Morphology, development and heterochrony of the carapace of Giant Amazon River Turtle Podocnemis expansa (Testudines, Podocnemidae)

Abstract

With aim to report the ontogeny of the osseous elements of the carapace in Peurodiras, 62 embryos and 43 nestlings of Podocnemis expansa were collected and submitted to the clearing and staining technique of bones and cartilages and study of serial histological slices. The carapace has mixed osseous structure of endo and exoskeleton, formed by 8 pairs of costal bones associated with ribs, 7 neural bones associated with neural arches, 11 pairs of peripheral bones, 1 nuchal, 1 pygal and 1 suprapygal. This structure begins its formation in the beginning of stage 16 with the ossification of the periosteal collar of the ribs. With exception of the peripheral bones, the other ones begin their ossification during the embrionary period. In histologic investigation it was found that the costal bones and neural bones have a close relation to the endoskeleton components, originating themselves as intramembranous expansions of the periosteal collar of the ribs and neural arches, respectively. The condensation of the mesenchyme adjacent to the periosteal collar induces the formation of spikes that grow in trabeculae permeated by fibroblasts below the dermis. The nuchal bone also ossifies in an intramembranous way, but does not show direct relation to the endoskeleton. Such information confirms those related to the other Pleurodira, mainly with Podocnemis unifilis, sometimes with conspicuous variations in the chronology of the ossification events. The formation of dermal plates in the carapace of Pleurodira and Criptodira follow the same pattern.

Morphogenetic and constructional differences of the carapace of aquatic and terrestrial turtles and their evolutionary significance

“…This scenario of the carapace ossification seems to be shared by all aquatic turtles. It was observed in many representatives of freshwater families such as Chelydridae (Sheil & Greenbaum, ), Emydidae (Rice, Riccio, Gilbert, & Cebra‐Thomas, ), Trionychidae (Cherepanov, ; Hirasawa et al, ; Rice et al, ; Sánchez‐Villagra et al, ; Sheil, ), Podocnemididae (Lima et al, ; Vieira et al, ), and Chelidae (Werneburg, Hugi, Müller, & Sánchez‐Villagra, ). The same developmental scenario is characteristic of sea turtles from the families Cheloniidae, Protostegidae, and Dermochelyidae, which have a reduced bony shell (see Hirayama, ; Kordikova, ).…”

“…Neurals II, IV, and VI, which lag behind in their development, find themselves inside these broad fontanelles. Later, the formation of neuro-costal sutures slows down the growth of neurals III, V, and VII, while neurals II, IV, and VI continue to broaden into the fontanelles between the outermost left and right costals and, finally, become the largest neurals (closing a mosaic of plates according to Pritchard, 1988 It was observed in many representatives of freshwater families such as Chelydridae (Sheil & Greenbaum, 2005), Emydidae (Rice, Riccio, Gilbert, & Cebra-Thomas, 2015), Trionychidae (Cherepanov, 1995;Hirasawa et al, 2013;Rice et al, 2015;Sánchez-Villagra et al, 2009;Sheil, 2003), Podocnemididae (Lima et al, 2011;Vieira et al, 2016), and Chelidae (Werneburg, Hugi, Müller, & Sánchez-Villagra, 2009).…”

“…The bony shell contains elements of various origins. The dorsal shield (carapace) is made up by neural and costal plates developing on the basis of endoskeletal vertebrae and ribs, while the periphery and the ventral shield (plastron) are composed of various dermal ossifications (Cherepanov, ; Gilbert, Bender, Betters, Yin, & Cebra‐Thomas, ; Hirasawa, Nagashima, & Kuratani, ; Lima et al, ; Rieppel, ; Scheyer, Bruüllmann, & Sánchez‐Villagra, ; Vickaryous & Sire, ; Vieira et al, ; Zangerl, ). Despite the conservatism of the basic model, the shape of the turtle shell and the structure of its parts are quite diverse.…”

A developmental staging system and musculoskeletal development sequence of the common musk turtle (Sternotherus odoratus)

“…Their peculiar anatomy has made them the object of several embryological studies focusing on the development and evolution of the turtle shell, [1][2][3][4][5][6][7][8][9] shoulder, [10][11][12] head, 13 skull, [14][15][16][17][18][19][20] and general skeletal development. [21][22][23][24][25][26][27][28][29][30][31] Developmental staging systems have been described for members of several clades of turtles (Figure 1), including. [32][33][34][35][36][37][38][39][40][41][42][43] Here, we provide a comprehensive staging system for the mid to late embryonic development of the Stinkpot or Common musk turtle (Sternotherus odoratus), a North American turtle of the family Kinosternidae.…”

“…Turtles are among the most transformed of all amniotes, bearing many unique features, most notably a rigid trunk encased in a carapace. Their peculiar anatomy has made them the object of several embryological studies focusing on the development and evolution of the turtle shell, 1‐9 shoulder, 10‐12 head, 13 skull, 14‐20 and general skeletal development 21‐31 . Developmental staging systems have been described for members of several clades of turtles (Figure 1), including 32‐43 .…”