Ossification patterns of the skeleton in the larvae of the common European toad Bufo bufo
DOI:
https://doi.org/10.14720/abs.60.1.15670Keywords:
skeleton, ossification, Bufo bufo, clearing and staining method for skeletonAbstract
We used a clearing and staining method for cartilage and bone to analyse the pattern of ossification in the skeleton of the common European toad, Bufo bufo, a species with rapid larval development. We focused on the ossification of vertebrae, pectoral and pelvic girdles, and limbs with an emphasis of the ossification in their distal parts. We found that the cartilage primordia of the skeleton were formed by the end of premetamorphosis (Stage 34). The first ossifications appeared in early prometamorphosis (Stage 39) and occurred concurrently in the neural arches, diaphyses of proximal elements of front and hind limbs, and in the proximal part of the ileum. The pectoral girdle was still completely cartilaginous at this stage. Ossification intensifies during prometamorphosis and gradualy progresses in a cranial - caudal direction along the spine and from proximal to distal parts of the skeleton, as well as to the epiphyses of the long bones. Fingers ossified in a posterio-anterior direction according to the main limb axis. As in most other anurans, the skeleton of Bufo is almost completely ossified by the end of the metamorphic climax (Stage 46). At this time, cartilage remains in the dorsal midline of the spine, in the distal parts of transverse processes of the vertebrae, the caudal part of the post-sacral region, as well as in the epiphyses, and carpals and metacarpals of the limbs, and in the suprascapula and the pubis of the girdles. These results show a conserved pattern of ossification in B. bufo common to other anurans despite its rapid rate of larval development.
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References
Badawy, G.M., Sakr, S.A., Atallah, M.N., 2012. Comparative study of the skeletogenesis of limb autopods in the developing chick Gallus domesticus and toad Bufo regularis. RJPBCS, 3 (4), 966-988.
Carter, D.R., Mikic, B., Padian, K., 1998. Epigenetic mechanical factors in the evolution of long bone epiphyses. Zool. J. Linn. Soc., 123, 163-168. DOI: https://doi.org/10.1111/j.1096-3642.1998.tb01298.x
Çiçek¸ K., Kumaş, M., Dínçer, A., 2011. Differentiation of bone tissue and long bone development in the Uludağ frog, Rana macrocnemis tadpoles. Biharean Biol., 5(2), 123-126.
Duellman, W., Trueb, L., 1986. Biology of Amphibians. In: Duellman, W. (ed.): Musculo-Skeletal System,1st ed. McGraw-Hill, New York, pp. 289-365.
Dunlap, K.D., Sanchiz, B., 1996. Temporal dissociation between the development of the cranial and appendicular skeletons in Bufo bufo (Amphibia: Bufonoidae). J. Herpetol., 30 (4), 506-513. DOI: https://doi.org/10.2307/1565693
Felisbino, S.L., Carvalho, H.F., 2002. Ectopic mineralization of articular cartilage in the bullfrog Rana catesbeiana and its possible involvement in bone structure. Cell Tissue Res., 307 (3), 357-365. DOI: https://doi.org/10.1007/s00441-001-0508-5
Gilbert, S.F., 2000. Developmental Biology. In: Gilbert, S.F. (ed.): Osteogenesis: The Development of Bones, 6th ed. Sinauer Associates Inc.,U.S., 695 pp.
Gosner, K.L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16 (3), 183-190.
Hanken, J., Wassersug, R.J., 1981. The visible skeleton. Functional Photography, 16(4), 22-26.
Haas, A., 1999. Larval and metamorphic skeletal development in the fast-developing frog Pyxicephalus adspersus (Anura, Ranidae). Zoomorphology, 119(1), 23–35. DOI: https://doi.org/10.1007/s004350050078
Kemp, N., Hoyt, J., 1969. Sequence of ossification in the skeleton of growing and metamorphosing tadpoles of Rana pipiens. J. Morph., 129(4), 415-443. DOI: https://doi.org/10.1002/jmor.1051290404
Liem, K.F., Bemis, W.E., Walker, W.F., Grande, L., 2001. Functional anatomy of the vertebrates: An evolutionary perspective, 3rd ed. Thomson Brooks/Cole. USA, 784 pp.
Nieuwkoop P.D., Faber J. 1956. Normal Table of Xenopus laevis (Daudin). A Systematical and Chronological Survey of the Development fro Fertilized Egg till the End od Metamorphosis. Elsevier., Amsterdam. Pough, F.H., Janis, C. M., Heiser, J. B., 2013. Vertebrate life, 9th ed. Pearson Educations, Inc. USA, 634 pp.
Pugener, L.A., Maglia, A.M., Trueb, L., 2003. Revisiting the contribution of larval characters to an analysis of phylogenetic relationships of basal anurans. Zool. J. Linn. Soc. 139, 129–155. DOI: https://doi.org/10.1046/j.1096-3642.2003.00075.x
Rieppel, O., 1994. Studies on skeleton formation in reptiles. Patterns of ossification in the skeleton of Lacerta agilis exigua Eichwald (Reptilia, Squamata). J. Herpetol, 28, 145-153. DOI: https://doi.org/10.2307/1564613
Ročkova, H., Roček, Z., 2005. Development of the pelvis and posterior part of the vertebral column DOI: https://doi.org/10.1111/j.0021-8782.2005.00366.x
in the Anura. J. Anat., 206(1), 17-35.
Rozenblut, B., Ogielska, M., 2005. Development and Growth of Long Bones in EuropeanWater Frogs (Amphibia: Anura: Ranidae), With Remarks on Age Determination. J. Morphol., 265, 304-317. DOI: https://doi.org/10.1002/jmor.10344
Semlitsch, R. 1994. Evolutionary consequences of non-random mating: do large male increase offspring fitness in the anuran Bufo bufo? Behav. Ecol. Sociobiol., 34, 19-24. DOI: https://doi.org/10.1007/BF00175454
Simsa, S., Monsonego Ornan, E., 2007. Endochondral ossification process of the turkey (Meleagris gallopavo) during embryonic and juvenile development. Poult. Sci., 86, 565. Taylor, A.S., Kollros, J.J., 1946. Stages in the normal development of Rana pipiens larvae. Anat. Rec., 94, 7-23. DOI: https://doi.org/10.1093/ps/86.3.565
Yildirim, E., Ugur, K., 2014. Comparative skeletogenesis of the Oriental Tree Frog Hyla orientalis (Anura: Hylidae). Zool. Anz., 253, 361–371. DOI: https://doi.org/10.1016/j.jcz.2014.04.002
Wake, D.B., Roth, G., 1989. The linkage between ontogeny and phylogeny in the evolution of complex systems. In Wake, D.B., and Roth, G., (eds.): Complex Organismal Functions: Integration and Evolution in Vertebrates, John Wiley & Sons, pp. 361-377.
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