Biology_of_Turtles

B

Figure 5.7  Structure of the fore (A) and hind (B) limb of Eurysternum wagleri, Aff. Solnhofia sp. (C) and Idiochelys fitzingeri (D) giving an idea of the Jurassic turtles of Cerin (France) living in aquatic conditions. Prints of webs are often visible between and around the digits suggesting the existence of paddles. (With thanks to R. Alberdsdörfer, H.V. Karl, and M. Maisch for their images and material, in particular for the unpublished Eurysternids from the Jurassic of Bavaria from the private collection of R. Albersdörfer.)

proportion of the fingers were still mobile and allowed articulations (Hay, 1908) but the others were flattened and immobile, having lost the ability to articulate, as is the case in modern marine turtle flippers. Santanachelys also had a flattened and lighter shell with a long bridge but with a protruded anterodorsal part, probably facilitating more extensive movement of the forelimbs. However, the littoral Neusticemys (skull unknown), a possible first protostegid from the late Jurassic of Argentina, already had a similar carapace and also an elongated forelimb (longer than the hindlimb) and flattened fingers with completely reduced articulations.

The complete transformation of the limbs into flippers in marine turtles occurred during the late Cretaceous. This modification included many other changes: the forelimb became much longer than the hindlimb, the humerus was flattened with an elongated ulnar trochanter, and the position of the deltopectoral crest was modified, becoming anteriorly directed. There was torsion of the elongated radius, flattened fingers that lost articulations between the elements, elongated fingers (particularly 2 to 4), reduction of the claws, skin enveloping all the limbs, and modification of the pectoral girdle (elongated coracoid, obtuse angle between scapula and acromion, and so on). In Cheloniidae, the deltopectoral crest is still linked to the humerus condyle, whereas in Dermochelyidae that link is lost and the crest develops transversely and the distal extremity is more expanded and widened; the flippers are much longer relative to other marine turtle species.

For comparison, it is interesting to consider the structural features of the Testudinidae, the single exclusively terrestrial turtle group. The structural pattern of these species includes a rather domed shell and more or less elephantine features of the short foreand hindlimbs. In particular, the short forelimb results from reduced lengths of the carpus and fingers segments, and also a reduction of the phalangeal formula (2-2-2-2-2 or 1), whereas the hindlimbs have short yet massive toes, the phalangeal formula being 2-2-2-2. There is no connecting web of tissue between the digits, which bear heavy claws. Proximally on the humerus, the length of the intertrochanteric fossa is longer, whereas on the femur the ventral fusion of the trochanters translates into smaller size and the depth of the intertrochanteric fossa. Concerning the locomotor muscles, these forms exhibit a reduced development of the pectoralis, a single biceps, a loss of pronator profundus, and a clear division of the extensor carpi radialis at the forelimb. Walker (1973) proposed that this last feature facilitates the placement of the hand in a dorsi-flexed position without a simultaneous extension of

the forearm. At the pelvis, the flexor tibialis complex is reduced to a single muscle. Reduction of the extrinsic muscles of the forelimb (flexor brevis superficialis, abductors of the fist and fifth digits, adductor digiti minimi, and lumbricales) and the hindlimb (flexor digitorum communis sublimis) suggests weak independent action of the fingers.

5.2.2.2.5 The Geometric Morphometry of the Shoulder Girdle and Humerus

Morphological traits of the limbs can be used to distinguish morphofunctional groups of turtles. Recently, geometrical morphometry based on the Procrustes method (Bookstein, 1991; Penin, 2003; Penin et al., 2002; Berge & Penin, 2004) was used to analyze the size and shape variations of two skeletal elements (the humerus from 69 species of 11 extant and 2 extinct families, and the shoulder girdle from 57 species of 13 families of extant adults specimens) and to understand the relationships of these structures aquatic and terrestrial locomotor adaptations (Depecker et al., 2006a, 2006b). According to Bookstein’s method (1991), 21 reference marks were placed on the humerus and 16 reference marks on the pectoral girdle (Figure 5.8). The data for the shoulder girdle (Depecker et al., 2006a) reveal that the first two principal components axes of Principal Component Analyses (PCA) represent 73.2% of the total variance. They allow the identification of four main groups, independent of size (Figure 5.9A):

Extant terrestrial turtles (Testudinidae)

Eight families of freshwater turtles (Geoemydidae or Bataguridae, Chelidae, Chelydridae, Emydidae, Kinisternidae, Pelomedusidae, Platysternidae and Podocnemididae)

Two other families of freshwater turtles (Carettochelyidae and Trionychidae) Two families of marine turtles (Cheloniidae and Dermochelyidae).

Data for the humerus (the first two principal components of PCA representing 51.2% of the total variance) also reveal similar distinct groups (Depecker et al., 2006b) (Figure 5.9B):

The extant terrestrial Testudinidae, including the supposed terrestrial fossil Ptychogaster The same eight families of freshwater turtles

The extant, highly aquatic, Trionychidae and the terrestrial fossil Meiolaniidae The extant highly aquatic Carettochelyidae

The Cheloniidae The Dermochelyidae

Figure 5.8  Position of 16 landmarks on the right shoulder girdle, dorsal posterior view (a) and lateral view (b), and 21 on the right humerus, ventral view (c) and dorsal view (d) in a semi-aquatic freshwater turtle (Chelydra serpentina). a, acromial process; co, coracoid; ef, ectepicondylar foramen; gl, glenoid cavity; hh, humeral head; hs, humeral shaft; sc, scapular prong; rc, radial condyle; tch, trochlee; tmaj, trochanter major; tmin, trochanter minor; uc, ulnar condyle (used with permission from Depecker et al., 2006a, 2006b).

IV

PC2

A F

D E PC1

B C

Figure 5.9  Principal Component Analyses of 88 shoulder girdles (top graph) and 122 humerus (bottom graph) onto the plane of the first principal component PC1 and PC2. Pleurodira and Cryptodira are not distinguished in the analysis. Filled circles correspond to groups I (top) and A (bottom) (Testudinidae). Open squares correspond to groups II (top) and B (bottom) (Emydidae, Geoemydidae or Bataguridae, Chelydridae, Platysternidae, Kinosternidae, Chelidae, Pelomedusidae, Podocnemididae). Filled squares correspond to group III (top) (Trionychidae and Carettochelidae) and the groups C (bottom) (Trionychidae and Meiolaniidae), D (bottom) (Carettochelyidae). Open triangles correspond to group IV (top) (Cheloniidae and Dermochelyidae) and groups E (bottom) (Cheloniidae) and F (bottom) (Dermochelyidae). Dorsal views of line diagrams of the humerus for the two extremities of PC1 and PC2 are presented. The line diagram of the shoulder girdle also changes along PC1 and PC2 (solid lines) with respect to the consensus (mean shape) in dotted line (used with permission from Depecker et al., 2006a, 2006b).

Based on a multivariate regression performed to calculate the correlation between humerus shape and the degree of specialization to aquatic habitat, the authors demonstrated relatively few differences in shape between terrestrial and semiaquatic turtles but greater differences between them and truly aquatic turtle species (Figure 5.10). In this latter group, the humerus shape (including robustness, larger and dorsoventrally flattered shaft, proximally developed medial trochanter, distally developed lateral trochanter, laterally enlarged radial condyle) appears directly related to the constraints associated with the group’s specific environments or habitats.

It is generally acknowledged that modern terrestrial and marine turtles may have evolved independently from less-specialized freshwater turtles (Gaffney, 1985; Gaffney & Meylan, 1988; Gaffney et al., 1991; Shaffer et al., 1997). For this reason, the authors used these freshwater turtles as a

Figure 5.10  Correlation between shape changes of the humerus (Vreg) and specialization for the aquatic habitat (aquatic gradient). Curve formula: y = 0.0144x2 + 0.0032x – 0.0377 (R2 = 0.81) Symbols are the same as in Figure 5.9. Ventral, dorsal, and lateral views of line diagrams of the humerus between both extremities of Vreg: dashed lines, semiaquatic turtles; full lines, marine turtles. Shape changes observed: a, longer humerus; b, larger shaft; c, flatter shaft; d, developed trochanter major; e, distal trochanter minor; f, enlarged radial condyle (used with permission from Depecker et al., 2006).

reference to analyze the shape of the shoulder girdle for each group of terrestrial and marine turtles (Figure 5.11). Unlike semiaquatic freshwater turtles, terrestrial forms exhibit a more massive girdle with a larger glenoid cavity, a wider angle between scapula and acromial process, a longer scapula (vertically oriented), and a shorter and broader (medially longer) coracoid. The highly aquatic freshwater turtles exhibit a more developed pectoral girdle ventrally (coracoid and acromial process) relative to the dorsal scapula. The coracoid is longer, broader, and more curved. The scapula is shorter, forming an acute angle with the acromial process. Comparatively, the marine turtles show a more massive girdle. The coracoid, which has a straight posterior border, is longer, whereas the acromial process and the scapula are shorter. The scapula forms an obtuse angle with the acromial process. The shoulders of terrestrial and marine turtles appear to be highly specialized. Large freshwater species such as the trionychids and carettochelyids also have a specialized pattern that is reminiscent of marine turtles.

Allometric investigation has showed that the shape of the shoulder girdle gradually changes with size: the coracoid becomes proportionally longer, whereas the scapula and the acromial process become proportionally shorter (Figure 5.12). The smallest turtle species occur among the terrestrial forms and the generalized freshwater turtles, whereas the largest species are terrestrial and marine turtles. The largest highly aquatic freshwater turtles (Pelochelys, some trionychine species) are the same size as the smallest marine turtles (Lepidochelys). When size increases, the coracoid becomes longer in marine turtles and both longer and broader in highly aquatic freshwater turtles.

Locomotor adaptations of aquatic and terrestrial species could explain these distinct groups. On land, the limbs must provide both support and propulsion (Williams, 1981). They act like beams to support the weight of the shell (Walker, 1962, 1971a, 1973). Jayes and Alexander (1980) and Van Leeuwen et al. (1981) noted that the vertical components of muscular forces in walking must be much larger than the horizontal components to counterbalance body weight. In contrast, for aquatic turtles the girdles do not play a supporting role, whereas propulsive forces are generated by the limbs acting against the water. The streamlined shape of the body of marine turtles is associated with hypertrophied flapping forelimbs that give an advantage in terms of locomotor efficiency

Figure 5.11  Discriminant traits of the shoulder girdle (dorsal posterior view), the semiaquatic freshwater turtles (dotted lines) being used as a reference to compare with other groups (solid lines), terrestrial forms (a) highly aquatic freshwater forms (b) and marine turtles (c). The shape and the orientation of the girdle are also given in relation to the shape of the shell (frontal view) in the same categories of turtles. The numbers indicate selected remarkable landmarks: 1 and 2, respectively medial anterior and posterior angles of the coracoid; 3 and 4, posterior border of the coracoid at maximal curvature and collar; 11, medial dorsal angle of the scapular prong; 12, limit between scapula and acromial process; 13 and 14, respectively medial anterior and posterior angles of the acromial process (used with permission from Depecker et al., 2006).

(Davenport et al., 1984). Walker (1973) suggested that there is a relationship between the shape of the shoulder girdle and the configuration of the turtle shell. Aquatic turtles possess a long coracoid, which gives them a mechanical advantage in swimming in terms of lever arms and muscular attachments. In this case, pectoral morphology is directly linked to the streamlined shape of the shell (Figure 5.11). In terms of terrestrial turtles, the humerus of an extinct member of the Meiolaniidae (representing a primary adaptation, i.e., the primary condition) is distinct from those of the Testudinidae, that represent a secondary return to terrestrial lifestyle from freshwater ancestors.

5.3Locomotion of the Aquatic Turtles

A highly specific structure, the turtle shell generates biomechanical limitations to the physical constraints of the terrestrial and aquatic environments and to body functioning. The inflexibility of the body axis obliges the turtles to use limb movements alone for propulsion. Significant variations in limb morphology are found in species that are specialized for particular patterns of locomotion (Walker, 1973). Shell mass and body geometry play an important role on land and also in shallow water. To demonstrate the importance of weight, Zani and Claussen (1995) experimented with increased extrinsic loads; they found a correlation between increased loads and a decrease of speed and stride length during terrestrial locomotion. However, weight and size are generally not limiting factors at sea and are probably favorable to other functions, such as high fecundity, gigantothermy, prolonged diving, oxygen storage, and resistance to heat loss (James et al., 2006). The greater

Figure 5.12  Allometric shape vectors calculated in all turtles Va1 (a), in terrestrial turtles Va2 (b), Va3 in highly aquatic freshwater turtles (c), in marine turtles Va4 (d). CS, centroid size; the groups I, II, III, and IV correspond to the graph A of Figure 5.9. Line diagrams corresponding to each graph show the variation between the smallest specimens (dotted lines) and the largest (solid lines) ones (used with permission from Depecker et al., 2006).

absolute body size of marine turtles could incorporate a larger pectoral musculature that is able to generate a greater swimming power. For this reason, the forward displacement of the center of mass, functionally related to stable swimming in freshwater aquatic turtles, becomes even more marked in the marine turtles (Davenport et al., 1984). Finally, as reported by Sukhanov (1974) it is important to note that some aquatic turtles, such as Platysternon or Chelus, do not swim well but often move on the bottom of lakes, streams, and so on. In addition, terrestrial as well as aquatic turtles (e.g., bottom-walkers like Chelydridae and Kinosternidae) walk on land, and the highly aquatic Apalone, for example, is able to cover large distances on land. The speed of progression varies from 0.2 kph (Gopherus, Clemmys) to 1.7 kph (Chrysemys) and 3.2 kph (Chelonoidis nigra of Galapagos) in relationship to the body size.

5.3.1Different Function of the Limbs

In water, the mechanics of thrust production by vertebrates varies markedly among different groups (Fish, 1996). One general approach corresponds to a typically asynchronous rowing action (limbs oriented in a horizontal plane), where the limbs use the water resistance to generate thrust by a retraction action or a paddling (limbs oriented in a vertical parasagittal plane). During rowing, retraction corresponds to a power phase of a cyclic movement in which protraction is the recovery phase. The power phase generates a large pressure drag that provides anterior thrust by reaction of the water (Figure 5.13). For this reason, some authors use the expression “drag-based propulsion” to characterize this system (Davenport et al., 1984; Fish, 1996; Wyneken, 1997). For maximum efficiency, there must be a maximum extension of area (by abduction of the digits and web extension) during the power phase. All anatomical structures that augment paddle area contribute to greater mechanical efficiency (for example, enlargement of fingers, flattening of claws, interdigital webbing, and so on). Conversely, the recovery phase—which repositions the limb—must ideally be a non-thrust generating stage. To avoid or to limit drag production during recovery, the paddles benefit from an adduction of the digits to reduce the total area, and also a change in timing to temporarily reduce the relative limb velocity.

A second approach corresponds to a more typically derived synchronous swimming mode when a lift force is used to generate the thrust. The limb becomes a hydrofoil and lift-based thrust is produced by its oscillation at a controlled angle of attack (Figure 5.14) relative to the effective water flow over it (Davenport et al., 1984). To enhance the lift and decrease hydrodynamic drag, the angle of attack should be small enough to avoid separation of the water flow from the hydrofoil surface. However, thrust is the resultant of lift and drag forces on the hydrofoil. Broadly speaking, the greatest thrust will be produced before the hydrofoil stalls, when both lift and drag are high. Thrust may be generated either during a specific phase of the cycle movement of the hydrofoil (upstroke or downstroke) or continuously during its entire duration of the cycle according to the direction of the general movement of the limb, the direction of the flow, and the angle of attack. During non-thrust generating phases, the angle of attack is reduced close to zero, reducing both lift and drag. The efficiency of propulsion is also a function of the shape of the hydrofoil.

5.3.2Different Patterns of Propulsion

As a group, aquatic turtles use both types of mechanical systems. In extant forms, the limbs of freshwater animals show rowing strokes during slower swimming in semiaquatic species (Figure 5.13) as well as in the faster swimming of the highly aquatic Trionychidae. Movement of the limbs is characterized by dominant antero-posterior movements, combined with a rotation of the limb to become perpendicular to the water flow during the retraction phase that generates thrust but parallel to flow during protraction (recovery phase). Foreand hindlimbs show similar movements, but the studies of Zug (1971) and Walker (1973) indicate that the hindlimbs predominate in generating thrust. Comparative kinematics of the forelimb during the swimming of slider (Trachemys scripta)

Figure 5.14  Kinematics of the swimming of Dermochelys coriacea showing the trajectory of the forelimbs extremity during their dorso ventral flapping, which could generate lift and propulsive components. An example of the forces exchanged is indicated to illustrate the hydrofoil function of the limb and the production of the propulsive force. Numbers are stages of the coordinated limb movements (used with permission from Davenport, 1987).

turtles. We must expect a great diversity of limb rowing mechanisms—in terms of their efficiency— according to phylogenetic differences among the freshwater turtles. In the absence of information on the movement of the foreand hindlimbs in diverse species of turtles ranging from the semiaquatic to highly aquatic freshwater turtles, it is difficult to draw general conclusions on the diversity of patterns used for propulsion. The diagonal mode of limb coordination used in these animals might lead to expectations of an equivalent role of foreand hindlimbs in thrust production and thrust intensity. However, there is more extensive webbing between the toes of the hind feet relative to the forefeet (Walker, 1973) in emydid turtles, which spend time in both terrestrial and aquatic habitats (Gibbons, 1970; Bodie & Semlitsch, 2000), producing a broader paddle-like foot that has a predominant role in generating drag-based thrust in water (Pace et al., 2001). However, extensive webbing between the toes of front and rear limbs (Webb, 1962) in softshell turtles (Trionychidae) suggests that both hindand forelimbs are sources of drag-based thrust in water—although softshells often dig in soft mud when seeking prey, so the webbed forelimbs may have a dual function.

The role of the tail in turtle propulsion was studied by Willey and Blob (2004) in juvenile common snapping turtles, Chelydra serpentina, during aquatic walking (Figure 5.16). Long muscular tails are characteristic of Chelydridae and Platysternidae and can facilitate the climbing inclines (Finkler & Claussen, 1997), in contrast to the vast majority of other extant turtles that possess reduced tails that play a negligible/limited role in locomotion (Pace et al., 2001; Walker, 1973; Zug, 1971). In the long-tailed forms, the tail may leave a twisted trail on the ground. Common snapping turtles move their tails cyclically during aquatic locomotion. This tail motion does not appear to be a passive effect of limb retractions but is potentially controlled by caudi-iliofemoralis contractions on the same side of the body. Lateral compression of the tail also suggests that lateral tail oscillations may conceivably accelerate water volume posteriorly and thus contribute to aquatic thrust. However, the functional effects of these tail movements demand greater study, particularly as such tail-based propulsion represents the only known involvement of the axial system in thrust generation in turtles.

Many publications have described the dominant dorsoventral flapping of the foreflippers acting as hydrofoils in extant sea turtles, the Cheloniidae and Dermochelyidae (Figure 5.14). The hindlimbs function as combined rudders and elevators (Davenport et al., 1984; Davenport & Clough, 1986; Davenport, 1987; Renous, 1988; Wyneken, 1988a, 1988b, 1997; Renous & Bels, 1991, 1993; Davenport & Pearson, 1994). Use of the foreflippers in combination with the streamlined body confers