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Geometric analysis of airway trees shows that lung anatomy evolved to enable explosive ventilation and prevent barotrauma in cetaceans

Robert L. Cieri, Merryn H. Tawhai, Marina Piscitelli-Doshkov, A. Wayne Vogl, Robert E. Shadwick

Posted on: 26 November 2024 , updated on: 27 November 2024

Preprint posted on 18 October 2024

Geometry determines how deep whales dive? How airway metrics can protect whales from crushing hydrostatic pressure

Selected by Sarah Young-Veenstra
Image credit: Dr.Haus. Reproduced under the Creative Commons Attribution-Share Alike 3.0 Unported license.

Background

Whales, dolphins, and porpoises, known collectively as cetaceans, face a unique challenge of being obligate air breathers whilst spending their lives entirely underwater. Cetaceans’ aquatic existence is made possible by a host of biological specializations, including the biomechanical structure of their respiratory pathway.

As air breathers in water, cetaceans hold their breath for the majority of their lives. From breath to breath, cetaceans inhale, dive, resurface, exhale, repeat. Such a routine would decimate the human body. Indeed, if a breath-hold diver resurfaces from a dive deeper than 25 meters without exhaling through the ascent, the individual would experience pulmonary barotrauma – a condition brought on by a drastic pressure imbalance between the external environment, wherein pressure is rapidly decreasing, and the lung, wherein the pressure is increasing. As the gaseous pressure within the lung increases, the air can break through the pulmonary membrane, causing alveolar rupture and hemorrhage. Remarkably, despite enduring breath-hold ascents constantly, cetaceans avoid barotrauma, which is made possible by the ability to store oxygen in their blood and muscles instead of lungs, allowing them to compress their lungs at depth, and escape pulmonary pressure effects.

Cetaceans seal their blowholes while underwater, meaning they cannot exhale until reaching the surface. Once they reach the surface, they get a single breath to exchange large volumes of air in a very short time. The demand to immediately ventilate upon resurfacing from a dive presumably requires that air be stored within the respiratory system, such that it is ready to be rapidly exhaled. For reference, in humans, a single breath (inhale and exhale) takes approximately 3 seconds and exchanges 10-15% of air in the lungs. Some cetacean species can exhale and inhale within a fraction of a second and exchange 80-90% of their air in a ventilation strategy called “explosive ventilation”, which is common in shallow diving (up to 100m) cetaceans. Deep diving (below 100m) cetaceans tend to breath via a slower ventilatory strategy, wherein a breath takes 1-2 seconds to exchange ~80% of their air. Species who utilize the slower ventilation strategy are often referred to as “logging” species because they are known to periodically lie at the surface in a sleep-like state, breathing at a reduced rate. Whether “explosive” or “slow” ventilators, cetaceans’ efficient ventilation seems to mandate air storage within the airway, which exists in direct contrast to the demand to store air outside the lungs to avoid pulmonary barotrauma.

A possible solution is storing “old air” that is ready to be exhaled in the respiratory system, but within proximal bronchi that are resistant to pressure-induced compression (See visualization in Figure 2A in Ceiri et al. 2024, bioRxiv). In which case, large airways would likely be found in deep diving logging species. Conversely, wide airways may be required to facilitate rapid air movement with minimal resistance, which would suggest that wide airways should be found in shallow diving explosive ventilating species. Ceiri and his team at the University of British Columbia were interested in this functional dichotomy and investigated how airway geometry evolved in response to these competing biomechanical challenges.

Key Findings

To gain understanding as to how airway facilitates cetacean diving strategy with respect to the two major biomechanical pressures (air storage [1] amid hydrostatic pressure at depth and [2] being ready for immediate exhale upon resurfacing), the research team investigated how the airway diameter and airway tree branching angle differs between species who fall into various dive depth and ventilation speed categories:

  • Shallow diving explosive ventilators: porpoises, dolphins
  • Shallow diving intermediate ventilators: minke whale
  • Moderate depth diving intermediate ventilators: orca whale
  • Deep diving intermediate ventilators: beluga whale
  • Deep diving logging ventilators: pilot whale, sperm whale, beaked whales

Additionally, the researchers investigated the airway geometry of a domestic pig to gauge how a terrestrial mammal compares to cetaceans.

Airway Diameter

Strahler diameter ratios describe the increase in tube diameter with each branch of the airway, moving from distal-most bronchioles to most proximal bronchi. The Strahler diameter ratios were highest in deep diving slow ventilating species, and diameters decreased as breathing speed got faster (See Figure 5 in Ceiri et al. 2024, bioRxiv).

This finding supports the authors’ “barotrauma hypothesis”, which expects that larger airways facilitate deep diving in cetaceans by providing compression-resistant air storage to protect the animal from barotrauma. Indeed, at the distal-most end of the airway, mammals, including cetaceans, have delicate bronchioles called acini that are responsible for gas exchange with the blood. The acini would be vulnerable to barotraumatic injury during dive resurfacing, but, in accordance with the barotrauma hypothesis, higher Strahler diameter ratios may protect the acini. As an individual dives to depth, and the pressure promotes organ compression, the acini compress and release their air into the adjacent airway; wider airways may provide enough extra space that the fragile acini can completely empty and, thereby, escape pulmonary barotrauma.

Furthermore, the authors pose that logging ventilation may be attributable to high Strahler diameter ratios. Counterintuitively, higher Strahler diameter ratios have been associated with increased flow resistance and, therefore, may necessitate logging ventilation to obtain enough oxygen. Lower Strahler diameter ratios facilitate higher rates of air flow and, potentially, more efficient ventilation. Therefore, the authors suggest that shallow diving cetaceans, who employ explosive ventilation strategies, may actually experience selection for lower Strahler diameter ratios – which would, further, align with the barotrauma hypothesis.

Airway Tree Branching Angle

The authors observed that the average angle of bronchiole branches tended to decrease with deeper routine dive depth and increase with speed of ventilation (See Figure 4 in Ceiri et al. 2024, bioRxiv). Based on this apparent association, the authors pose that acute branching of the airway may facilitate more powerful ventilation cycles as the angular structure allows more and faster gas flow between acini and major bronchi.

Conclusion

This study investigated how airway geometry is associated with diving behaviour in cetaceans and, ultimately, suggests that wide airways evolved as a means for coping with hydrostatic pressure during dives by storing air to protect against pulmonary barotrauma when resurfacing.

Why I chose this preprint

I was enthralled by how this study explores what, initially, appeared to be a striking dichotomy of demands in how whales cope with two competing biomechanical challenges. I am fascinated by the complexity of animals who live in challenging environments and how it seems that, as science advances, more questions arise. This study, not only found support for their hypothesis, but also found that the demands were not, in fact, dichotomous.

Questions for the Authors and Future Directions

  1. I think it was interesting to compare the cetacean airways to that of a pig! I’m curious as to why you chose a pig for comparison? And there was little mention of the results regarding the pig. I’m wondering what the major observed differences were between cetaceans and pig, and whether pig airways were more similar to shallow/ deep diving/ rapid ventilating/ logging ventilating cetaceans?
  2. I think it’s a fascinating association between airway branching angle and ventilation speed. I’m wondering if you might expand on how a more angular airway might facilitate explosive ventilation? Were the pig’s airway branches much less angular than the cetaceans’?
  3. Do you know whether there are differences in the breathing-musculature of rapid vs. logging ventilators? Could ventilation type be impacted by strength of exhale/ inhale (i.e., might explosive ventilators have stronger breathing muscles)?
  4. The ages of animals observed in your analysis ranged from neonate to adult. Do you expect age and development might have any bearing on the results?

Tags: balaenopters acutorostrata, barotrauma, behaviour, biomechanics, blood shunt, decompression sickness, delphinapterus leucas, diving physiology, globicephala macrorhynchus, kogia breviceps, mesoplodon bidens, mesoplodon densirostris, mesoplodon europaeus, metabolism, orcinus orca, phocoena phocoena, phocoenoides dalli, pressure, stenella frontalis, sus domesticus, tursiops truncatus

doi: https://doi.org/10.1242/prelights.38999

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