Number of Ossification Centers in the Anuran Cranial Bones Depends upon the Rate of Development: Experimental Evidence

Sergei V. Smirnov, Anna B. Vassilieva


Cranial development was compared in Rana temporaria (Anura; Ranidae) and Bombina variegata (Anura; Discoglossidae) specimens reared at normal, high, and low level of thyroid hormone (TH). Sequence and timing of cranial ossification as well as rate of a particular bone’s differentiation and growth depend upon TH level. Also, bones which normally develop from a single ossification center (frontoparietal, parasphenoid, vomer, squamosal, angulosplenial, septomaxilla, pterygoid, and premaxilla) were revealed to form from two or more ossification centers in specimens reared at high and low TH level. This indicates them to develop from several early precalcified anlagen which normally fuse prior to the beginning of calcification thus appearing as a single ossification center. Changes in the rate of a particular bone’s differentiation and growth caused by manipulation with a TH level may cause precocious beginning of their calcification or their delayed fusion. As a result, they begin to calcify prior to their fusion thus appearing as several separate ossification centers. Number of ossification centers depends upon the rate of cranial and overall somatic development. Interspecies and individual differences in the rate of cranial and overall ontogeny are responsible for the inter- and intraspecific variability in the number of ossification centers recorded in anurans.


anurans; skull; bones; ontogeny; ossification centers; thyroid hormone

Full Text:



Banbury B. and Maglia A. M. (2006), «Skeletal development of the Mexican spadefoot, Spea multiplicata (Anura: Pelobatidae)», J. Morphol., 267, 808 – 821.

Bernasconi A. F. (1951), «Über den Ossifikationsmodus bei Xenopus laevis Daud»., Mem. Soc. Helvet. Sci. Nat., 79, 191 – 252.

Brown F. A., Jr. (1952), «Endocrine mechanisms», in C. L. Prosser (ed.), Comparative Animal Physiology, W. B. Saunders Co., Philadelphia – London, pp. 725 – 775.

Brown S. M. (1980), Comparative Ossification in Tadpoles of the Genus Xenopus (Anura, Pipidae). Masters Thesis, San Diego State Univ., San Diego, CA (cit. after Trueb and Hanken, 1992)

Čihák R., Královec K., and Roček Z. (2003), «Developmental origin of the frontoparietal bone in Bombina variegata (Anura: Discoglossidae)», J. Morphol., 255, 122 – 129.

Davies M. (1989), «Ontogeny of bone and the role of heterochrony in the myobatrachine genera Uperoleia, Crinia, and Pseudophryne (Anura: Leptodactylidae: Myobatrachinae)», J. Morphol., 206, 269 – 300.

de Sa R. O. (1988), «Chondrocranium and ossification sequence of Hyla lanciformis», J. Morphol., 195, 345 – 355.

de Sa R. O. and Trueb L. (1991), «Osteology, skeletal development, and chondrocranial structure of Hamptophryne boliviana (Anura: Microhylidae)», J. Morphol., 209, 311 – 330.

Erdmann K. (1933), «Zur Entwicklung des knöchernen Skelets von Triton und Rana unterbesonderer Berücksichtigung der Zeitfolge der Ossifikationen», Z. Anat. EntwGesch., 101, 566 – 651.

Gaudin A. J. (1978), «The sequence of cranial ossification in the California toad, Bufo boreas (Amphibia, Anura, Bufonidae)», J. Herpetol., 12, 309 – 318.

Gosner K. L. (1960), «A simplified table for staging anuran embryos and larvae with notes on identification», Herpetologica, 16, 183 – 190.

Griffiths I. (1954a), «On the nature of the fronto-parietal in Amphibia, Salientia», Proc. Zool. Soc. London, 123, 781 – 792.

Griffiths I. (1954b), «On the ‘otic element’ in Amphibia Salientia», Proc. Zool. Soc. London, 124, 35 – 50.

Hall J. A. and Larsen J. H. (1998), «Postembryonic ontogeny of the spadefoot toad, Scaphiopus intermontanus (Anura: Pelobatidae): skeletal morphology», J. Morphol., 238, 179 – 244.

Hanken J. and Hall B. K. (1988a), «Skull development during anuran metamorphosis. II. Role of thyroid hormone in osteogenesis», Anat. Embryol., 178, 219 – 227.

Hanken J. and Hall B. K. (1988b), «Skull development during anuran metamorphosis. I. Early development of the three first bones to form — the exoccipital, the parasphenoid, and the frontoparietal», J. Morphol., 195, 247 – 256.

Jarvik E. (1942), «On the structure of the snout in Crossopterygians and lower Gnathostomes», Zool. Bidr. Uppsala, 21, 237 – 675.

Jarvik E. (1967), «The homologies of frontal and parietal bones in fishes and tetrapods», Colloq. Int. Cent. Nat. Rech. Sci., 163, 181 – 213.

Kemp N. E. and Hoyt J. A. (1965), «Influence of thyroxine on order of ossification of bones of the skull of Rana pipiens», Am. Zool., 5, 719.

Kemp N. E. and Hoyt J. A. (1969), «Sequence of ossification in the skeleton of growing and metamorphosing tadpoles of Rana pipiens», J. Morphol., 129, 415 – 444.

Klembara J., Tomášik A., and Kathe W. (2002), «Subdivisions, fusions, and extended sutural areas of dermal skull bones in Discosauriscus Kuhn (Seymouriamorpha: Discosauriscidae)», N. Jb. Geol. Palaontol. Abh., 223, 317 – 349.

Klembara J., Pančišin L., and Tomášik A. (2004), «The first record of a subdivided nasal and frontoparietal in Bombina bombina (Anura, Discoglossidae)», Biologia (Bratislava), 59, 293 – 296.

Lebedkina N. S. (1979), The Evolution of the Amphibian Skull, Nauka, Moscow [in Russian].

Lebedkina N. S. (1986), «The homologies of temporal bones in Amphibia and Reptilia», in: Z. Roček (ed.), Studies in Herpetology, Charles University, Prague, pp. 303 – 305.

Lebedkina N. S. (2004), The Evolution of the Amphibian Skull, Pensoft, Sofia.

Reinbach W. (1939), «Über das Os supratemporale von Pelobates fuscus», Morphol. Jb., 84, 169 – 186.

Roček Z. (1981), «Cranial anatomy of frogs of the family Pelobatidae Stannius, 1856, with outlines of their phylogeny and systematics», Acta Univ. Carol. Biol., 1980, 1 – 164.

Roček Z. (2003), «Larval development in Oligocene palaeobatrachid frogs», Acta Palaeontol. Pol., 48, 595 – 607.

Smirnov S. V. (1992), «The influence of variation in larval period on adult cranial diversity in Pelobates fuscus (Anura: Pelobatidae)», J. Zool. Lond., 226, 601 – 612.

Smirnov S. V., Vassilieva A. B., and Merkulova K. M. (2008), «Role of heterochronies in the morphogenesis of amphibian skull bones: an experimental study», Dokl. Biol. Sci., 418, 64 – 66.

Smirnov S. V. and Vassilieva A. B. (2003), «Skeletal and dental ontogeny in the smooth newt, Triturus vulgaris (Urodela: Salamandridae): role of thyroid hormone in its regulation», Russ. J. Herpetol., 10(2), 93 – 110.

Smirnov S. V. and Vassilieva A. B. (2005), «Skull development in normal, TH-exposed, and goitrogen-treated axolotls, Ambystoma mexicanum», Russ. J. Herpetol., 12(2), 113 – 126.

Trueb L. and Hanken J. (1992), «Skeletal development in Xenopus laevis (Anura, Pipidae)», J. Morphol., 214, 1 – 41.

Vassilieva A. B. and Smirnov S. V. (2007), »The role of thyroid hormones in the bony skull development in the common frog (Rana temporaria, Ranidae)», Dokl. Biol. Sci., 413, 11 – 114.

Wiens J. J. (1989), «Ontogeny of the skeleton of Spea bombifrons (Anura: Pelobatidae)», J. Morphol., 202, 29 – 51.



  • There are currently no refbacks.

You can subscribe to the print or electronic version of the journal on the site of EastView Company. If you have any questions, please write to the email