Structure and biomechanical properties of the trachea of the striped dolphin Stenella coeruleoalba: Evidence for evolutionary adaptations to diving

Abstract

This study analyzes the structure and mechanical properties of the trachea of the striped dolphin Stenella coeruleoalba, one of the most common cetacean species. The cetacean trachea is made up of closed or semiclosed cartilaginous rings without a paries membranaceus. Our results indicate that the inner lining of the trachea contains erectile tissue in which several venous lacunae permeate the mucosa. We also observed and described the presence of peripheral neurons containing nitric oxide along the rim of the venous lacunae. Data obtained from compression and tensile tests and comparison with the pig and goat tracheas indicate a higher stiffness and a different, higher breaking point for the dolphin trachea. On the whole, our data suggest that the trachea of the striped dolphin possesses structural properties that allow rapid filling with blood, possibly in relation to dive activities, and also allow modifications due to increased pressure and immediate return to the original shape without risks of permanent bending or rupture, as would happen in a terrestrial mammal. As the organ undergoes intense pressure difference during descent to optimal foraging depth and subsequent rapid ascent to surface, especially in deep dives of hundreds of meters, the specific structural and biomechanical peculiarities of the trachea of the striped dolphin may represent an evolutionary adaptation to life in the water and to diving.

A comparative analysis of marine mammal tracheas

“…Although we did not find interspecific variation in tracheal rings apart from age-related changes, further histology and greater sample size may have indicated otherwise. Our study was different from the approach by Cozzi et al (Cozzi et al, 2005), where strain curves were used to assess the compliance of the trachea in the striped dolphin (Stenella coeruleoalba). Our approach allowed a simultaneous assessment of both compression and expansion of the trachea.…”

“…Previous studies have published accounts of the anatomical characteristics of the trachea in marine mammals (Scholander, 1940;Slijper, 1962;Sokolov et al, 1968;Kooyman and Sinnett, 1979;Bagnoli et al, 2011;Cozzi et al, 2005). In this study, we separated the various structural characteristics observed into five distinct categories depending on the continuity of cartilage throughout the circumference of the tracheal rings and compliance values, thus correlating form and function in a more complete descriptive manner.…”

“…Additionally, the contribution of peritracheal and endotracheal tissue properties (e.g. engorgement of endotracheal venous plexus) was not investigated (Cozzi et al, 2005;Costidis and Rommel, 2012). Thus, the tracheal compliance in live animals may prove to be different.…”

“…Simple morphological comparisons between shallow diving species of cetacean and deep diving cetaceans (beaked whales) may not be appropriate, as they have demonstrated vastly different dive behavior. In addition, other anatomical features of the trachea may affect compliance; for example, connective tissue or the endotracheal venous plexus, which may fill and displace the intra-tracheal air volume (Cozzi et al, 2005;Costidis and Rommel, 2012). It would make sense that associated tissues as well as engorgement would affect compliance in measurements taken in situ rather than in excised tracheas.…”

“…Given the predicted lung volumes and diffusion rates, theoretical models (Bostrom et al, 2008) allow predictions as to how pressure affects the volume in the various compartments of the respiratory system and how physiologic pulmonary shunts might develop. However, these models are influenced by compliance estimates for the various portions of the respiratory system and little mechanical information currently exists for the upper airways of marine mammals (Sokolov et al, 1968;Cozzi et al, 2005;Bagnoli et al, 2011), making predictions for respiratory changes uncertain.…”