The dive response redefined: underwater behavior influences cardiac variability in freely diving dolphins

Abstract

SUMMARYA hallmark of the dive response, bradycardia, promotes the conservation of onboard oxygen stores and enables marine mammals to submerge for prolonged periods. A paradox exists when marine mammals are foraging underwater because activity should promote an elevation in heart rate (f H ) to support increased metabolic demands. To assess the effect of the interaction between the diving response and underwater activity on f H , we integrated interbeat f H with behavioral observations of adult bottlenose dolphins diving and swimming along the coast of the Bahamas. As expected for the dive response, f H while resting during submergence (40±6beatsmin , and occurred during post-dive surface intervals. During submergence, the level of bradycardia was modified by activity. Behaviors such as simple head bobbing at depth increased f H by 40% from submerged resting levels. Higher heart rates were observed for horizontal swimming at depth. Indeed, the dolphins operated at 37-58% of their f H,max while active at depth and approached 57-79% of their f H,max during anticipatory tachycardia as the animals glided to the surface. f H was significantly correlated with stroke frequency (range0-2.5strokess -1 , r0.88, N25 dives) and calculated swim speed (range0-5.4ms -1 , r0.88, N25 dives). We find that rather than a static reflex, the dive response is modulated by behavior and exercise in a predictable manner.

Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals

“…To record ECGs, two suction cup electrodes (5 cm diameter with a 2-cm diameter silver plate electrode) were placed on the sternum of the dolphins directly below the pectoral fin insertions, and above the right scapula according to Noren et al 8 For the Weddell seals, two 2 cm diameter silver electrodes were placed on shaved areas of skin in lateral and ventral axillary areas, and covered with neoprene patches glued to the fur. Shielded wires soldered to the electrodes were connected to the monitors and enabled ECG waveforms to be recorded continuously throughout the experimental sessions ( Supplementary Fig.…”

“…This was verified by manual calculation of r-r intervals for each heart beat within segments of the time-stamped ECG trace containing arrhythmias. In contrast to previous analyses 7,8 , transition periods during ascent and descent were examined in addition to the steady-state exercise responses while swimming at depth. To make the data sets comparable between species, we limited the ECG analyses to dives that remained within reported species-specific calculated aerobic dive limits [2][3][4] .…”

“…As a result, the potential for conflict between diving and exercise responses for air-breathing marine predators has remained a long-standing debate [6][7][8] . The expectation is that marine mammals are adapted for underwater exercise, and thereby uniquely safeguarded from submersion-related injuries that occur in terrestrial species 9 .…”

DIVING IN A WARMING WORLD: Thermal constraints on the diving capacity of estuarine crocodiles (Crocodylus porosus)

“…However, several studies have rejected this hypothesis, with the view that an adaptive function of the PBS may not exist (Hicks, 2002;Eme et al, 2009;Hicks and Wang, 2012). The initiation of the 'dive response' appears to be context specific in some species (Gaunt and Gans, 1969;Noren et al, 2012); with crocodylians, for example, markedly reducing heart rate (65 ± 6% reduction) during predator avoidance dives (i.e. 'fright-dives') and only small cardiovascular changes (14 ± 6% reduction) accompanying voluntary, undisturbed dives (Wright et al, 1992).…”

“…These alterations facilitate prolonged submergences by lowering oxygen demands and animals enter a hypometabolic state where oxygen demands are lower than surface metabolic rates (Davis et al, 2004;Hastie et al, 2007). The initiation of the 'dive response' appears to be context specific in some species (Gaunt and Gans, 1969;Noren et al, 2012); with crocodylians, for example, markedly reducing heart rate (65 ± 6% reduction) during predator avoidance dives (i.e. 'fright-dives') and only small cardiovascular changes (14 ± 6% reduction) are observed during voluntary, undisturbed dives (Wright et al, 1992).…”