Cheloniid Sea Turtles Use a Novel "Shell Pump" Mechanism for Lung Ventilation

Abstract Body : Introduction and Objective
Unlike other amniotes, turtles can’t move their ribs to breathe due to ankylosing of the ribs to other shell skeletal components. Instead, most turtles ventilate their lungs with a sling-like set of muscles housed within their typically rigid shell. Sea turtles, however, have more flexible shells that appear to expand when they inhale. It is unclear whether this expansion is active or caused by passive elastic recoil. If it is active, what biomechanical mechanism could convert muscle shortening within the shell to active expansion of the entire shell?

Materials and Methods
We used a combination of standard video, X-ray Reconstruction of Moving Morphology (XROMM), and ex vivo manipulations to determine whether shell expansion is active or passive in two species of sea turtles.

Results
Video observations showed that the carapaces of juvenile green sea turtles, Chelonia mydas, and juvenile and adult loggerheads, Caretta caretta depress during exhalation and elevate during inhalation. Our XROMM analyses of C. caretta revealed that the distal edges of each half of the carapace translate medially as the dorsal ridge of the shell elevates, a lever system analogous to a scissor lift car jack. To test whether these motions were produced via elastic recoil or active muscular effort, we then simulated ventilation in a postmortem subadult green sea turtle. We observed only minor amounts of passive recoil during these ex vivo manipulations, indicating that ventilatory shell movements are produced via active muscular effort.

Conclusion
We conclude that cheloniid sea turtles use an active, muscle-driven scissor jack lever to expand the shell and produce a novel “shell pump” lung ventilation mechanism.

Significance/Implication
When sea turtles come to the surface to breathe they are more vulnerable to predation, particularly from sharks spotting their silhouetted forms from below. Sea turtles take large breaths in quick succession, presumably to reduce their time and vulnerability at the air-water interface. Cheloniid sea turtles have been described as “blowing” air out at the surface, much like a whale, and then rapidly and forcefully replenishing their lung volume before resubmerging to the relative safety of the depths. Our discovery of the shell pump provides a mechanism for the large breaths, i.e., large tidal volumes, observed in cheloniid sea turtles, relative to other turtles. We hypothesize that shell flexibility in sea turtles evolved to protect the lungs during deep dives, and subsequently was recruited as part of lung ventilation to increase tidal volume and reduce time spent breathing at the surface.

Funding Sources - Bushnell Graduate Research and Education Fund.