Staging criteria for embryos of the spiny softshell turtle,<i>Apalone spinifera</i>(testudines: Trionychidae)

Greenbaum, Eli; Carr, John L.

doi:10.1002/jmor.10036

Cited by 41 publications

(67 citation statements)

References 21 publications

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“…Early shell morphogenesis and subsequent variation was examined to establish the temporal window for turtle developmental divergence. During this time frame, the shoulder girdle was excised and gross anatomical details of the developing scapula were examined across equivalent developmental stages of representative lineages; staging followed established criteria [18][19][20].…”

Section: Methodsmentioning

confidence: 99%

Skeletal remodelling suggests the turtle's shell is not an evolutionary straitjacket

Cordero

Quinteros

2015

Biol. Lett.

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Recent efforts to decipher the enigma of the turtle's shell revealed that distantly related turtle species deploy diverse processes during shell development. Even so, extant species share in common a shoulder blade (scapula) that is encapsulated within the shell. Thus, evolutionary change in the correlated development of the shell and scapula probably underpins the evolution of highly derived shell morphologies. To address this expectation, we conducted one of the most phylogenetically comprehensive surveys of turtle development, focusing on scapula growth and differentiation in embryos, hatchlings and adults of 13 species. We report, to our knowledge, the first description of secondary differentiation owing to skeletal remodelling of the tetrapod scapula in turtles with the most structurally derived shell phenotypes. Remodelling and secondary differentiation late in embryogenesis of box turtles (Emys and Terrapene) yielded a novel skeletal segment (i.e. the suprascapula) of high functional value to their complex shell-closing system. Remarkably, our analyses suggest that, in soft-shelled turtles (Trionychidae) with extremely flattened shells, a similar transformation is linked to truncated scapula growth. Skeletal remodelling, as a form of developmental plasticity, might enable the seemingly constrained turtle body plan to diversify, suggesting the shell is not an evolutionary straitjacket.

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Section: Methodsmentioning

confidence: 99%

Skeletal remodelling suggests the turtle's shell is not an evolutionary straitjacket

Cordero

Quinteros

2015

Biol. Lett.

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“…For preservation, embryos from the 2000 season were fixed in 3% buffered formalin (buffered with 4 g monobasic sodium phosphate and 6 g dibasic sodium phosphate per liter of formalin) for at least a day, rinsed in water, and transferred to 70% ethanol for long-term storage (Simmons, 1995). Relative developmental stages of all embryos were assigned according to the external morphological criteria of Greenbaum and Carr (2003), modified from Yntema (1968). Measurements of external morphology were made with dial calipers to the nearest 0.1 mm.…”

Section: Methodsmentioning

confidence: 99%

“…Gray indicates either presence of ossification without retention of Alizarin Red stain or ossification present in some, but not all, specimens; black indicates ossification by retention of Alizarin red stain in all specimens. Ϫ and ϩ indicate early and late examples of particular stages; developmental stages from morphological criteria of Greenbaum and Carr (2003). cation is apparent in Centrale 4, ulnare, and pisiform simultaneously with Distal Carpal 5 and Metacarpal V (both postaxial elements; Fig. 12, Stage 25).…”

Section: Comparison Of Sequence and Pattern Of Ossification In Apalonmentioning

confidence: 98%

“…Although the developmental criteria of Apalone spinifera (Greenbaum and Carr, 2003) are designed to provide maximal congruence with those developed for Chelydra serpentina (Yntema, 1968), these two criteria diverge considerably beyond comparisons of limb morphology and direct comparisons between Apalone and Chelydra in terms of developmental stages are inappropriate. Additionally, in both species rapid ossification of elements within several developmental stages (e.g.…”

Section: Comparative Osteology and Developmentmentioning

confidence: 98%

“…Currently, a standard series of stages summarizing the embryonic development of all turtles remains elusive (Bellairs and Kamal, 1981;Ewert, 1985). Of the greater than 285 known species of turtles (Zug et al, 2001), external morphological criteria for staging the entire prehatching ontogeny exist for only approximately 10 species (C. serpentina: Yntema, 1968; Chrysemys picta: Mahmoud et al, 1973;Caretta caretta, Chelonia mydas, Chelonia depressa, Eretmochelys imbricata, Lepidochelys olivacea, and Dermochelys coriacea: Miller, 1985;Caretoochelys insculpta: Beggs et al, 2000; Apalone spinifera: Greenbaum and Carr, 2003;see also Ewert, 1985).…”

Section: Comparative Osteology and Developmentmentioning

confidence: 99%

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Osteology and skeletal development of Apalone spinifera (Reptilia: Testudines: Trionychidae)

Sheil

2003

Journal of Morphology

143

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Despite considerable attention that other groups of reptiles have received, few descriptions of the development and sequences of chondrification and ossification of the entire skeleton of turtles exist. Herein, the adult skeleton of the spiny softshell turtle, Apalone spinifera (Testudines: Trionychidae), is described; this description forms a basis of comparison for the embryonic skeleton and its ontogenesis. Descriptions are made on the basis of cleared and double-stained embryos and dry skeletal postembryonic specimens. The embryonic chondrocranium of A. spinifera is described and compared to those of Emys orbicularis and Caretta caretta, the sequence of chondrification of fore- and hindlimbs are compared with published descriptions of Chelydra serpentina and Chrysemys picta, and the sequence of ossification of elements is compared with those of C. serpentina, Lacerta vivipara, and Alligator mississippiensis. In A. spinifera, the first elements that ossify (Stage 17) are associated with the dermatocranium and mandible, followed by elements of the dermal skull table, lower jaw, and dermal elements of the plastron. In A. spinifera, the sequence of chondrification of limb elements is similar to that of C. serpentina; however, the sequence of ossification varies greatly among Apalone, Chelydra, Lacerta, and Alligator.

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Ultrastructure of eggshell and embryological development ofSalvator merianae(Squamata: Teiidae)

Arrieta

Olea

Rodríguez

et al. 2020

The Anatomical Record

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The objective of this study was to characterize the external morphology of Salvator meriane embryos in different stages of embryonic development and establish a relationship with the ultrastructure of the shell from oviductal transit to hatching. A total of 120 embryos were analyzed to describe their external morphology, and 78 eggs were used for the analysis of the shell. For embryonic development, the series was established according to the total length of the body. We established 40 embryonic stages from the primitive streak. In the early stages, the external morphological features are the C-shaped body, the maxillary, and mandibular fusion processes with the frontal process and the fusion of the forelimb with the digital plate. In the middle stages, the eyelid appears, and there are claws on the toes, cornification of fingers, and the onset of pigmentation. The last stage of embryonic development is characterized by the beginning of the formation of the scales, appear the toenails, and finalize the entire pigmentation. Regarding the relationship that exists with the ultrastructure of the egg during development, it was possible to observe a marked change in the composition of the shell and well-marked compaction during embryonic development, which may be related to the transport of calcium during embryonic ossification. Our results allowed us to show the complete sequence of embryonic development, determining the laying stage for this species. It was possible to establish a relationship with the ultrastructure of the eggshell from the oviductal transit to the moment of hatching.

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Staging criteria for embryos of the spiny softshell turtle,Apalone spinifera(testudines: Trionychidae)

Cited by 41 publications

References 21 publications

Skeletal remodelling suggests the turtle's shell is not an evolutionary straitjacket

Skeletal remodelling suggests the turtle's shell is not an evolutionary straitjacket

Osteology and skeletal development of Apalone spinifera (Reptilia: Testudines: Trionychidae)

Ultrastructure of eggshell and embryological development ofSalvator merianae(Squamata: Teiidae)

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