A standardized series of embryonic stages for the emydid turtle Trachemys scripta

Interspecific comparisons of embryological development in turtles have been confounded by differences in morphology, number of stages, and relative detail of information provided for stages. To mitigate this problem for the family Emydidae, the largest family of turtles, a 27-stage scheme is presented for Trachemys scripta. Because the earliest stages of development are comparable across all turtle taxa, only the latter portion of development (stages 12–26) is emphasized. Stages are defined on the basis of forelimb and claw morphological criteria described previously for Chelydra serpentina. Résumé : La comparaison interspécifique du développement embryonnaire chez les tortues est difficile à cause des différences dans la morphologie, dans le nombre de stades et dans la quantité d’informations disponibles sur chaque stade. Pour résoudre ce problème chez les Emydidae, la plus grande famille de tortues, j’ai conçu un schéma en 27 étapes, présenté ici pour Trachemys scripta. Comme les premières phases du développement sont semblables chez toutes les tortues, l’emphase est mise sur la dernière partie du développement (stades 12–26). Les stades sont définis en fonction de critères morphologiques concernant les pattes antérieures et les griffes, critères déjà utilisés pour Chelydra serpentina. [Traduit par la Rédaction] 1370 Greenbaum Introduction To standardize developmental comparisons across taxa, previous workers have suggested using measures of body size, chronological age, and morphological stage (Hall and Miyake 1995). Because of disparate sizes and timing of development associated with different taxa or experimental conditions, interspecific comparisons are obfuscated or impossible when measurement or absolute chronological age data are used without other information (Greenbaum and Carr 2002). Morphological stages of development, such as those of tadpoles (Gosner 1960), utilize discrete changes in morphological features through time, thereby affording relative comparisons among taxa regardless of species, incubation temperature, hydric conditions, or other variable factors that affect embryological development. When specific taxa do not conform to all criteria for a given stage, one can identify changes that are useful for studies of sequence heterochrony (Smith 2001). Prior to the formal description and standardization of embryonic developmental stages in turtles, researchers used measurement ranges to describe approximate ages of embryos (Risley 1933). Ewert (1985) expended considerable effort to stage embryos of turtle taxa from papers published before the advent of staging criteria, using both external and internal morphological characteristics. In recent studies of embryological development of turtles, interspecific comparisons were hampered by the use of staging schemes with disparities in (i) number of stages; (ii) choice of morphological criteria for stages; and (iii) detail of morphological description. Yntema (1968) used 27 stages of development to describe a morphologically based staging sequence for the turtle Chelydra serpentina. Similar schemes, also with 27 stages, have been described for the trionychids Apalone spinifera (Greenbaum and Carr 2002) and Pelodiscus sinensis (Tokita and Kuratani 2001), the carettochelydid Carettochelys insculpta (Beggs et al. 2000), and the testudinid Testudo hermanni (Guyot et al. 1994). However, Mahmoud et al. (1973) described 23 stages of development for the emydid Chrysemys picta, and 31-stage schemes were developed for sea turtles (Crastz 1982; Miller 1985; Renous et al. 1989). Because the morphology and number of stages described for C. picta (Mahmoud et al. 1973) are incongruent with the well-established scheme for C. serpentina (Yntema 1968), most recent studies of embryonic freshwater turtles have used Yntema’s (1968) criteria to stage embryos. However, comparing most turtles with the staging criteria for C. serpentina is difficult because of disparate morphology; for example, trionychids lack carapace scutes and testudinids have highly modified claws. Comparisons are also confounded by the limited morphological descriptions of later Yntema (1968) stages and the subjectivity of choosing which morphological features are most important for delimiting stages, especially in the case of species that simultaneously display characteristics of two stages of C. serpentina. Some researchers avoid these issues by giving a range of Yntema (1968) stages; Cherepanov (1995) used this strategy in a study of shell development in P. sinensis. Most investigators of turtle development cite Yntema’s (1968) staging scheme without addressing the ways in which development in their taxa differs from that in C. serpentina (Crews et al. 1991; White and Thomas 1992). Because different authors stress different sets Received 27 November 2001. Accepted 26 June 2002. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 6 September 2002. E. Greenbaum. Division of Herpetology, Natural History Museum and Biodiversity Research Center, and Department of Ecology and Evolutionary Biology, 1345 Jayhawk Boulevard, The University of Kansas, Lawrence, KS 66045-7561, U.S.A. (e-mail: elig@ku.edu). J:\cjz\cjz8008\Z02-111.vp Tuesday, September 03, 2002 2:45:41 PM Color profile: Disabled Composite Default screen