Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper accelerations of bottlenose dolphins (Tursiops truncatus) and Weddell seals (Leptonychotes weddellii) diving from the surface to 4200 m. Here we report that both exercise and depth alter the bradycardia associated with the dive response, with the greatest impacts at depths inducing lung collapse. Unexpectedly, cardiac arrhythmias occurred in 473% of deep, aerobic dives, which we attribute to the interplay between sympathetic and parasympathetic drivers for exercise and diving, respectively. Such marked cardiac variability alters the common view of a stereotypic 'dive reflex' in diving mammals. It also suggests the persistence of ancestral terrestrial traits in cardiac function that may help explain the unique sensitivity of some deep-diving marine mammals to anthropogenic disturbances.
Heat transfer from the periphery is in important thermoregulatory response in exercising mammals. However, when marine mammals submerge, peripheral vasoconstriction associated with the dive response may preclude heat dissipation at depth. To determine the effects of exercise and diving on thermoregulation in cetaceans, we measured heat flow and skin temperatures of bottlenose dolphins (Tursiops truncatus) trained to follow a boat and to dive to 15 m. The results demonstrated that skin temperatures usually remained within 1 degree C of the water after all exercise levels. Heat flow from peripheral sites (dorsal fin and flukes) increased over resting values immediately after exercise at the water surface and remained elevated for up to 20 min. However, post-exercise values for heat flow from the flukes and dorsal fin decreased by 30-67% when dolphins stationed at 15 m below the surface. The pattern in heat flow was reversed during ascent. For example, mean heat flow from the flukes measured at 5 m depth, 40.10 +/- 2.47 W.m-2, increased by 103.2% upon ascent. There is some flexibility in the balance between thermal and diving responses of dolphins. During high heat loads, heat transfer may momentarily increase during submergence. However, the majority of excess heat in dolphins appears to be dissipated upon resurfacing, thereby preserving the oxygen-conserving benefits of the dive response.
During diving, marine mammals must balance the conservation of limited oxygen reserves with the metabolic costs of swimming exercise. As a result, energetically efficient modes of locomotion provide an advantage during periods of submergence and will presumably increase in importance as the animals perform progressively longer dives. To determine the effect of a limited oxygen supply on locomotor performance, we compared the kinematics and behavior of swimming and diving bottlenose dolphins. Adult bottlenose dolphins (Tursiops truncatus) were trained to swim horizontally near the water surface or submerged at 5 m and to dive to depths ranging from 12 to 112 m. Swimming kinematics (preferred swimming mode, stroke frequency and duration of glides) were monitored using submersible video cameras (Sony Hi-8) held by SCUBA divers or attached to a pack on the dorsal fin of the animal. Drag and buoyant forces were calculated from patterns of deceleration for horizontally swimming and vertically diving animals. The results showed that dolphins used a variety of swimming gaits that correlated with acceleration. The percentage of time spent gliding during the descent phase of dives increased with depth. Glide distances ranged from 7.1+/−1.9 m for 16 m dives to 43.6+/−7.0 m (means +/− s.e.m.) for 100 m dives. These gliding patterns were attributed to changes in buoyancy associated with lung compression at depth. By incorporating prolonged glide periods, the bottlenose dolphin realized a theoretical 10–21 % energetic savings in the cost of a 100 m dive in comparison with dives based on neutral buoyancy models. Thus, modifying locomotor patterns to account for physical changes with depth appears to be one mechanism that enables diving mammals with limited oxygen stores to extend the duration of a dive.
During diving, marine mammals initiate a series of cardiovascular changes that include bradycardia and decreased peripheral circulation. Because heat transfer from thermal windows located in peripheral sites of these mammals depends on blood flow, such adjustments may limit their thermoregulatory capabilities during submergence. Here, we demonstrate how the thermoregulatory responses of bottlenose dolphins (Tursiops truncatus) are coordinated with the diving response. Heart rate, skin temperature and heat transfer from the dorsal fin and flank were measured while dolphins rested on the water surface, stationed 5–50 m under water and floated at the surface immediately following a dive. The results showed that heat flow ranged from 42.9+/−7.3 to 126.2+/−23.1 W m(−)(2) and varied with anatomical site and diving activity. Upon submergence, heat flow declined by 35 % from the dorsal fin and by 24 % from the flank. An immediate increase in heat flow to levels exceeding pre-dive values occurred at both sites upon resurfacing. Changes in heart rate during diving paralleled the thermoregulatory responses. Mean pre-dive heart rate (102.0+/−2.6 beats min(−)(1), N=26) decreased by 63.4 % during dives to 50 m and immediately returned to near resting levels upon resurfacing. These studies indicate that heat dissipation by dolphins is attenuated during diving. Rather than challenge the diving response, heat transfer is delayed until post-dive periods when the need for oxygen conservation is reduced.
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