High heart rates in hunting harbour porpoises.

The impressive breath-hold capabilities of marine mammals are facilitated by both enhanced O2 stores and reductions in the rate of O2 consumption via peripheral vasoconstriction and bradycardia, called the dive response. Many studies have focused on the extreme role of the dive response in maximizing dive duration in marine mammals, but few have addressed how these adjustments may compromise the capability to hunt, digest and thermoregulate during routine dives. Here, we use DTAGs, which record heart rate together with foraging and movement behaviour, to investigate how O2 management is balanced between the need to dive and forage in five wild harbour porpoises that hunt thousands of small prey daily during continuous shallow diving. Dive heart rates were moderate (median minimum 47-69 bpm) and relatively stable across dive types, dive duration (0.5-3.3 min) and activity. A moderate dive response, allowing for some perfusion of peripheral tissues, may be essential for fuelling the high field metabolic rates required to maintain body temperature and support digestion during diving in these small, continuously feeding cetaceans. Thus, despite having the capacity to prolong dives via a strong dive response, for these shallow-diving cetaceans, it appears to be more efficient to maintain circulation while diving: extreme heart rate gymnastics are for deep dives and emergencies, not everyday use.

Drivers of the dive response in trained harbour porpoises (Phocoena phocoena).

Pronounced dive responses through peripheral vasoconstriction and bradycardia enable prolonged apnoea in marine mammals. For most vertebrates, the dive response is initiated upon face immersion, but little is known about the physical drivers of diving and surfacing heart rate in cetaceans whose faces are always mostly submerged. Using two trained harbour porpoises instrumented with an ECG-measuring sound-and-movement tag (DTAG-3), we investigated the initiation and progression of bradycardia and tachycardia during apnoea and eupnoea for varying levels of immersion. We show that paranasal wetting drives bradycardia initiation and progression, whereas apnoea leads to dive-level bradycardia eventually, but not instantly. At the end of dives, heart rate accelerates independently of lung expansion, perhaps in anticipation of surfacing; however, full tachycardia is only engaged upon inhalation. We conclude that breathing drives surface tachycardia, whereas blowhole wetting is an important driver of bradycardia; however, anticipatory/volitional modulation can overrule such responses to sensory inputs.

Low hunting costs in an expensive marine mammal predator.

Many large terrestrial mammalian predators use energy-intensive, high-risk, high-gain strategies to pursue large, high-quality prey. However, similar-sized marine mammal predators with even higher field metabolic rates (FMRs) consistently target prey three to six orders of magnitude smaller than themselves. Here, we address the question of how these active and expensive marine mammal predators can gain sufficient energy from consistently targeting small prey during breath-hold dives. Using harbor porpoises as model organisms, we show that hunting small aquatic prey is energetically cheap (<20% increase in FMR) for these marine predators, but it requires them to spend a large proportion (>60%) of time foraging. We conclude that this grazing foraging strategy on small prey is viable for marine mammal predators despite their high FMR because they can hunt near continuously at low marginal expense. Consequently, cessation of foraging due to human disturbance comes at a high cost, as porpoises must maintain their high thermoregulation costs with a reduced energy intake.

Wild harbour porpoises startle and flee at low received levels from acoustic harassment device.

Acoustic Harassment Devices (AHD) are widely used to deter marine mammals from aquaculture depredation, and from pile driving operations that may otherwise cause hearing damage. However, little is known about the behavioural and physiological effects of these devices. Here, we investigate the physiological and behavioural responses of harbour porpoises (Phocoena phocoena) to a commercial AHD in Danish waters. Six porpoises were tagged with suction-cup-attached DTAGs recording sound, 3D-movement, and GPS (n = 3) or electrocardiogram (n = 2). They were then exposed to AHDs for 15 min, with initial received levels (RL) ranging from 98 to 132 dB re 1 µPa (rms-fast, 125 ms) and initial exposure ranges of 0.9-7 km. All animals reacted by displaying a mixture of acoustic startle responses, fleeing, altered echolocation behaviour, and by demonstrating unusual tachycardia while diving. Moreover, during the 15-min exposures, half of the animals received cumulative sound doses close to published thresholds for temporary auditory threshold shifts. We conclude that AHD exposure at many km can evoke both startle, flight and cardiac responses which may impact blood-gas management, breath-hold capability, energy balance, stress level and risk of by-catch. We posit that current AHDs are too powerful for mitigation use to prevent hearing damage of porpoises from offshore construction.

Heart rate and startle responses in diving, captive harbour porpoises (Phocoena phocoena) exposed to transient noise and sonar.

Anthropogenic noise can alter marine mammal behaviour and physiology, but little is known about cetacean cardiovascular responses to exposures, despite evidence that acoustic stressors, such as naval sonars, may lead to decompression sickness. Here, we measured heart rate and movements of two trained harbour porpoises during controlled exposure to 6-9 kHz sonar-like sweeps and 40 kHz peak-frequency noise pulses, designed to evoke acoustic startle responses. The porpoises initially responded to the sonar sweep with intensified bradycardia despite unaltered behaviour/movement, but habituated rapidly to the stimuli. In contrast, 40 kHz noise pulses consistently evoked rapid muscle flinches (indicative of startles), but no behavioural or heart rate changes. We conclude that the autonomous startle response appears decoupled from, or overridden by, cardiac regulation in diving porpoises, whereas certain novel stimuli may motivate oxygen-conserving cardiovascular measures. Such responses to sound exposure may contribute to gas mismanagement for deeper-diving cetaceans.

Cognitive control of heart rate in diving harbor porpoises.

Marine mammals have adapted to forage while holding their breath in a suite of aquatic habitats from shallow rivers to deep oceans. The key to tolerate such extensive apnea is the dive response, which comprises bradycardia and peripheral vasoconstriction. Although initially considered an all-or-nothing reflex [1], numerous studies on freely diving marine mammals have revealed substantial dynamics of the dive response to meet the impending dive demands of depth, duration and exercise [2]. Such adjustments are not only autonomic responses, but are under acute cognitive control in pinnipeds [3] living amphibiously on land and in water. The fully aquatic cetaceans would similarly benefit from cognitive cardiovascular control; however, even though they have exercise-modulated diving bradycardia [2] and full voluntary control of their respiratory system to such extent that even mild anesthesia often leads to asphyxiation [4], cognitive cardiovascular control has never been demonstrated for this large group of marine mammals. To address this, we tested the hypothesis that porpoises modulate bradycardia according to anticipated dive duration. Two harbor porpoises, instrumented with ECG recording tags, were trained to perform 20- and 80-second stationary dives, during which they adjusted bradycardia to the anticipated duration, demonstrating cognitive control of their dive response.