SUMMARYThe limb girdles and lungs of turtles are both located within the bony shell, and therefore limb movements during locomotion could affect breathing performance. A mechanical conflict between locomotion and lung ventilation has been reported in adult green sea turtles, Chelonia mydas, in which breathing stops during terrestrial locomotion and resumes during pauses between bouts of locomotion. We measured lung ventilation during treadmill locomotion using pneumotach masks in three individual Terrapene carolina (mass 304-416 g) and found no consistent mechanical effects of locomotion on breathing performance. Relatively small tidal volumes(2.2±1.4 ml breath-1; mean ± s.d., N=3 individuals) coupled with high breath frequencies(36.6±26.4 breaths min-1; mean ± s.d., N=3 individuals) during locomotion yield mass-specific minute volumes that are higher than any previously reported for turtles (264±64 ml min kg-1; mean ± s.d., N=3 individuals). Minute volume was higher during locomotion than during recovery from exercise(P<0.01; paired t-test), and tidal volumes measured during locomotion were not significantly different from values measured during brief pauses between locomotor bouts or during recovery from exercise(P>0.05; two-way ANOVA). Since locomotion does not appear to conflict with breathing performance, the mechanism of lung ventilation must be either independent of, or coupled to, the stride cycle. The timing of peak airflow from breaths occurring during locomotion does not show any fixed phase relationship with the stride cycle. Additionally, the peak values of inhalatory and exhalatory airflow rates do not differ consistently with respect to the stride cycle. Together, these data indicate that T. carolina is not using respiratory-locomotor coupling and limb and girdle movements do not contribute to lung ventilation during locomotion. X-ray video recordings indicate that lung ventilation is achieved via bilateral activity of the transverse (exhalatory) and oblique (inhalatory) abdominal muscles. This specialized abdominal ventilation mechanism may have originally circumvented a mechanical conflict between breathing and locomotion in the ancestor of turtles and subsequently allowed the ribs to abandon their role in lung ventilation and to fuse to form the shell.
It is reasonable to presume that locomotion should have a mechanical effect on breathing in turtles. The turtle shell is rigid, and when the limbs protract and retract, air in the lungs should be displaced. This expectation was met in a previous study of the green sea turtle, Chelonia mydas; breathing completely ceased during terrestrial locomotion (Jackson and Prange, 1979. J Comp Physiol 134:315-319). In contrast, another study found no direct effect of locomotion on ventilation in the terrestrial box turtle, Terrapene carolina (Landberg et al., 2003. J Exp Biol 206:3391-3404). In this study we measured lung ventilation during treadmill locomotion in a semi-aquatic turtle, the red-eared slider, Trachemys scripta. Sliders breathed almost continuously during locomotion and during brief pauses between locomotor bouts. Tidal volume was relatively small (approximately 1 mL) during locomotion and approximately doubled during pauses. Minute ventilation was, however, not significantly smaller during locomotion because breath frequency was higher than that during the pauses. We found no consistent evidence for phase coupling between breathing and locomotion indicating that sliders do not use locomotor movements to drive breathing. We also found no evidence for a buccal-pump mechanism. Sliders, like box turtles, appear to use abdominal musculature to breathe during locomotion. Thus, locomotion affects lung ventilation differently in the three turtle species studied to date: the terrestrial Te. carolina shows no measurable effect of locomotion on ventilation; the semi-aquatic Tr. scripta breathes with smaller tidal volumes during locomotion; and the highly aquatic C. mydas stops breathing completely during terrestrial locomotion.
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