Biology_of_Turtles

Figure 3.23  Carapaces of subadult Notochelys platynota showing isolated persistent fontanels.

that is persistent until near-maturity, by which time all the other fontanels have closed. It is located directly above the (somewhat rudimentary) inguinal buttress.

The previous batagurid species share a tropical-forest-floor, leaf-litter, or shallow stream and puddle environment, which seems to correlate with the production of very large, hard-shelled eggs that are not buried but merely concealed beneath a few leaves. In the American tropics, this niche is occupied by the batagurids Rhinoclemmys punctularia, R. diademata, R. melanosterna, and so on.

In several large riverine batagurids (namely Batagur baska, Callagur borneoensis, Kachuga kachuga, K. dhongoka, and K. trivittata), extensive intercostal fontanels are present in the young but they close progressively with growth and have disappeared in females by the time mature size is reached. Alternatively, in the males (which reach a much smaller adult size than the females), the fontanels do not disappear but the rather sharp, rough inner edges of several of the juvenile fontanels become smooth and rounded, producing the effect of a series of four or five “portholes” that persist even in old animals (Figure 3.24). In some cases, adjacent pairs of these portholes may coalesce, becoming incompletely separated by a bony spike. The function of this strange condition is arguable. Hypothetical explanations must include consideration of the fact that the shell in at least some of these turtles is unusually thick and the internal buttresses developed to a remarkable degree. Furthermore, adults achieve fully ankylosed shells. There is thus a bizarre disparity between the massive overall armoring and the contrasting vulnerability resulting from the persistence of the fontanels, which become permanent openings in the bony shell covered with paper-thin scutes.

The adaptive value must also take note of the presumption that the persistent fontanels are so important that they exist in spite of the apparent need for these turtles to have exceptionally heavy armor. Furthermore, the interpretation must explain why the fontanels are retained in this way only

Figure 3.24  Costal “portholes” of adult male Callagur borneoensis.

in males. A possible hypothesis is that the lungs, situated in the bony pocket on each side of the shell, protected fore and aft by the heavy buttressing but exposed to vibrations or pressure waves impacting upon the fontanels, serve as a sort of echo chamber to provide exceptional sensitivity to waterborne (or airborne) vibrations. It may be no coincidence that female turtles of the genera Batagur and Callagur are known as “tuntong” in Malayalam, a word that translates as “thumper.” Perhaps there has been great selectivity for the males to be able to detect the thumping as the female closes and conceals her nest, and it may allow such males to be the first to locate and mate with a given female after she returns to the water.

3.6Plastral Reduction

Typically, the plastron covers nearly the entire underside of a turtle, but this is not always the case. The plastron in most species has multiple functions—that of physical protection for the underside of the animal; providing a strong crossbar to prevent splaying of the sides of the carapace if the animal suffers vertical compression; and providing anchorage for the insertion of a wide range of muscles associated with the anterior and posterior limb girdles, as well as those responsible for plastron closure in hinged species.

Nevertheless, in certain turtle species the plastron is reduced to a cruciform condition that would appear to reduce the “protective breastplate” function of the “Bauchpanzer” to a significant degree, and that thus requires some explanation. Extant representatives of such species include the snapping turtles (Chelydra and Macrochelys), and several kinosternids (Sternotherus, Staurotypus, Claudius). The details of plastral reduction in these species are very varied, but the common

“tilt” to accommodate the depressed mandible during threat display. Scutes are reduced to just four pairs, probably corresponding to the humerals, pectorals, femorals, and anals. Most of the bridge is covered with soft tissue, with a short extension from the pectoral scute covering the proximal part. Axillary and inguinal scutes are lacking.

In the closely related Kinosternon and Sternotherus, a shared feature is the absence of the entoplastron, an omission otherwise known only in Dermochelys among extant turtles. Kinosternon includes both species with enlarged plastra as well as those with reduced ones; the plastral kinesis and associated musculature are quite different in the two morphotypes (Bramble et al., 1984). In the small-plastron forms of Kinosternon (i.e., K. subrubrum steindachneri, K. angustipons, K. herrerai, K. chimalhuaca, and K. dunni, with non-overlapping ranges in Florida, Caribbean Costa Rica, eastern Mexico, western Mexico, and northwestern South America, respectively), the plastron presents both anterior and posterior “hinges” although actual kinesis is very modest, with none of the capability for forceful full elevation of both anterior and posterior lobes seen in the large-plas- tron species. The reduced plastral kinesis is very similar to that of Sternotherus, and the two genera are often combined into one, although Sternotherus does show some unique features, including a reduction in size of the plastral scutes and proliferation of soft tissue along the scute borders, as well as a long anterior interhumeral seam.

The double kinesis in the Kinosternon complex involves an anterior lobe composed of the paired epiplastra, a fixed midsection including the hyoplastra and hypoplastra, and a posterior lobe including the xiphiplastra. The anterior lobe scutation involves a small anterior element preceding two pairs of larger scutes, the midsection is covered by a single pair of scutes, and the posterior lobe bears two further pairs. Homology and thus nomenclature of these scutes is somewhat complex, but the single anterior scute (absent in Sternotherus carinatus) is considered to be the gular, followed by paired humerals. The next pair, seemingly the pectorals, are in fact just the anterior parts of those scutes, with the greater part of the pectorals lying posterior to the anterior hinge and covering the midsection of the plastron. The abdominal scutes, large in most turtles, are absent. The scutes covering the posterior lobe are the femorals and anals. Evidence for this nonintuitive interpretation, with the pectorals transversely split by the anterior hinge, are presented by Hutchison and Bramble (1981) and discussed by Pritchard (2003).

3.7Deformities

It is not unusual to find tortoises with deformities of shell growth. These are discussed in the following sections.

3.7.1“Pyramiding”

Pyramiding is often seen in tortoises that have been raised under unnatural conditions of humidity and diet, and it results in the vertebral and costal scutes having the central areolae sharply elevated. It also occurs to a mild degree in nature in such tortoises as Geochelone pardalis, whereas wild adult females of Psammobates tentorius tentorius may show extreme pyramiding (Figure 3.26). The potential for the condition is thus evident even in certain tortoises living in the wild, with an entirely natural diet and environment. Some species, including Geochelone carbonaria, may develop carapace pyramiding in captivity but this is never shown in wild specimens. The condition usually makes itself evident during the post-hatchling months, and much more rarely first manifests itself later in life. It has long been believed that the condition resulted primarily from a diet too rich in protein, and an alternative cause was believed to be an unnatural ratio of calcium to phosphate in the diet. Secondary causes were attributed to overfeeding, dietary fiber, temperature, UV light, and so on. However, current belief is that the condition derives from excessively dry conditions, and when hatchlings are raised on a substrate of wet sphagnum, shells will develop normally (Wiesner & Iben, 2003).

Figure 3.26  Pathological shell pyramiding in juvenile Astrochelys radiata (left) and normal adult female

Psammobates tentorius tentorius (right).

3.7.2Kyphosis

This “humpbacked” condition appears to be congenital and shows up occasionally in many species. It is particularly dramatic when it occurs in trionychids, in which the normally flat turtle takes on the appearance of a tall sombrero (Figure 3.27). Lordosis, or swayback, is also seen occasionally and may be the normal condition in old specimens of such specialized, flat-shelled species as Platysternon megacephalum and Malacochersus tornieri. Scoliosis, or kyphoscoliosis, in which the spinal column forms lateral curves or kinks, may be encountered as a rare condition in many turtle species.

3.7.3Scute Abnormalities

The standard chelonian configuration described previously that includes five vertebral scutes and four pairs of costals, with about 22 marginals, is remarkably stable but even apart from the minor, species-specific variations mentioned here, it is not unusual for deviations—even drastic ones—to occur. They are more frequent in the carapace than in the plastron, and some of the various configurations that may exist are described by Zangerl (1969), who also observed that a particular set of repetitive variants, each with a definite frequency of occurrence, appears to be characteristic of each species or subspecies. Some scute abnormalities appear to be genetic; others result from accidents, injury, or other trauma during the embryonic stage.

Certain far-reaching derived or abnormal conditions may occur repetitively. An example of this is the replacement of the normal straight series of five vertebral scutes by an asymmetrical zigzag series of eight or nine individual elements, each often reduced to a triangular shape (Figure 3.28).

Figure 3.30  “Geodesic” bony carapace of Manouria impressa. Carapace with scutes on right.

bridges connecting the plastron to the peripheral bones. However, a few tortoise species—which happen to run the gamut from the most flattened species of all to the most highly domed—develop very thin or extensively fenestrated shells, with bones of reasonable thickness offering some structural support retained only around the scute sulci.

In Malacochersus tornieri, the plastron has a huge central fontanel, and the flattened carapace is extensively fenestrated although the scutes themselves are thin and unspecialized. The structure corresponds to the unique ecology. Rigidity and strength have been sacrificed in favor of literal flexibility; both plastron and carapace can be depressed with light finger pressure, even in adult specimens. This extraordinary degree of shell reduction allows accommodation to the pressures encountered when the tortoise takes refuge in deep, irregular rock fissures, from which few, if any, predators can extract it. Although the tortoise is seemingly highly vulnerable when outside such crevices, it compensates by spending very little time outside.

In Manouria impressa, the plastron is fully ossified and unreduced, although the carapace is extensively fenestrated (Figure 3.30). As in Malacochersus, the bony carapace is retained at normal thickness only around the scute sulci, but the resulting structure is perfectly rigid as a result of the extraordinary thickening of the dorsal scutes. This thickening does not generate elevation or “pyramiding” of the scutes, but rather the thickening extends inward, with each somewhat lens-shaped scute fitting into a shallow concavity in the bony carapace. The shell in this species is somewhat flattened but not nearly as much as in Malacochersus, and it is rigid rather than flexible. M. impressa is found at high altitudes in tropical and subtropical southeast Asia but details of its ecology remain lacking. A curious feature is that the costal scute areolae, often clearly defined even in adults, are located near the centers of the scutes. In most turtles, the costal aureolae become increasing displaced toward the vertebrals with growth (Malaclemys is an exception).