Ontogenetic changes in tracheal structure facilitate deep dives and cold water foraging in adult leatherback sea turtles

Abstract

SUMMARYAdult leatherbacks are large animals (300-500kg), overlapping in size with marine pinniped and cetacean species. Unlike marine mammals, they start their aquatic life as 40-50g hatchlings, so undergo a 10,000-fold increase in body mass during independent existence. Hatchlings are limited to the tropics and near-surface water. Adults, obligate predators on gelatinous plankton, encounter cold water at depth (<1280m) or high latitude and are gigantotherms that maintain elevated core body temperatures in cold water. This study shows that there are great ontogenetic changes in tracheal structure related to diving and exposure to cold. Hatchling leatherbacks have a conventional reptilian tracheal structure with circular cartilaginous rings interspersed with extensive connective tissue. The adult trachea is an almost continuous ellipsoidal cartilaginous tube composed of interlocking plates, and will collapse easily in the upper part of the water column during dives, thus avoiding pressure-related structural and physiological problems. It is lined with an extensive, dense erectile vascular plexus that will warm and humidify cold inspired air and possibly retain heat on expiration. A sub-luminal lymphatic plexus is also present. Mammals and birds have independently evolved nasal turbinates to fulfil such a respiratory thermocontrol function; for them, turbinates are regarded as diagnostic of endothermy. This is the first demonstration of a turbinate equivalent in a living reptile.

Penguin lungs and air sacs: implications for baroprotection, oxygen stores and buoyancy

“…There are also other potential compensatory mechanisms to avoid tracheal barotrauma. Submucosal veins in the walls of cetacean and sea turtle tracheas have been postulated to become engorged at depth, thus decreasing tracheal volume and providing protection (Cozzi et al, 2005;Davenport et al, 2013Davenport et al, , 2009Davenport et al, , 2014Ninomiya et al, 2005). It is unknown whether such submucosal venous plexuses exist in the tracheal walls of penguins.…”

Behaviour and buoyancy regulation in the deepest-diving reptile: the leatherback turtle

“…Leatherbacks seem to fit the pattern shown by some marine mammals such as the northern bottlenose whale, Hyperoodon ampullatus (Hooker and Baird, 1999), and the beluga whale, Delphinapterus leucas (Martin and Smith, 1992), of diving upon inhalation and performing slow ascents to help reduce the risks of decompression sickness. This behavioural mechanism is coupled to several physical -for example, small collapsible lungs and compressible trachea (Lutcavage and Lutz, 1997;Davenport et al, 2009) -and physiological -for example, large blood and muscle oxygen stores (Lutcavage et al, 1992) and cardiovascular adjustments during diving (Southwood et al, 1999) -adaptations that might decrease the susceptibility of animals to the bends (Kooyman and Ponganis, 1998;Fahlman et al, 2006). However, body angles and vertical velocities during the ascent increased with increasing maximum depth, contradicting this hypothesis.…”

“…The only true deep-diving marine reptile (defined here as exploiting typical mean dive depths ≥100m) is the leatherback turtle, Dermochelys coriacea (Vandelli 1761), which is also the largest and most morphologically and physiologically distinct of the sea turtles. The thin flexible cartilaginous carapace and highly reduced plastron (Wood et al, 1996;Wyneken, 2001) in addition to compliant chest walls (Lutcavage and Lutz, 1997), compressible, cartilaginous tracheal tube (Davenport et al, 2009) and small collapsible lungs [i.e. relative to hard-shelled turtles (Lutcavage and Lutz, 1997)] are probably adaptations to the impressive diving abilities of this species.…”

Behavioral and metabolic contributions to thermoregulation in freely swimming leatherback turtles at high latitudes

“…Vascular heat exchangers at the base of the flippers (Greer et al, 1973) and blood flow adjustments (Bostrom et al, 2010) permit tight control of heat loss at the extremities, and a vascular plexus lining the trachea minimizes respiratory heat loss (Davenport et al, 2009b). In order to maintain a steady T b in cold water, the rate at which heat is lost to the environment must be matched by the rate of heat gain.…”