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

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

• Landberg, T., Mailhot, J.D., Brainerd, E.L. Lung
  ventilation during treadmill locomotion in a
  terrestrial turtle, Terrapene carolina. Journal
  of Experimental Biology. 206 (2003) 3391-3404.

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Background Information

• Anatomy with regard to breathing mechanisms
• Limb girdles (pectoral and pelvic) and lungs both
  located within bony shell
• Rigid shell contains fixed volume
• Air in lungs displaced when axial/appendicular
  elements move within the shell
• Retraction of pectoral/pelvic limb and girdle
  elements into shell drives air out of lungs
• Protraction of limb elements creates
  subatmospheric pressures, producing inhalation

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• Mechanical interactions between locomotion and
  breathing in extant tetrapods are of particular
  interest because lung ventilation is hypothesized
  to conflict with locomotion in the common
  ancestor of amniotes
• In primitive amniotes, locomotion and ventilation
  come into mechanical conflict because locomotion
  requires unilateral activity of axial musculature
  while costal ventilation requires bilateral
  activity of those same muscles
• Some vertebrates have independently evolved to
  cope with this constraint by developing body
  postures or alternative ventilatory mechanisms
  that partially decouple breathing from locomotion
• i.e. mammals, birds, crocodilians
• Lizards gular pump to supplement lung
  ventilation while costal musculature is used for
  locomotion
• Alternative breathing mechanisms such as gular
  pump may be employed during locomotion for
  turtles, if limb movements interfere with their
  breathing however, previous studies show that
  gular oscillations do not contribute to lung
  ventilation of resting turtles

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• Two main breathing mechanisms
• 1. Action of oblique (OA) and transverse
  abdominis (TA), diaphragmaticus, and striatum
  pulmonale muscles
• TA and OA alternate bilateral muscle activity to
  produce exhalation-inhalation breathing cycles at
  rest
• TA and OA considered primary ventilation
  mechansim for turtles
• present in all extant species
• active consistently during lung ventilation
• 2. Limb-pump ventilation mechanism
• Limbs and girdles contribute to ventilation and
  redistribution of air into lungs
• Muscles of pectoral/pelvic limbs and girdles are
  active during ventilation at rest as well as
  during limb movement during locomotion

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Hypothesis

• If these muscles are used for both breathing and
  locomotion, then locomotion may either interfere
  or assist breathing.
• Respiratory and locomotor functions of
  vertebrates often highly integrated
• Many vertebrates couple breathing and locomotion
• Goals of this study were to determine whether T.
  carolina breathes during locomotion
• Does locomotion alter breathing performance
• Are ventilation and locomotion temporally coupled
• Are airflow rates directly affected by stride
  cycle
• Are lung ventilation mechanisms the same as in
  resting animals

• Information about breathing performance during
  locomotion may help interpret evolution of lung
  ventilation mechanisms in relation to turtles
  unique morphology

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Methods

• Three individual Terrapene carolina triunguis
• Controlled temperature of 30 deg C to maximize
  voluntary locomotion
• Constructed pneumotach masks that did not
  interfere with vision, hearing, or breathing
• Holes made for nares and mouth
• Connected to a differential pressure transducer
• Ventilatory airflow recorded simulataneously with
  lateral view x-ray and light video images
• Four part experiment
• Acclimation to mask, treadmill chamber, and
  temperature
• Pre-exercise
• Locomotion
• Recovery

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Results

• Airflow recordings show large exhalations
  accompany head and limb retraction and plastral
  adduction lung ventilation still occurs in fully
  retracted position
• Front and back halves of plastron connect to each
  other and the carapace by ligamentous connective
  tissue
• Lungs are located in the dorsal region of the
  carapace with large neck retractor muscles
  situated between them
• high domed shape of carapace allows for large
  residual lung volume
• Lung ventilation occurs continuously during
  treadmill locomotion
• Evidence that gular pump is not employed because
  airflow recordings would show small inhalations
  followed by little or no exhalation
• Highest breath frequency recorded during period
  of locomotion
• An average airflow rate was calculated for
  inhalations and exahalations to determine whether
  limb movements affect airflow rates during
  locomotion
• Results not consistent
• Few statistically significant differences between
  inhalatory and exhalatory peak airflow rates

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• X-ray recordings tracked movement of inguinal
  flanks during breathing
• Determine whether abdominal muscles are mechanism
  for breathing during locomotion
• At rest and locomotion exhalation accompanied by
  dorsal movement of the marker inhalation
  accompanied by ventral movement of the marker
• Inguinal flanks move in phase with ventilatory
  cycle and indepently from stride cycle

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Discussion

• Green sea turtles exhibit breathing that ceases
  during locomotion, whereas box turtles have been
  found to breathe continuously
• Findings did not support the hypotheses
• 1. T. carolina does not couple breathing with
  locomotion
• Mammals and birds breathing and locomotion are
  coupled due to pressurization cycles of stride
  and breath in thoracic cavity
• 2. Limb movements do not contribute to lung
  ventilation during locomotion
• Lizards breathing performance is impeded with
  increasing locomotive speed because axial muscles
  are needed at times for breathing and locomotion
  simultaneously

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• Timing of breaths relative to stride cycle
• At rest and during locomotion
• Little difference between peak inhalatory and
  exhalatory airflow rates
• Indicates that locomotion has no mechanical
  effect on breathing
• Breathing and stride cycle are independent of
  each other
• Lung ventilation mechanism must be separate from
  locomotor system
• TA and OA muscles used to breathe when at rest
  and most likely are the mechanism for breathing
  during locomotion
• No evidence for gular pump or limb mechanism
• Species lacks diaphragmaticus and striatum
  pulmonale muscles

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Chelonia mydas vs. Terrapene carolina

• Kinematics of locomotion
• C. mydas front limbs retract simultaneously to
  push body forward, a bilateral synchronous motor
  pattern which is also used during limb-pump lung
  ventilation
• May cease breathing during locomotion because
  pressurized lungs are used to stabilize limb
  movements
• T. carolina alternating gait with one diagonal
  pair of limbs extended while other pair is flexed
• A more balanced effect on internal shell volume,
  in addition to abdominal muscles separate from
  the locomotor muscles, provides explanation for
  absence of effect of locomotion on ventilation

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Conclusion

• Specialized ventilatory functions of abdominal
  muscles were favored by natural selection since
  they permit breathing during locomotion
• Shell-less ancestor of turtle most likely relied
  on mechanism similar to that of extant lizards
  (axial bending during locomotion, rotation of
  ribs during ventilation) and would have
  experienced a mechanical conflict as do lizards
• Hypothetical ancestor gave rise to turtles as
  ribs abandoned ventilatory function and fused
  into the shell
• Thus, extant turtles are not subject to the
  constraint experienced by shell-less ancestor or
  extant lizards because their ribs do not
  contribute to either locomotion or ventilation