Sacrum and Pelvic Girdle Development in Lacertidae

Yegor B. Malashichev


Sacrum and pelvis structure and development in four species of Lacertidae currently assigned to different genera are studied: Lacerta agilis, L. vivipara, L. saxicola, Podarcis muralis. Size, shape, and position relationships between the cartilaginous elements as well as patterns and sequence of chondrification and ossification are given. Two sacral segments are characterized by a number of markers such as the branching of iliac arteries, development of the paired lymphatic hearts, and degeneration of sacral myomeres beginning from the dividing sacral myoseptum. Lizard species differ one from another by the number of presacral vertebrae and the extent of ossification. Degeneration of sacral myomeres and formation of the sacral gap in myomeres play a crucial role in development of sacral ribs and in the direction of their growth. Sacral vertebrae are defined as vertebrae, which ribs or transverse processes develop at the place of the sacral gap. There are ribs vs. diapophyses in Lacertidae and most probably in other lizards. Caudal ribs are not found, but prerequisites for their development take place, so they might be expected as a rare anomaly in Lacertidae. There is a strict order of maturation of skeletal elements: vertebral centra and neural arches, ilium, pubis, ischium and sacral ribs, which has its reflection in the adult phenotype. Additional elements of the pelvic girdle, namely, epipubis, epiischium, and hypoischium develop along the axial fibrous ligament and undergo chondrification and calcification separately. A hypothesis that the overall shape of the pelvic girdle is formed under the influence of the visceral cavity is partly supported. Cause-and-effect explanations of sacrum and pelvis morphogenesis are given. Certain anomalies of sacral structure are described and discussed in developmental terms.


sacrum; pelvic girdle; ribs; development; Lacertidae; anomalies; morphogenesis

Full Text:



Akita K. (1992), «An anatomical investigation of the muscles of the pelvic outlet in Iguanas (Iguanidae Iguana iguana) and Varanus (Varanidae Varanus (dumerillii)) with special reference to their nerve supply», Anat. Anz., 174, 119 – 129.

Arribas O. J. (1999), «Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Mertens, 1921, sensu lato) and their relationships among the Eurasian lacertid radiation», Russ. J. Herpetol., 6(1), 1 – 22.

Anisimova E. V. (1990), «Structure, development and variability of the sacro-pelvic area in common newt (Triturus vulgaris L.)», Vestn. LGU. Ser. 3. Biol., Issue 1 (No. 3), 3 – 10 [in Russian].

Borkhvardt (Borchwardt) V. G. (1977), «Development of the vertebral column in embryogenesis of Lacerta agilis», Zool. Zh., 56, 576 – 587 [in Russian].

Borkhvardt V. G. (1982), Morphogenesis and Evolution of the Axial Skeleton (a Theory of Skeletal Segment), Izd. LGU, Leningrad [in Russian].

Borkhvardt V. G. (1992), «On the origin of tetrapod sternum», Vestn. SPbGU. Ser. 3. Biol., Issue 1 (3), 3 – 11 [in Russian].

Borkhvardt V. G. (1995), «On the formation of sacroiliac skeletal complex in the onthogenesis (sic) of Tetrapoda», Zool. Zh., 74, 84 – 94 [in Russian].

Borkhvardt V. G. and Malashichev Y. B. (2000), «Correlative changes during early morphogenesis of the sacroiliac complex in squamate reptiles», Anat. Anz., 182(5), 439 – 444.

Braun V. A. and Goryshin N. I. (1978), «Climate chambers with programming of photoperiodic and temperature rhythms for ecological research», Vestn. LGU, No. 3, 26 – 34 [in Russian].

Cligny M. A. (1899), Vertébres et Cœurs lymphatique des Ophidiens, Imprimerie L. Danel, Lille.

Dal Sasso C. and Signore M. (1998), «Exceptional soft-tissue preservation in a theropod dinosaur from Italy», Nature, 392, 383 – 387.

Davis A. P. and Capecchi M. R. (1994), «Axial homeosis and appendicular skeleton defects in mice with a targeted disruption of hoxd-11», Development, 120, 2187 – 2198.

Dufaure J. P. and Hubert J. (1961), «Table de dévelopement du lézard vivipare, Lacerta vivipara Jacquin», Arch. Anat. Micr. Morph. Exp., 50, 309 – 327.

El-Toubi M. R. (1938), «The osteology of the lizard Scincus scincus (Linn.)», Bull. Fac. Sci. Egyptian Univ., 14, 1 – 39.

El-Toubi M. R. (1947), «Sacral ribs of Lacertilia», Nature, 159, 342.

El-Toubi M. R. and Khalil A. (1950), «Caudal ribs in geckos», Nature, 166, 1120.

Fromental-Ramain C., Warot X., Lakkaraju S., et al. (1996), «Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning», Development, 122, 461 – 472.

Gerard M., Chen J-Y., Gronemeyer H., Chambon P., Duboule D., and Zákány J. (1996), «In vivo targeted mutagenesis of a regulatory element required for positioning the Hoxd-11 and Hoxd-10 expression boundaries», Gen. Devel., 10, 2326 – 2334.

Ghurtovoj N. N., Matveev B. S., and Dzerzhinsky F. J. (1978), Practical Zootomy of Vertebrates, Vysshaya Shkola, Moscow [in Russian].

Hardaway T. E. and Williams K. L. (1975), «A procedure for double staining cartilage and bone», Br. J. Herpetol., 5(4), 23 – 27.

Hinchliffe J. R. and Johnson D. R. (1983), «Growth of cartilage», in: B. K. Hall (ed.), Cartilage, Vol. 2, Acad. Press, New York, pp. 255 – 295.

Hoffstetter R. and Gasc J.-P. (1969), «Vertebrae and ribs of modern reptiles», in: C. Gans (ed.), Biology of the Reptilia. Vol. 1. Morphology A, Acad. Press, London – New York, pp. 201 – 310.

Holder L. A. (1960), «The comparative morphology of the axial skeleton in the Australian Gekkonidae», Zool. J. Linn. Soc. (Lond.), 44, 300 – 335.

Kamel A. E. (1951), «Sacral ribs of Lacertilia», Nature, 168, 660 – 661.

Kamel A. E. (1952), «On the development of the ribs in the sacral region of a reptile Chalcides ocellatus (Forskäl)», Publ. l’Inst. Fouad 1er du Desert, 1, 1 – 77.

Kovalenko E. E. (1992), The Anomalies of the vertebral Column in Tailless Amphibians, Izd. SPbGU, St. Petersburg [in Russian]

Malashichev Y. B. (1999), «Evolutionary changes of the pelvic girdle in Tetrapoda — evidence from ontogenetic studies», in: J.-Y. Chen, P. K. Chien, D. J. Bottjer, G.-X. Li, and F. Gao (eds.), Int. Symp. The Origins of Animal Body Plans and Their Fossil Records, June 20 – 25, Early Life Research Center, Kunming, pp. 27 – 30.

Malashichev Y. B. and Borkhvardt V. G. (1999), «On sacral myomeres in embryos of reptiles with fully developed and reduced limbs», in: C. Miaud and R. Guyétant (eds.), Current Studies in Herpetology, Le Bourget du Lac/France (SEH), pp. 305 – 307.

Malashichev Y. B. and Pawlowska-Indyk A. (1997), «Temperature dependent variability and sacrum features displacement in Bombina variegata (Anura: Discoglossidae)», in: Z. Rocek and S. Hart (eds.), Herpetology’97. Abstrs. of the 3rd World Congr. of Herpetol., August 2 – 10, 1997, Prague, p. 134.

Mayer W. and Bischoff W. (1996), «Beiträge zur taxonomischen Revision der Gattung Lacerta (Reptilia: Lacertidae). Teil 1: Zootoca, Omanosaura, Timon und Teira als eigenständige Gattungen», Salamandra, 32, 171 – 180.

Moodie R. L. (1907), «The sacrum of Lacertilia», Biol. Bull., 13, 84 – 93.

Raynaud A., Gasc J.-P., Renous S., and Pieau C. (1975), «Étude comparative, embryologique et anatomique, de la région pelvi-cloacale et de sa musculature chez le lézard vert (Lacerta viridis Laur.) et l’orvet (Anguis fragilis L.)», Mém. Mus. Natl. Hist. Nat. Nouv. Ser. Ser. A. Zool., 95, 1 – 62.

Rieppel O. (1992), «Studies on skeleton formation in reptiles. III. Patterns of ossification in the skeleton of Lacerta vivipara Jacquin (Reptilia, Squamata)», Fieldiana. Zool. New Ser., 68, 1 – 25.

Rieppel O. (1993), «Studies on skeleton formation in reptiles. V. Patterns of ossification in the skeleton of Alligator mississipiensis Daudin (Reptilia, Crocodylia)», Zool. J. Linn. Soc. (Lond.), 109, 301 – 325.

Rieppel O. (1994), «Studies on the skeleton formation in reptiles. Patterns of ossification in the skeleton of Lacerta agilis exigua Eichwald (Reptilia, Squamata)», J. Herpetol., 28, 145 – 153.

Romer A. S. (1956), Osteology of the Reptilia, Univ. Chicago Press, Chicago.

Sabatier A. (1880), Ceintures et des Membres Antérieurs et Postérieurs dans la Série des Vertébrés, Montpellier, Paris

Saint-Girons H. (1985), «Comparative data on lepidosaurian reproduction and some time tables», in: C. Gans and F. A. Billett (eds.), Biology of the Reptilia. Vol. 15, Wiley, Chichester, pp. 35 – 58.

Smith D. M. and Tabin C. J. (1999), «BMP signaling specifies the pyloric sphincter», Nature, 402, 748 – 749.

Stephenson N. G. (1960), «The comparative osteology of Australian geckos and its bearing on their morphological status», Zool. J. Linn. Soc. (Lond.), 44, 278 – 299.

Tremblay P., Dietrich S., Mericskay M., Schubert F. R., Li Z., and Paulin D. (1998), «A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors», Dev. Biol., 203, 49 – 61.

Wellborn V. (1933), «Comparative osteological examinations of Geckonids, Eublepharids and Uroplatids», Herpetol. Transl., 1997, 1, 1 – 101.

Werner Y. L. (1971), «The ontogenetic development of the vertebrae in some gekkonoid lizards», J. Morphol., 133, 41 – 92.

Wiedersheim R. (1898), Grundriss der vergleichenden Anatomie der Wirbelthiere, Verlag von Gustav Fischer, Jena.

Wilting J., Kurz H., Brand-Saberi B., et al. (1994), «Kinetics and differentiation of somite cells forming the vertebral column: studies on human and chick embryos», Anat. Embryol., 190, 573 – 581.

Zákány J. and Duboule D. (1999), «Hox genes and the making of sphincters», Nature, 401, 761 – 762.


  • There are currently no refbacks.