Analysis of Cardiac Development in the TurtleEmys orbicularis(Testudines: Emidydae) using 3‐D Computer Modeling from Histological Sections

Abstract

In this article we present a 3-D modeling study of cardiac development in the European pond turtle, Emys orbicularis (of the reptilian order Testudines). The study is aimed at elucidating the embryonic development of the horizontal septum in the ventricle and underscoring the importance of 3-D reconstructions in studying morphogenesis. Turtles possess one common ventricle, partly divided into three cava by a vertical and a horizontal septum, of which the embryonic origins have so far not been described. We used serial sectioning and computerized high-resolution 3-D reconstructions of different developmental stages to create a chronological overview of cardiogenesis, in order to study this process. This has yielded a new understanding of the development of the horizontal septum and (directly related) the looping of the heart tube. This looping is found to be markedly different from that in the human heart, with the turtle having two clear bends in the part of the heart tube leaving the primitive ventricle, as opposed to one in humans. It is this particular looping that is reponsible for the formation of the horizontal septum. In addition to our findings on the ventricular septation this study has also yielded new insights into the developmental origins of the pulmonary vein. The 3-D reconstructions were built using our platform TDR-3-D base and enabled us to study the developmental processes in specific parts of the turtle heart separately and in three dimensions, over time. The complete 3-D reconstructions have been made available to the reader via internet using our 3-D model browser application, which allows interactive viewing of the models. The browser application can be found on bio-imaging.liacs.nl/galleries/emysorbicularis/TurtleGallery.html, along with additional images of both models and histological sections and animation sequences of the models. By allowing the reader to view the mate-

Evolution and Development of Ventricular Septation in the Amniote Heart

“…the turtle Emys ( Fig. 2A, B ), harboring an extensive loop of the OFT [17], the subepicardium, here referred to as epicardial cushion, is almost as elaborate as the flanking endocardial atrioventricular (AV) and OFT cushions.…”

Structure and function of the hearts of lizards and snakes

“…There are multiple synonyms for the term ‘muscular ridge’ and presently there is little consensus on the nomenclature (Webb et al ., ; Farrell et al ., ; Bertens et al ., ). It was originally coined as Muskelleiste by Brücke () and, hence, translated to ‘muscular ridge’ in English literature.…”

“…Some later authors preferred ‘horizontal septum’ arguing that ‘muscular ridge’ is ambiguous since the ventricle contains multiple muscular ridges or trabecular sheets (e.g. Holmes, ; Van Mierop & Kutsche, 1985 b ; Bertens et al ., ). The horizontal septum, however, is only ‘horizontal’ at particular transverse sections and actually has a rather spiraling shape towards the apex, probably inspiring Acolat () to coin the sensible term ‘Cloison hélicoïdale’, French for ‘helical septum’.…”

“…It has therefore repeatedly been hypothesized to constitute an important part of the complete ventricular septum of mammals, crocodilians and birds (however, see Sections II.5 and III; e.g. Bertens et al ., ). Defining the vertical septum as the sheet with the shortest distance to the atrioventricular valves, we measured its length in multiple species of squamates and testudines [Fig.…”

“…; Benninghoff, ; Buchanan, ; Farrell et al , ) and the embryonic cushion complex of amniotes (e.g. Goodrich, ; Moorman & Christoffels, ; de Lange et al , ; Bertens, Richardson & Verbeek, ; Jensen et al , 2013a). There are no chordae tendinae and papillary muscles as seen in mammals and birds, but the valvular insertion into the myocardium serves a similar function and may develop from the same embryological structures.…”