old world and new world desert rodents. In: (D.B. Webster, A.N. Popper and R.R. Fay, eds.) The evolutionary biology of hearing. Springer, Berlin Heidelberg New York. pp. 625–631.

About the article

Corresponding author: Fatemeh Tabatabaei Yazdi, Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad, Azadi Square, 91735 Mashhad, Iran, e-mail: ,

Received: 2013-03-12

Accepted: 2014-05-27

Published Online: 2014-07-18

Published in Print: 2015-05-01

Citation Information: Mammalia, ISSN (Online) 1864-1547, ISSN (Print) 0025-1461, DOI: https://doi.org/10.1515/mammalia-2013-0043. Export Citation

Comments (0)

Please log in or register to comment.
Log in