A comparative analysis of marine mammal tracheas

Abstract

In 1940, Scholander suggested that stiffened upper airways remained open and received air from highly compressible alveoli during marine mammal diving. There are few data available on the structural and functional adaptations of the marine mammal respiratory system. The aim of this research was to investigate the anatomical (gross) and structural (compliance) characteristics of excised marine mammal tracheas. Here, we defined different types of tracheal structures, categorizing pinniped tracheas by varying degrees of continuity of cartilage (categories 1-4) and cetacean tracheas by varying compliance values (categories 5A and 5B). Some tracheas fell into more than one category along their length; for example, the harbor seal (Phoca vitulina) demonstrated complete rings cranially, and as the trachea progressed caudally, tracheal rings changed morphology. Dolphins and porpoises had less stiff, more compliant spiraling rings while beaked whales had very stiff, less compliant spiraling rings. The pressure-volume (P-V) relationships of isolated tracheas from different species were measured to assess structural differences between species. These findings lend evidence for pressure-induced collapse and re-inflation of lungs, perhaps influencing variability in dive depth or ventilation rates of the species investigated.

Respiratory function and mechanics in pinnipeds and cetaceans

“…However, these differences in the terminal airways did not result in a marked difference in the pressure-related pulmonary shunt during forced dives in a pressure chamber (Kooyman and Sinnett, 1982). One explanation may be the significant variation in compliance estimates of the upper airways between species (Bagnoli et al, 2011;Davenport et al, 2013;Moore et al, 2014). A comparative study showed that deep-diving pinnipeds have a more compliant trachea as compared with more shallow-diving species whereas deep-diving cetaceans have a stiffer trachea than shallow-diving cetaceans .…”

“…The relationship between estimated total lung capacity (TLC est ; broken line, Kooyman, 1973) and M b for marine mammals reveals that the volume of most breaths of marine mammals is not close to the vital capacity of the animal. References: bottlenose dolphin (Fahlman et al, 2015b), gray seal (Reed et al, 1994), Weddell seal (Kooyman et al, 1971), harbor porpoise (Reed et al, 2000), California sea lion (Kerem et al, 1975;Matthews, 1977), pilot whale (Olsen et al, 1969), killer whale (Spencer et al, 1967;Kasting et al, 1989), beluga whale (Kasting et al, 1989;Epple et al, 2015), walrus (Fahlman et al, 2015a), Patagonia sea lion (Fahlman and Madigan, 2016) Denison and Kooyman, 1973;Kooyman, 1973;Tarasoff and Kooyman, 1973;Leith, 1976;Kooyman and Sinnett, 1979;Kooyman and Cornell, 1981;Fahlman et al, 2011Fahlman et al, , 2014Fahlman et al, , 2015bMoore et al, 2011Moore et al, , 2014. Studies using trained marine mammals that voluntarily participate have been used to define flowvolume characteristics (Olsen et al, 1969;Kooyman and Cornell, 1981;Fahlman et al, 2015b;Fahlman and Madigan, 2016).…”

“…Marine mammals are reported to have reinforced airways (Kooyman and Sinnett, 1982), and there appears to be significant variability between orders and species (Wislocki, 1929(Wislocki, , 1942Bélanger, 1940;Wislocki and Belanger, 1940;Goudappel and Slijper, 1958;Denison and Kooyman, 1973;Henk and Haldiman, 1990;Wessels and Chase, 1998;Ninomiya et al, 2005;Bagnoli et al, 2011). In the sea lion and cetaceans, the cartilaginous reinforcement extends down to the entrance of the alveoli or alveolar sac -there are no respiratory bronchioleswhereas in the seal the last few millimeters of the conducting airway are reinforced with muscle and appear to be much more compliant (Tarasoff and Kooyman, 1973;Cozzi et al, 2005;Bagnoli et al, 2011;Moore et al, 2014). As discussed above, Scholander (1940) proposed that the cartilaginous reinforcement prevents the compression of the airway, facilitating alveolar collapse and cessation of gas exchange, and preventing excessive N 2 uptake (Fig.…”

“…Piscitelli et al, 2013), but these reviews focus on the structural properties of excised tissues, which may not always reflect the functional properties of live animals (Kooyman, 1973;Ponganis, 2015). For example, compliance estimates of excised tissues do not account for the influence of surrounding structures that encase the respiratory system (Cozzi et al, 2005;Fahlman et al, 2011Fahlman et al, , 2014Moore et al, 2014). Likewise, pulmonary volume changes during compression of entire dead specimens cannot account for the potential effects of blood engorgement of the tracheal mucosa in cetaceans (Leith, 1976;Cozzi et al, 2005;Davenport et al, 2013).…”

Lung mechanics and pulmonary function testing in cetaceans

“…Despite the value of these theoretical studies, the results should be interpreted with caution, as the current understanding of how gas exchange is affected by compression of the respiratory system is rudimentary at best. Recent studies suggest that there is considerable structural (anatomical) and functional (compliance) variability in the upper and lower airways of different orders, families and species of marine mammals (Moore et al, 2014;Piscitelli et al, 2010Piscitelli et al, , 2013.…”