Lung ventilation during treadmill locomotion in a terrestrial turtle, Terrapene carolina

The 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.