Biology_of_Turtles

of the postcranial characters linked to the presence of armor, may be homoplasies. However, shared characters may be retained, and pareiasaurs arguably appear to be the closest relatives to the chelonians (Rieppel, 1996). Pareiasaurs (Gregory, 1946; Lee, 1993, 1996a, 1996b, 1997) are not unique candidates for ancestors of turtles. Procolophonids (Reisz & Laurin, 1991; Laurin & Reisz, 1995), captorhinids (Gaffney & McKenna, 1979), diapsids (crocodiles, lepidosauromorph diapsids) (de Braga & Rieppel, 1997; Hedges & Poling, 1999; Platz & Conlon, 1997; Rieppel, 1995, 2000; Rieppel & de Braga, 1996; Rieppel & Reisz, 1999; Zardoya & Meyer, 2001) have all been presented as possibilities but none are convincing for the following reasons:

1.Some theories are based on extant forms and many derived characters without taking into account the plesiomorphic states of the Triassic turtles and their evolution.

2.Some of them present plesiomorphic characters as derived states, implying unlikely reversions.

3.Some characters are considered as synapomorphies whereas they are not strictly homologous. The question of ancestry is therefore still debatable.

As in the evolution of birds, turtles probably followed a “narrow pathway” determined only by a small number of characters. For birds, flight was definitive; for turtles, the definitive character appears to be their structural protection. This definition has greatly impacted the design of the turtle body. It is difficult to understand the biological roles of all of the particular chelonian characters because several roles can often be played by a single, unique structure. This probably explains why a structure can persist when one of its roles, often the most evident, has disappeared during evolution. For turtles, shell initially provided protection against predators but today serves additional roles, such as providing a highly efficient hydrodynamic shape (e.g., Dermochelys) or even acting as a respiratory organ (some Tryonychidae; Davenport & Wong, 1992) under conditions when environmental physical conditions are constraining. The turtle body bauplan has shown great temporal stability and has offered a novel source of diversity.

5.2.2.2 Variation of the Basic Pattern within the Aquatic Environment

In spite of the constraints imposed by the basic pattern, chelonians show a wide adaptive radiation in terrestrial, semi-aquatic, and highly aquatic forms in fresh and marine waters. This adaptation to an aquatic life clearly appears at two levels of the body plan: the shell and the locomotor appendages. In general, changes correspond to an adaptation of the shell shape and modifications of the foreand hindlimbs as paddles and flippers that are efficient for swimming in the aquatic environment. Various studies have quantified the correlations associated with the transformations affecting the form of the shell together with the form of the pectoral and pelvic girdles and also the humerus and femur.

5.2.2.2.1 Modification of Shell Shape in Extant Turtles

We note that in water, an incomplete and reduced pedomorphic shell (Lapparent de Broin et al., 1996; Lapparent de Broin, 2000b) seems to be favored. However, considering the physical constraints of the aquatic environment (hydrostatic pressure and hydrodynamic forces), there is no clear relationship between a lighter shell and the aquatic life, except for the flattening of the shell, which is more hydrodynamically efficient. It is possible that the flattening associated with a more streamlined shape has sometimes been facilitated by pedomorphic lightening. Many aquatic forms have solid shells (e.g., Carettochelys), a secondarily strengthened armor with hard skin (cheloniid marine turtles, forms with fontanelles), or a mosaic of plates (Dermochelyidae), or secondary bony callosities (plastron of Trionychidae, Carettochelyidae) for protection. Additionally, the plastral buttresses remain well developed in many freshwater turtles. The shell, with pedomorphic fontanels and cartilaginous links between plastron and carapace or between pleural disc and peripheral border, is

cruciform plastron (Chelydridae, some fossil Kinosternidae, fossil Laurasiatic Carettocheyidae, Asiatic Cretaceous and Paleocene cryptodires). The elements of both types of adaptation combined to select the general pattern of the shell.

To better understand the effects of environment on turtle shell morphology, Claude et al. (2003) conducted a study of the Testudinoidea, the most taxonomically and ecologically diversified group. The results showed that mean shell size did not differ significantly between terrestrial and aquatic forms. However, the authors noted greater shell variation for the terrestrial forms; for instance, species living in rocky crevices have a strongly serrated carapace, whereas species living under leaf litter have a flat carapace. In comparison, box turtles, which live in forested areas and leaf litter, have domed shells with a hinged plastron to provide the animals with more complete protection (Feldman & Parham, 2002). Such variation was related to a more complex adaptive process in the terrestrial environment that provides multiple niches. The flat shell morphology of many aquatic forms, a design that enhances hydrodynamics, was considered to be more homogeneous and more functionally constrained than in the terrestrial environment (Figure 5.5).

5.2.2.2.2 Paddles and Flippers in Extant Turtles

Significant variations in limb morphology are seen in species specialized for particular types of aquatic life. Three types of swimming appendages have arisen:

•Small-footed paddles consisting of mobile digits bearing long claws and short webs (found in most freshwater turtles, with differing amounts of webbing between the digits of fore and hind feet)

•Long mobile digits connected by an expanded web with reduced claws (Trionychidae, Carettochelyidae)

•Long rigid flippers (anterior edge longer than posterior edge (Cheloniidae, Dermochelyidae)

These different structures classically correspond to three subpatterns: the semiaquatic forms, the highly aquatic freshwater forms, and the marine forms (Figure 5.6).

The semiaquatic pattern, occurring in numerous species in various lineages of turtles characterized by specific phylogenetic features (Table 5.1), seems the most difficult to define. The Emydidae, especially Trachemys scripta—listed as Pseudemys in Walker (1973) and Chrysemys scripta in Davenport et al. (1984)—is often chosen to exemplify it. In this pattern, the coracoid is approximately as long as the scapula, the angle between the scapula and acromion is 90°, and the femur is a little longer than the humerus. Protraction and abduction of the limbs are governed by powerful muscles, for example, at the forelimb, the common mass of the teres major and latissimus dorsi, the deltoideus, and the triceps brachii with a smaller scapular part. Both parts of the biceps act in humeral retraction and elbow flexion. The forearm extensors and flexors are all present and complex; however, the intrinsic muscles of the digits are less complex than in better swimmers such as the highly aquatic Trionychidae. In the hindlimb, the dorsal puboischiofemoralis internus and the ventral puboischiofemoralis externus, as well as the flexor tibialis, constitute powerful complexes of muscles, whereas the puboischiotibialis is vestigial or absent. The shank extensors and flexors are numerous and complex. The phalangeal formula is usually 2-3-3-3-3. All of the digits bear long claws, which are typically longer in males for use in courtship. There is some information on overall animal locomotor performance (Walker, 1962, 1963, 1973; Zug, 1971; Davenport et al., 1984; Wyneken, 1997). However, to date there has been no mechanical approach to the study as with some terrestrial forms (Van Leeuwen et al., 1981). Electromyographic data have been recently published (Earhart & Stein, 2000; Gillis & Blob, 2001; Stein, 2003).

The highly aquatic pattern is characterized by the more elaborate paddles (Zug, 1971; Walker, 1973) of the Trionychidae. In the pectoral girdle, the dorsal scapula and ventral acromion form an angle of approximately 65°, whereas the coracoid is elongated. At the pelvic girdle, the pectineal

5 1

4 3 2

5

4

3 2 1

5 1

2

4

5

2

4

3

Figure 5.6  Variation of the limbs in extant turtles. From top to bottom: an extant terrestrial testudinid, a freshwater form, a highly aquatic trionychid, a highly aquatic carettochelid, and a marine turtle. Some representation of the skeleton of the fore and the hind limbs illustrate the modification in a natatory paddle and a flipper. Numbers correspond to the different digits of both limbs. A circle underlines the forward displacement of the center of mass.

fingers. The fibers of the abductor digiti minimi and lumbricales enter the web, enabling greater control over web form. The lumbricales play the same role in the foot.

The elongated coracoid and the increasing area of attachment of associated muscles—including the supracoracoideus, coracobrachialis magnus, and biceps—seem to be clearly related to aquatic locomotion. However, the most important features concern the structure and the functioning of the paddles. The complex relationship and division of the extensors and flexors of the forearm, and especially the hand, suggest a great mobility of the digits and an accurate movement of each of them in the paddle. To assume this movement, muscles have changed their orientations and insertion points to connect new areas.

The case of Carettochelys, the only non-marine turtle with true flippers, merits special consideration. According to previous descriptions (Waite, 1905; Walther, 1921; Pritchard, 1979), the animal has hypertrophied forelimbs used synchronously to swim by flapping as occurs in extant sea turtles. However, the flippers show a structure comparable with that of the flippers of Trionychidae, despite some modifications, mainly of the humerus, similar to marine forms. Although Carettochelys undoubtedly demonstrates synchronized flapping of its flippers, there appears to be no convincing demonstration yet that this flapping results in lift-based rather than drag-based

Table 5.1a

Examples of Structural Features Characterizing Different Extant or Fossil Species Possessing Distinct Habitats in Terrestrial or Aquatic Environments: Summary of Characters Implicated in Locomotion*

112 Biology of Turtles

Table 5.1a (continued)

Examples of Structural Features Characterizing Different Extant or Fossil Species Possessing Distinct Habitats in Terrestrial or Aquatic Environments: Summary of Characters Implicated in Locomotion*

Table 5.1b

Examples of Structural Features Characterizing Different Extant or Fossil Species Possessing Distinct Habitats in Terrestrial or Aquatic Environments: Summary of Characters Implicated in Locomotion*

114 Biology of Turtles

Table 5.1b (continued)

Examples of Structural Features Characterizing Different Extant or Fossil Species Possessing Distinct Habitats in Terrestrial or Aquatic Environments: Summary of Characters Implicated in Locomotion*

Notice the problem of homology of the alleged “hooked fifth metatarsal” in Chelonii, here considered as a element of the tarsus; see text for more discussion of this issue. In Erymnochelys, the autopod 5 has one independent quadrangular, flattened and hooked in T tarsal element as in other turtles with a “hooked tarsal,” besides one metatarsal and three phalanges; the hooked bone cannot be a tarso-metatarsal element. As in all the other turtles, the element following the hooked bone of the finger 5 has the typical morphology of a metatarsal and not of a phalange. In Cheloniidae, there is a semihooked tarsal 5 and a flattened and expanded metatarsal 1. Carapace: terrestrial type, ■; aquatic type, summary of hydrodynamic characters of the shell, ▼ (1, flattened shell; 2, oblong shell by anterior protrusion (a) and posterior sharpened extremity (b), 3, cordiform, 4, enlarged surface of the shell and raising posterior edges, 5, smooth surface, 6, carinated shell with oriented ridges (s), 7, elastic skinned edges. Facilitation of rowing movements: ●, cruciform plastron giving space for limb musculature.

propulsion. Interestingly, members of the Trionychidae sometimes show brief bursts of synchronized forelimb movement when digging in sediment (Davenport, unpublished).

The marine pattern of extant turtles (Hirayama, 1994; Hirayama & Chitoku, 1996; Manlius, 1996; Walker, 1973), the Cheloniidae and Dermochelyidae, is characterized by forelimbs modified into wing-like rigid flippers and hindlimbs into semi-rigid paddles or rudders. In contrast to the selection of a large flexible skinned surface with mobile digits, as in the Trionychidae, the coracoid is elongated in relation to a powerful locomotor musculature and an angle greater than 90° exists between acromion and scapula. The rigidity of the flippers stems from a loss of joint mobility in the digits and metapodial elements, and an associated reduction, loss, or replacement of muscular units of the hand and foot by connective tissue (fascialization). In the pelvic girdle, the pectineal process of the pubis is exceptionally large. The humerus is stouter and flatter than in non-marine taxa, with a proximally shifted ulnar process. The intertrochanteric fossa is reduced by displacement of the deltoid crest toward the opposite trochanter. The three central digits in the foreflipper are greatly elongated by increasing the length of the metacarpals and phalanges rather than by hyperphalangy. An enlarged pisiform supports the ulnar border of the flipper. The femur, which is similar in length to the humerus, is flat, as are the tibia and fibula. The intertrochanteric fossa also is reduced.

As in the other aquatic turtles, the muscles, latissimus dorsi, subscapularis, pectoralis, and supracoracoideus are large but in marine turtles the deltoideus scapularis and coracobrachialis magnus are also enlarged. The flexors of the elbow and hand are well developed, except the flexor brevis superficialis and the lumbricales. The adductors of the fingers are absent. The supinator manus is vestigial, the extensores radialis profundus are absent, and the extensor digitorum communis is distally reduced to a connective tissue fascia. At the hindlimb, parts of the puboischiofemoralis show a more extensive origin, whereas units of the shank and foot are reduced to a fascia (extensor digitorum communis) or are absent (flexor digitorum communis sublimis) (Manlius, 1996; Walker, 1973; Wyneken, 2001, 2003).

5.2.2.2.3 Structure of the Posterior Zeugopod: The Hooked Fifth Tarso-metatarsus or Fifth Tarsus

Chelonians are characterized by the presence of a hooked bone at the angle of the foot. There is some debate about whether there is a homologous bone equivalent found in other reptiles (Guibé, 1970; Romer, 1956; Schaeffer, 1941; Rieppel & Reisz, 1999). The hooked bone is considered to be the fusion of either tarsal 4 and tarsal 5 (a hooked tarsal), or tarsal 5 with metatarsal 5 (Romer, 1956; Schaeffer, 1941; Rieppel & Reisz, 1999). It is apparently also present in some Squamata and all crocodiles. Its ontogenetic formation and morphology have not been adequately studied in any group where it is present. This bone is not similar morphologically across the different groups of reptiles where it appears. In crocodilians, it is a long bone that resembles a metatarsal curved slightly proximally. In turtles, there are considerable differences in shape: it can either be a rectangular bone with a small prolongation in the middle of the distal face, articulating with a bone similar in shape to the metatarsal, or it may be a more quadratic bone. Its homology, ontogenetically and morphologically, is not known and will have to be studied employing a cladistic approach, including every form with and without a hooked bone and considering its shape. In terms of its role in locomotion, it appears to act as a pisiform-like bone that supports the back of the foot and increases the surface area of the limb. The bone that distally articulates with the “hooked bone” has clearly a metatarsal and not a phalange shape. Besides, fossil taxa such as Eurysternids (Figure 5.6) and extant forms such as the pleurodiran Erymnochelys (Table 5.1) clearly present a rather quadratic hooked bone, distally followed by four bones, a metatarsal, and three phalanges.

5.2.2.2.4 Shells and Limbs in Aquatic Fossils

The fossils of Trionychidae and Carettochelyidae had limbs with elongation and flattening of wellarticulated elements, phalangeal multiplication, and reduction in the number of claws. Similarly, new anatomical developments are seen in other fossil forms. The late Jurassic families of littoral turtles, especially the Plesiochelyidae, Thalassemydidae, and Eurysternidae, which spread into the European seas, were primarily characterized by a flattened or carinated shell with a relatively light dermal skeleton, pedomorphic in the two latter families (Lapparent de Broin et al., 1996; Lapparent de Broin 2000b; see the various processes of pedomorphosis in Kordikova, 2000). The autopods were enlarged, when known—i.e., in the Eurysternidae. The radius was curved and longer than the ulna. Digits two to five were particularly elongated, producing a small paddle, but they still retained distinct mobile finger and toe elements, as well as inter-digital webbing. The hindlimb was longer than the forelimb primitively. Eurysternidae, especially known by their skull (Solnhofia group: Lapparent de Broin, 2001), are characterized—as in marine turtles—by a descending parietal process much reduced in length and inferiorly notched, at the rear of the inter-orbital foramen. This notch is thought to have housed hypertrophied lachrymal glands adapted for salt excretion (Hirayama, 1998). This feature could conceivably have been acquired in a non-marine hypersaline environment, such as a tropical lagoon subject to evaporation, and subsequently proved appropriate to life in the marine environment. In the second wave of “marine” cryptodires, early Cretaceous Santanachelys (Protostegidae from the freshwater lake of Araripe) had the same skull notch particularity and similar limb characters as the Eurysternid European forms (Figure 5.7). However, a