Biology_of_Turtles

Figure 9.2  Adult turtle heart after removal of the pericardium and gubernaculum cordis. The atria are large and relatively thin-walled. The muscular ventricle shows no external indication of the three internal compartments. The great vessels are large and prominent as they emerge from the anteroventral aspect. (From Wyneken, 2001. With permission.)

Physiological studies of other reptiles link intracardiac shunting and digestion. The drainage of the upper gastrointestinal (GI) system suggests a functional link in turtles. Much of the blood supply to the turtle GI system arises from the left aorta. The great vessels and the GI system receive vagal innervation. The left aorta, the middle of the three great vessels, turns dorsolaterally and passes the level of the stomach before producing three branches: the gastric artery, the celiac artery, and the superior mesenteric artery draining to the stomach, pancreas, duodenum stomach, liver, and gallbladder. The superior (or anterior) mesenteric artery gives off many branches that fan out through the intestinal mesenteries and supply the small intestines. After giving off the superior mesenteric artery, the left aorta continues posteriorly where it joins the right aorta (typically) to form a single dorsal aorta. The position where the two join is variable but generally occurs within the middle third of the body.

Within the lung, capillaries join venules that flow into veins that drain into the pulmonary veins. The pulmonary veins travel along the ventral surface of each bronchus, then exit the lung anteriorly and arch medially. They enter the left atrium dorsolaterally. Venous blood from the body drains into the sinus venosus from four major veins: the left precava (left superior vena cava), the right precava (superior vena precava), the left hepatic vein, and the postcava (posterior vena cava).

to 78% of the carapace length (for example, Caretta caretta, Gopherus agasszii, Testudo graeca, and T. scripta span this range; Figure 9.4). The lungs are located dorsally and are

Postcava

Dorsal aorta

Dorsal aorta

B

Great vessels

Ventricle

Pulmonary Aortas artery &

vein

Figure 9.3  (A) Diagram of the dorsal (left) and ventral (right) turtle cardiopulmonary system vasculature.

(B) The same views of the vasculature and heart as an MRI taken in vivo. The turtle’s neck was retracted during imaging, so the carotids and their branches are not fully extended.

attached to the carapace and vertebral column via a pulmonary ligament. In some species (e.g., Lepidochelys kempii and C. caretta), the lungs are more closely attached to the vertebral column than in other species (T. scripta and Geochelone carbonaria). Turtles have an intrapulmonary bronchus that extends most or all of the length of each lung and structurally separates the lungs of most species into medial and lateral chambers. Freshwater turtles and some tortoises show torsion of the lobes so that the structure appears more complex in the species examined (Perry, 1998).

Turtle lungs are structured differently than mammalian lungs (Figure 9.5). The bronchus is unbranched, so there is no bronchial tree. There are no alveoli. The parenchyma is organized into thin walls (trabeculae) that surround niches (Figure 9.5). The niches contain shallow open box-like ediculi (or ascini) or faveolar spaces that are deeper than they are wide (Duncker, 2004; Perry, 1998). These air exchange structures are associated with suites of other morphological, behavioral,

Figure 9.6  Dissection of the ventral surface of the lungs of C. caretta showing the long intrapulmonary bronchus. (From Wyneken, 2001. With permission.)

muscles (Gans & Hughes, 1967; Gaunt & Gans, 1969). Rates and flows vary depending on whether the animal is aquatic or terrestrial. Inspiration and expiration are active processes and are decoupled from locomotor activity (Landberg et al., 2003). Turtles have no diaphragm muscle separating pulmonary and coelomic compartments, but some species possess a membranous post-pulmonary ligament, which partially separates the pulmonary and coelomic compartments.

9.7CardioVascular Shunts

Shunts are responsible for rerouting blood. Intracardiac shunting mechanisms have anatomical and hydrodynamic basis; they route blood between systemic and pulmonary circuits (Figure 9.7). They are involved in changing myocardial oxygenation and coordinating the movement of blood among the ventricular compartments. Within reptiles, there are at least three other groups of peripheral shunts that can reroute blood: the pulmonary artery–systemic aorta shunt, the intrapulmonary shunt, and peripheral shunts such as the vascular circumflex of the distal limbs.

9.7.1Cardiac Shunts

Cardiac shunts are associated with intraventricular flow, rerouting of blood between pulmonary and systemic circuits (Figure 9.7), and require an incomplete ventricular septum; these are found in noncrocodilian reptiles, including turtles. Shunts regulate blood flow and respond, in part, to blood gases; they are often described as “right to left” (R-L) referring to the shift in blood from the pulmonary circulation to the body (the system), and “left to right”(L-R), referring to the shift of some blood back to the lungs and the body when physiological conditions permit (Wang et al., 1997; Hicks, 2002).

Wang et al. (2001) demonstrated that the low systemic blood oxygen levels that result from the large R-L shunt may serve to regulate metabolism. Yet, when any of several physiological or environmental events (temperature, exercise, or digestion) increase metabolism, the R-L cardiac shunt becomes less strong and oxygen delivery to the body increases. Hicks (2002) explored this and other “adaptive hypotheses” for the functional significance of cardiac shunts. He concluded that comparative and experimental studies document the function of shunts but do not provide supporting data for the adaptive value of cardiac shunts.

the remainder of the respiratory process is rather consistent. Of particular significance is the turtle’s ability to use anaerobic metabolism for relatively long periods. The buffering systems within the body (blood, pericardial fluid, and shell) are able to compensate for the buildup of lactic acid and hydrogen ions during anaerobiosis (Stecyk et al., 2004).

Turtles are not limited to gas exchange through the pulmonary tissues. Some aquatic species have an ability to exchange respiratory gases through the integument, pharynx, or cloaca. Softshelled turtles (Trionychidae), may obtain up to 70% of their oxygen during submergence through the leathery shell (Stone et al., 1992). Highly vascularized pharyngeal papillae are also able to extract dissolved oxygen from the water. In some Australian sideneck turtles, cloacal bursae function in gas exchange (King and Heatwole, 1994).

9.9Overview

The functional relationships of the cardiopulmonary system components (the pump, pipes, and ventilation) remain enigmatic. Physiologically invasive studies show that cardiac shunting occurs, yet morphological correlations are loose at best. At present, separation of systemic and pulmonary blood flows has been compared in vivo in few species. Even the limited survey of intracardiac and great vessel structures greatly exceeds the measurement of function. Correlations between structure and function are more closely associated with behaviors that include diving habits, migratory activity, and prolonged apnea.

Major morphological differences in cardiopulmonary structure among turtle taxa include the degree of separation of the ventricular compartments through muscular ridge development, the presence and form of pulmonary artery sphincters, and, in the lungs, size and density of air exchange structures. Differences tend to correlate with ecological specialization; however, the adaptive value of some aspects has not been experimentally demonstrated. The structural–functional features of the cardiopulmonary systems generally are correlated to the ecology and behavior; however, this is not always the case. Comparisons among species in the morphology of the structures directing L-R and R-L shunt development indicate moderate development in the loggerhead sea turtle (C. caretta), a migratory, intermediate depth, diving species, greater development in Galapagos tortoises (G. elephantopus). For example, anatomical evidence of mechanisms for the development of strong L-R and R-L shunts is weak (small muscular ridge development or no clear vascular sphincters in pulmonary circuit) in shallow diving freshwater turtles, T. scripta, the most studied species. Yet, the physiological evidence for L-R and R-L shunting in these turtles and some small tortoises is robust. Wang et al. (2001) reason that species that can sustain the highest metabolic rates also should possess the highest degree of anatomical ventricular separation and therefore, weaker intracardiac shunting. Turtles generally lack high metabolic rates. Arguably the most endothermic species (D. coriacea) may maintain high metabolic rates, but the cardiac and great vessel anatomies imply mechanisms for developing strong L-R and R-L shunting. Theoretically, this species may retain the heart morphology of its smaller, primarily ectothermic youth. Juvenile stages are ectothermic at smaller body sizes (Eckert, 2002). Unfortunately, outflow from the heart has yet to be measured in this species. The ontogeny of cardiopulmonary structure and function has not been studied in any species.

9.10Comparisons with Other Reptiles

The respiratory tracts of most reptiles are anatomically and physiologically different from those of mammals. Reptiles lack a bronchial tree, and air exchange surfaces (ascini and faveoli) differ in structure from the alveoli of mammals.

In addition to airway structure, there are significant differences in lung structure and function among the four major reptilian groups: turtles, snakes, lizards, and crocodilians. Turtles all have multichambered lungs with an unbranched bronchus. Lizards cover the range from simple lungs in

geckos, to multichambered lungs of iguanas, to those with long diverticula or lobes (chameleons), and the multichambered lungs with branched bronchi in varanids and helodermids. In snakes, the left lung is reduced or absent. Snakes lungs are elongate and have a highly vascular anterior part (the respiratory lung) and the caudal portion is an avascular sac (saccular lung). Many turtle and tortoise species have poorly vascularized lobes along their lateral and caudal periphery; however, the distinction is not as great as in snakes. Not surprisingly, species-specific specializations in lung structure and function are related to the ecology and behavior of the species; those lungs with the greatest surface area and complexity are found in the more active, wide-ranging, or predatory reptilian species.

Ventilation of the lungs occurs without the assistance of a diaphragm. Movements of the dorsal and ventral ribs by intercostal muscles drive ventilation in lizards. Lizards may also supplement air movement with gular pumping. Snakes use movements of the dorsal ribs for ventilation. Turtles and tortoises ventilate by movements of inguinal, axial, and shoulder muscles to change the pressure within the pleuroperitoneal cavity. Buccal oscillation is functionally separate from ventilation in turtles (Brainerd and Owerkowicz, 2006). Some aquatic species of turtle (some Australian side-necks and mud turtles) may supplement lung-based gas exchange through highly vascular gas exchange surfaces in the cloaca.

9.11Conclusions

The turtle cardiopulmonary systems vary in the extent of lung surface area, architecture of the ventricle, and the form of the pulmonary arteries. These three characteristics are grossly correlated with behavior and ecology. Turtle hearts may be viewed as fiveor six-chambered, with the chambers having context-specific roles in routing blood to the body or to the lungs and the body. Unique features of testudine cardiopulmonary systems include a weakly to moderately developed muscular ridge, pulmonary artery sphincters, highly variable cardiac output, intracardiac and intrapulmonary shunts, episodic ventilation, and diversity in lung form, size, and surface area.

Acknowledgments

I thank S. Epperly, C. Farmer, M. Godfrey, B. Jensen, C. Johnson, K. Kardong, P. Lutz, S. Milton, J.A.G. Rhodin, M.D., A.G.J. Rhodin, M.D., F. Steinberg, M.D., M. Salmon, M. Starck, B. Tuller, T. Wang, and D. Wilke for technical assistance, thoughtful discussions, and/or critical review. W. Teas, J. Weege, D.V.M., D. Mader, D.V.M., S. Milton, Gumbo Limbo Environmental Center, Harbor Branch Oceanographic Institute, Loggerhead Marinelife Center, National Marine Fisheries Service, and the ARAV provided access to specimens.

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