Encyclopedia of Animal Cognition and Behavior

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Testudines Morphology

  • Larissa Ferreira-Cunha
  • Angele MartinsEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-47829-6_1437-1

What Are the “Testudines”?

Testudines (also known as chelonians) is an order composed of about 300 reptile species popularly known as turtles, tortoises, and terrapins that can occupy a wide variety of ecological niches, from marine and freshwater to terrestrial environments (Uetz et al. 2019; Ernst and Barbour 1989; Fig. 1).
Fig. 1

Examples of the morphological diversity in Testudines: Terrapins (ad), tortoises (e, f) and turtles (g). Figures (ae): Roberto Murta/Bicho do Mato; Figure (f): Camila Mattedi

Such animals exhibit a combination of ancestral and extremely specialized features that are exclusive to the individuals belonging to this order (Pough et al. 2018). Distinctive chelonian characteristics are the presence of a shell composed by the carapace (upper part of the shell; Fig. 2a), plastron (lower part of the shell, Fig. 2b), and the location of the shoulder girdle within the rib cage. Such characters are well developed even in the earliest known turtles (Renous et al. 2008).
Fig. 2

Schematic illustration of the carapace (a) and plastron (b) of Chelonia mydas

The chelonian skull is a highly modified structure: typically rather broad and flat and greatly expanded behind the eye area but with a short and narrow facial region (Fig. 3). Additionally, the skull is akinetic, i.e., it does not present any area where the bones articulate (=move) among themselves; the pterygoids (bones associated to the upper part of the skull) are solidly fused to the braincase, and the highly developed and peculiar quadrate is tightly bound to a great lateral expansion of the optic capsule. The temporal roof does not present any opening (also known as fenestra) but is generally emarginated from behind or below or both. Teeth are lost and have been replaced functionally by a horny bill (Romer 1956).
Fig. 3

Skull of Caretta caretta in dorsal (a), lateral (b), and ventral (c) views illustrating the absence of skull openings (temporal fenestrae) and teeth

The vertebral number is nearly invariable in chelonians, with all living turtles having eight cervical vertebrae. Cervical ribs (when present) are rudimentary and confined to the posteriormost vertebrae. The trunk has ten dorsal vertebrae with the first and last attached but not fused to the carapace and the middle eight firmly fused or co-ossified with the neural bones of the carapace. The two sacral vertebrae link the pelvic girdle to the vertebral column by short and stout ribs. The caudal vertebrae number is variable but usually less than 24 in most species. The trunk ribs extend outward and fuse with the costal bones of the outer shell. Both elongation and shortening of the neck vertebrae result in distinct neck lengths among chelonians (Vitt and Caldwell 2009).

As in other reptiles, the divisions of the dorsal and ventral group of trunk muscles (epaxial and hypaxial) are not evident and are reduced to fit organs within the shell. In contrast, appendicular, head, and neck muscles are extremely well developed (Vitt and Caldwell 2009; Kardong 2014). The limb structure of turtles is highly variable, reflecting the environment and locomotory modes of the species (Fig. 4). For instance, marine species and the freshwater Carettochelys have well-developed flippers with extremely elongated digits that do not move independently (Fig. 4a). Most aquatic species have well-developed webbing between the digits, which still retain some independent mobility (Fig. 4b). Terrestrial chelonians (i.e., tortoises) usually have stout limbs capable of lifting their heavy bodies off the substrate but are obviously ineffective for swimming (Fig. 4c). Their digits are usually reduced, and the feet are equipped with thick pads (Pough et al. 2004).
Fig. 4

Examples of different limb structures exhibited by Testudines. (a) Sea turtle flipper in adaptation to strictly marine environments; (b) terrapin flipper exhibiting webbing between digits in adaptation to aquatic environments but capable of climbing in river rocks; (c) stout limb of a tortoise, in adaptation to terrestrial environment

Additionally, the Testudines share a series of characteristics with several fossil groups, such as a distinctive ear region wherein the eardrum is supported by the squamosal (rather than by the quadrate) and by the retroarticular process, a backward projection of the lower jaw. Further, the foot is unique in the way the digits articulate with the ankle bones (Kardong 2014). Although there has been a wide debate on the origin of the modified anapsid skull, its features associated to the shell and post-cranial skeleton are unique among all known vertebrates (Pough et al. 2018).

Cryptodira X Pleurodira

Extant chelonians belong to two lineages, which are mainly distinct in relation to the mode of neck retraction into the carapace: Cryptodira and Pleurodira (Herrel et al. 2008). Cryptodira represents the most diverse group of hidden-neck turtles found throughout the temperate and tropical regions of the world (Moustakas-Verho et al. 2017), exhibiting an S-neck retraction (vertical plane) inside the shell. Pleurodirans are known as side-necked turtles, with a lateral retraction (horizontal plane), with distribution occurring mostly along the Southern Hemisphere (Herrel et al. 2008; Moustakas-Verho et al. 2017). Pleurodires have a specialized cervical vertebrae (CV) anatomy with the CV5-CV6 articulation being the major point of flexure in neck retraction what reflects a key point for the evolution of Pleurodira (Mariani and Romano 2015). This specialization guarantees them a longer neck, improving performance in the capture of mobile food in the water (Herrel et al. 2008).

In addition to differences in the neck, cryptodires possess an ancestral musculoskeletal morphology, with most hip muscles originating on the pelvic girdle. In these species, the pelvic girdle is not fused to the shell. In contrast, pleurodires exhibit a derived morphology, in which fusion of the pelvic girdle to the shell is present and has resulted in shifts in the origin of most hip muscles onto the interior of the shell (Mayerl et al. 2017). Moreover, skulls may vary in size and shape, mostly regarding their jaw architecture and musculature, with pleurodires usually exhibiting flatter and broader skulls. Such an architecture might have allowed the evolution of gape-and-suck mode of feeding, which is present in several South American species such as the matamata (Chelus fimbriatus).

The Turtle Shell

The body of extant turtles is well known because of their distinct shape in relation to other tetrapods. It is composed by their shell, which is variously modified to provide protection from predators, shelter from the environment, enhance thermoregulation, and act as a rich reservoir of fats, minerals, and water. By enabling extensive concealment of extremities, shell-closing systems deter potential predators and promote survival both on land and in shallow water (Nagashima et al. 2012; Cordero 2017; Cordero et al. 2018). While the tortoise shells are very often high and domed – possibly as an adaptation to hamper predation – aquatic turtles usually bear streamlined shells (mostly for swimmers), although some shells may be less streamlined often with ridge carapaces to assist camouflage (mostly for species that are bottom-walkers).

The turtle bony armor has apparently originated independently many times in reptilian evolution, but the chelonian type of armor has appeared only once (Zug 1971), with this turtle-specific arrangement having persisted over the last 210 million years (Lyson and Joyce 2012). However, the turtle shell is an evolutionary innovation that has been a mystery for evolutionary biology (Ferreira 2016), with its homologies being debated since at least the nineteenth century (Moustakas-Verho et al. 2017). Many biologists have for long claimed that the turtle shell takes shape from skin cells adjacent to the ribs that are transformed into bone in the course of development. However, Japanese developmental biologists have recently suggested that the shell is most likely a direct outgrowth of bones themselves (Lubick 2013). Additionally, extraordinary fossil discoveries indicate that terrestrial early turtle-like reptiles exhibit transitional features that eventually gave rise to the fully shelled Proganochelys. Turtle-like fossils, such as Eunotosaurus (260 million years old), Pappochelys (240 million years old) and Odontochelys (220 million years old) suggest that the ventral shell elements evolved first, followed by broadened ribs that eventually gave rise to the fully hardened dorsal shell. This has recently led to the intriguing hypothesis that the incipient shell might have evolved as an adaptation to life underground, rather than, as traditionally thought, an anti-predator defense. Moreover, other distinctive turtle skull and limb traits were distinct in these fossils (Cordero 2017).

The carapace is formed from costal bones fused with ribs, neural bones fused with thoracic vertebrae, peripheral bones, and an anterior nuchal bone, covered by keratinized epidermal shields (Burke 1989; Moustakas-Verho et al. 2017). Developmental evidence and muscular attachments suggest that the nuchal bone is derived from the cleithra of the ancestral tetrapod pectoral girdle (Gilbert et al. 2001).

The plastron is the order-defining skeletal structure for turtles (Rice et al. 2016) formed from the suturing together of an entoplastron (interclavicle), epiplastra (clavicles), and three to five paired bones (Moustakas-Verho et al. 2017). The absence of the ventral portion of the ribs and the sternum suggests that plastron assumed their role (Rice et al. 2016). There are a few hypotheses the plastral bones of turtles and the gastralia of other tetrapods are homologous (Gilbert et al. 2001), but such suggestion has still been a debate over the years.

The dorsal and ventral armor are covered by a keratinized epithelium, and two epithelial appendages might be present in the turtle shell: scutes (large epidermal shields separated by furrows and forming a unique mosaic) and tubercles (numerous small epidermal bumps located on the carapaces of some species). Recent studies have suggested the scute of the turtle shell as an evolutionary novelty, whereas tubercles are homologous to reptilian scales (Moustakas-Verho and Cherepanov 2015).

Although the body structure is the same in all individuals, the shell morphology varies according to habits of each species (e.g., flat shells are more hydrodynamic, which may justify their presence in aquatic turtles). In addition, the interspecific shape variation in terrestrial turtles is greater than in aquatic species (Claude et al. 2003). This type of variability can be explained by the complexity of the adaptive landscape in terrestrial environments in relation to aquatic ones, providing multiple niches (Schluter 1986). Additionally, turtle species can often be recognized by the tessellation and pigmentation of scutes on their shell, and scutes have been independently lost or reduced in certain freshwater and marine taxa (Moustakas-Verho et al. 2017).

Modifications and Adaptations to an Enclosed Body

Diversification of the turtle shell comprises remarkable phenotypic transformations, mostly regarding their internal visceral organization, locomotor apparatus, neck region, and copulatory mechanism (Cordero et al. 2018). For instance, internal muscle connections and limb articulations were modified during the repeated evolution of shell kinesis in small-bodied terrestrial or semiaquatic turtles, as well as modifications of the limbs in terrestrial species (tortoises). Also, change in the muscles that enable lung function was necessary to accommodate early steps in the evolution of the shell.

The location of the heart varies within reptilian lineages and even within taxa, although the heart tends to be positioned roughly along the axial midline. In chelonians, part of the heart is often deep to margins of the humeral and pectoral scutes; however, in some species, it is positioned more posteriorly along the midline between humeral-pectoral and pectoral-abdominal scute lines. The heart was repositioned during the evolution of soft-shell turtles, being relatively displaced to the right, and typically just caudal to the level of the acromion processes and cranial to the distal procoracoid process – procoracoid cartilage junction (Wyneken 2009; Cordero 2017).

Changes in the muscles that enable lung function were also necessary to accommodate early steps in the evolution of the shell. As most tetrapods inhale by ribs expansion (aided by muscle functions), incorporation of the ribs into the turtle shell negates the costal movements that effect lung ventilation in other air-breathing amniotes. Recent studies have indicated that the early stem lineage of turtles deviated from the basal amniote body plan (in which locomotion and breathing are coupled) and evolved a division of function in which the ribs took on a stabilizing role, whereas the abdominal muscles became specialized to ventilate the lungs. Instead, turtles have a unique abdominal muscle-based ventilatory apparatus which most likely evolved through a division of labor between the ribs and muscles of the trunk in which the abdominal muscles took on the primary ventilatory function, whereas the broadened ribs became the primary means of stabilizing the trunk. These changes occurred approximately 50 million years before the evolution of the fully ossified shell (Lyson et al. 2014).

The independent evolution of the carapace and plastron also required several musculoskeletal changes such as muscle modification, shortening of the trunk, widening of the ribs, encapsulation of the ventral scapula into the chest, loss of intercostal muscles, and reorganization of the respiratory muscles (Rice et al. 2016). For instance, internal muscle connections and limb articulations were modified during the repeated evolution of shell kinesis in small-bodied terrestrial or semiaquatic turtles. Moreover, the evolution of jumbo-sized shells was accompanied by modifications of the limbs in terrestrial species (Cordero 2017). Additional particular characteristic of the chelonians is the location of the girdles within the rib cage. The pectoral girdle is composed of a long scapula, an acromion process, and a coracoid process differing them to the other tetrapods (Renous et al. 2008).

Conclusion

Chelonians have evolved a novel generalized structural body plan with unique functional mechanisms which guaranteed their evolutionary success along about 220 million of years. The turtle shell provides defense, shelter, and physiological balance, and their distinct enclosed body has resulted in several modifications in the axial skeleton, appendages and appendicular muscles, as well as visceral topography. Even though several issues regarding chelonians evolutionary history are still under debate, this group has carried specialization a long way and without doubt to the greatest extreme of any of the chordates.

Cross-References

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Departamento de Vertebrados, Museu NacionalUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Laboratório de Anatomia Comparativa de Vertebrados, Departamento de Ciências Fisiológicas, Instituto de Ciências Biológicas, Campus Darcy RibeiroUniversidade de BrasíliaBrasiliaBrazil

Section editors and affiliations

  • Marieke Cassia Gartner
    • 1
  1. 1.Zoo AtlantaAtlantaUSA