The development of cranial base and cranial vault bones at successive stages of embryonic development in Grass snake Natrix natrix (Serpentes, Colubridae) is described in the article. The stages of embryo development are determined by the table of stages of normal development, suggested by Zehr (Copeia 2:322–329, 1962). 35 N. natrix embryos were examined; 20 embryos were studied with histological methods; 15 embryos were cleared and double-stained with alizarin red and alcian blue. The sequence of appearance and formation of cranial base and cranial vault bones are determined. New features in the appearance and mode of ossification of some bones are revealed: the postorbital, parietal bones and basisphenoid are formed from two ossification centers and the prefrontal bone—from three ossification centers; the supraoccipital bone is formed as a paired bone; the laterosphenoid is shown to be formed as a cartilage-replacement bone. The new data I received can be used in further comparative researches on the reptile skull development and studies on reptile phylogeny.
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Bäckström K (1931) Rekonstruktionsbilder zur Ontogenie des Koopfskelettes von Tropidonotus natrix. Acta Zool (Stock) 12:83–144
Boughner JC, Buchtova M, Fu K, Diewert V, Hallgrimsson B, Richman JM (2007) Embryonic development of Python sebae—I: staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology 110:212–230
Chekanovskaya OV (1936) Development of the skull in Grass snake (Tropidonotus natrix). Arch Anat Hist Embr 15(3):3–33 (in Russian)
Culling CFA (1974) Handbook of histopathological and histochemical techniques, 3rd edn. Butterworth, London
de Beer GR (1926) Studies on the vertebrate head. II. The orbito-temporal region of the skull. Q J Microsc Sci 70:263–370
Franklin MA (1945) The embryonic appearance of centres of ossification in the bones of snakes. Copeia 2:68–73
Haluska F, Alberch P (1983) The cranial development of Elaphe obsolete (Ophidia, Colubridae). J Morphol 178:37–55
Herna´ndez-Jaimes C, Jerez A, Ramı´rez-Pinilla MP (2012) Embryonic development of the skull of the Andean lizard Ptychoglossus bicolor (Squamata, Gymnophthalmidae). J Anat 221:285–302
Iordansky NN (1971) Cranium kineticism in reptile evolution. J Gen Biol 32(3):348–365 (in Russian)
Iordansky NN (1978) Kineticism of snake skull (unspecialized forms). Zoologicheskii zhurnal 47(2):240–252 (in Russian)
Jackson K (2002) Post-ovipositional development of the monocled cobra, Naja kaouthia (Serpentes: Elapidae). Zoology 105:203–214
Jerez A, Sanchez-Martinez PM, Guerra-Fuentes RA (2015) Embryonic skull development in the neotropical viviparous skink Mabuya (Squamata: Scincidae). Acta Zool Mex 31(3):391–402
Kamal AM, Hammouda HG (1965a) The development of the skull of Psammophis sibilans. III. The osteocranium of a late embryo. J Morphol 116:296–310
Kamal AM, Hammouda HG (1965b) The laterosphenoid bone in the Ophidia. Anat Anz 116:116–123
Kamal AM, Hammouda HG, Mokhtar FM (1970) The development of the osteocranium of the Egyptian Cobra I. The embryonic osteocranium. Acta Zool 51:1–17
Klembara J (2004) Ontogeny of the palatoquadrate and adjacent lateral cranial wall of the endocranium in prehatching Alligator mississippiensis (Archosauria: Crocodylia). J Morphol 262:644–658
Kovtun MF, Sheverdyukova HV (2011) Formation of the prootic foramina in Grass snake, Natrix natrix (Ophidia, Colubridae) chondrocranium embryogenesis. Vestnik Zool 45(6):561–565 (in Russian)
Kovtun MF, Sheverdyukova HV (2015) Early stages of skull embryogenesis in the Grass snake, Natrix natrix (Serpentes, Colubridae). Russ J Dev Biol 46(4):222–230
Parker WK (1878) On the structure and development of the skull in the common snake (Tropidonotus natrix). Philos Trans R Soc Lond 169:385–417
Polachovski KM, Werneburg I (2013) Late embryos and bony skull development in Bothropoides jararaca (Serpentes, Viperidae). Zoology 116:36–63
Pringle JA (1954) The cranial development of certain South African snakes and the relationship of these groups. Proc Zool Soc Lond 123:813–865
Rieppel O (1976) The homology of the lateroshenoid bone in snakes. Herpetologica 32(4):426–429
Rieppel O, Zaher H (2001) The development of the skull in Acrochordus granulates (Schneider) (Reptilia: Serpentes), with special consideration of the otico-occipital complex. J Morphol 249:252–266
Romer AS (1956) Osteology of the reptiles. The university of Chicago Press, Chicago
Severtsov AN (2012) Essays on the theory of evolution: individual development and evolution. Librokom, Moscow (in Russian)
Sheverdyukova HV (2012a) Development of the ethmoidal region of the chondrocranium in the Grass snake, Natrix natrix (Ophidia, Colubridae), embryogenesis. Vestnik Zool 46(3):247–257 (in Russian)
Sheverdyukova HV (2012b) Polar cartilages and formation of crista sellaris in grass snake’s chondrocranium Natrix natrix (Opidia, Colubridae) at the early stages of embryogenesis. Vestnik Zool 46(5):461–468
Simons EV, Van Horn JR (1971) A new procedure for whole-mount alcian blue staining of the cartilaginous skeleton of chicken embryos, adapted to the clearing procedure in potassium hydroxide. Acta Morphol Neerl Scand 8:281–292
Werneburg I, Sanchez-Villagra MR (2015) Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles. Evolution 69(1):254–263
Werneburg I, Polachowski KM, Hutchinson MN (2015) Bony skull development in the Argus monitor (Squamata, Varanidae, Varanus panoptes) with comments on developmental timing and adult anatomy. Zoology 118:255–280
Williston SW, Gregory WK (1925) The osteology of the reptiles. Harvard University Press, Cambridge
Zehr DR (1962) Stages in the normal development of the common garter snake Thamnophis sirtalis sirtalis. Copeia 2:322–329
The study was funded by the state budget.
Conflict of interest
The author declares that she has no conflict of interest.
All applicable international, national and institutional guidelines for the care and use of animals were followed.
No humans have been studied in the experiment.
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Sheverdyukova, H.V. Development of the osteocranium in Natrix natrix (Serpentes, Colubridae) embryogenesis I: development of cranial base and cranial vault. Zoomorphology 136, 131–143 (2017). https://doi.org/10.1007/s00435-016-0333-8
- Ossification center