Andreas Fahlman

Deadly diving? Physiological and behavioural management of decompression stress in diving mammals

Decompression sickness (DCS; ‘the bends’) is a disease associated with gas uptake at pressure. The basic pathology and cause are relatively well known to human divers. Breath-hold diving marine mammals were thought to be relatively immune to DCS owing to multiple anatomical, physiological and behavioural adaptations that reduce nitrogen gas (N2) loading during dives. However, recent observations have shown that gas bubbles may form and tissue injury may occur in marine mammals under certain circumstances. Gas kinetic models based on measured time-depth profiles further suggest the potential occurrence of high blood and tissue N2 tensions. We review evidence for gas-bubble incidence in marine mammal tissues and discuss the theory behind gas loading and bubble formation. We suggest that diving mammals vary their physiological responses according to multiple stressors, and that the perspective on marine mammal diving physiology should change from simply minimizing N2 loading to management of the N2 load. This suggests several avenues for further study, ranging from the effects of gas bubbles at molecular, cellular and organ function levels, to comparative studies relating the presence/absence of gas bubbles to diving behaviour. Technological advances in imaging and remote instrumentation are likely to advance this field in coming years.

Estimating the effect of lung collapse and pulmonary shunt on gas exchange during breath-hold diving: The Scholander and Kooyman legacy

We developed a mathematical model to investigate the effect of lung compression and collapse (pulmonary shunt) on the uptake and removal of O(2), CO(2) and N(2) in blood and tissue of breath-hold diving mammals. We investigated the consequences of pressure (diving depth) and respiratory volume on pulmonary shunt and gas exchange as pressure compressed the alveoli. The model showed good agreement with previous studies of measured arterial O(2) tensions (Pa(O)(2)) from freely diving Weddell seals and measured arterial and venous N(2) tensions from captive elephant seals compressed in a hyperbaric chamber. Pulmonary compression resulted in a rapid spike in Pa(O)(2) and arterial CO(2) tension, followed by cyclical variation with a periodicity determined by Q(tot). The model showed that changes in diving lung volume are an efficient behavioural means to adjust the extent of gas exchange with depth. Differing models of lung compression and collapse depth caused major differences in blood and tissue N(2) estimates. Our integrated modelling approach contradicted predictions from simple models, and emphasised the complex nature of physiological interactions between circulation, lung compression and gas exchange. Overall, our work suggests the need for caution in interpretation of previous model results based on assumed collapse depths and all-or-nothing lung collapse models.

Deep diving mammals: Dive behavior and circulatory adjustments contribute to bends avoidance

A mathematical model was created that predicted blood and tissue N(2) tension (P(N2)) during breath-hold diving. Measured muscle P(N2) from the bottlenose dolphin after diving repeatedly to 100 m (Tursiops truncatus [Ridgway and Howard, 1979, Science, 4423, 1182-1183]) was compared with predictions from the model. Lung collapse was modelled as a 100% pulmonary shunt which yielded tissue P(N2) similar to those reported for the dolphin. On the other hand, predicted muscle P(N2) for an animal with a dive response, reducing cardiac output by 66% from surface values (20.5 to 6.8l x min(-1)), also agreed well with observed values in the absence of lung collapse. In fact, modelling indicated that both cardiovascular adjustments and dive behaviour are important in reducing N2 uptake during diving and enhancing safe transfer of tissue and blood N2 back to the lung immediately before coming to the surface. In particular, diving bradycardia during the descent and bottom phase together with a reduced ascent rate and increase in heart rate reduced mixed venous P(N2) upon return to the surface by as much as 45%. This has important implications as small reductions in inert gas load (approximately 5%) can substantially reduce decompression sickness (DCS) risk by as much as 50% (Fahlman et al., 2001, J. Appl. Physiol. 91, 2720-2729).

Tracheal compression delays alveolar collapse during deep diving in marine mammals

Marine mammals have very compliant alveoli and stiff upper airways; an adaptation that allows air to move from the alveoli into the upper airways, during breath-hold diving. Alveolar collapse is thought occur between 30 and 100 m and studies that have attempted to estimate gas exchange at depth have used the simplifying assumption that gas exchange ceases abruptly at the alveolar collapse depth. Here we develop a mathematical model that uses compliance values for the alveoli and upper airspaces, estimated from the literature, to predict volumes of the respiratory system at depth. Any compressibility of the upper airways decreases the volume to contain alveolar air yielding lung collapse pressures 2x that calculated assuming an incompressible upper airway. A simple relationship with alveolar volume was used to predict relative pulmonary shunt at depth. The results from our model agree with empirical data on gas absorption at depth as well as the degree of tracheal compression in forced and free diving mammals.

Could beaked whales get the bends? Effect of diving behaviour and physiology on modelled gas exchange for three species: Ziphius cavirostris, Mesoplodon densirostris and Hyperoodon ampullatus.

A mathematical model, based on current knowledge of gas exchange and physiology of marine mammals, was used to predict blood and tissue tension N2 (P(N2)) using field data from three beaked whale species: northern bottlenose whales, Cuviers beaked whales, and Blainvilles beaked whales. The objective was to determine if physiology (body mass, diving lung volume, dive response) or dive behaviour (dive depth and duration, changes in ascent rate, diel behaviour) would lead to differences in P(N2) levels and thereby decompression sickness (DCS) risk between species. Diving lung volume and extent of the dive response had a large effect on end-dive P(N2). The dive profile had a larger influence on end-dive P(N2) than body mass differences between species. Despite diel changes in dive behaviour, P(N2) levels showed no consistent trend. Model output suggested that all three species live with tissue P(N2) levels that would cause a significant proportion of DCS cases in terrestrial mammals. Cuviers beaked whale diving behaviour appears to put them at higher risk than the other species, which may explain their prevalence in strandings after the use of mid-frequency sonar.

Patterns of respiration in diving penguins: is the last gasp an inspired tactic?

SUMMARY Humboldt penguins Spheniscus humboldti in captivity and free-living Magellanic penguins S. magellanicus were fitted with loggers to determine beak angles during breathing. The Humboldt penguins were also fitted with masks for determining rates of air flow during breathing. During periods of higher gas exchange requirement, Humboldt penguins opened their beaks during inspiration, where tidal volume was linearly correlated with both change in beak angle and maximum beak angle, closed them slightly during the final stages of inspiration and finally closed them during expiration. Substantial differences were apparent between individuals. Contrary to the condition proposed for most birds, our data suggest that expiration is passive during periods of high respiratory tidal volumes, and that the increased resistance of the respiratory pathway serves to slow air flow so as to maximize gas exchange in the lungs. During foraging, Magellanic penguins at the surface between dives showed similar breathing patterns but maximum beak angles were much higher and breath cycle time shorter, as would be expected for animals attempting to maximize gas exchange. Both maximum beak angle per breath and breath frequency changed systematically over the surface pause; both were initially high, then decreased to a low before rising again to a maximum just before diving. Based on known changes in tidal volume with beak angle derived from Humboldt penguins, a simple model is proposed to examine rates of gas exchange over the surface pause. This indicates that the observed patterns do not maximize the rate of transfer of oxygen over the whole of the surface pause but are rather concerned with an initial rapid accumulation of oxygen in the tissues followed by effective carbon dioxide release.

Hyperbaric computed tomographic measurement of lung compression in seals and dolphins.

SUMMARY Lung compression of vertebrates as they dive poses anatomical and physiological challenges. There has been little direct observation of this. A harbor and a gray seal, a common dolphin and a harbor porpoise were each imaged post mortem under pressure using a radiolucent, fiberglass, water-filled pressure vessel rated to a depth equivalent of 170 m. The vessel was scanned using computed tomography (CT), and supported by a rail and counterweighted carriage magnetically linked to the CT table movement. As pressure increased, total buoyancy of the animals decreased and lung tissue CT attenuation increased, consistent with compression of air within the lower respiratory tract. Three-dimensional reconstructions of the external surface of the porpoise chest showed a marked contraction of the chest wall. Estimation of the volumes of different body compartments in the head and chest showed static values for all compartments except the lung, which showed a pressure-related compression. The depth of estimated lung compression ranged from 58 m in the gray seal with lungs inflated to 50% total lung capacity (TLC) to 133 m in the harbor porpoise with lungs at 100% TLC. These observations provide evidence for the possible behavior of gas within the chest of a live, diving mammal. The estimated depths of full compression of the lungs exceeds previous indirect estimates of the depth at which gas exchange ceases, and concurs with pulmonary shunt measurements. If these results are representative for living animals, they might suggest a potential for decompression sickness in diving mammals.

Changes in dive behavior during naval sonar exposure in killer whales, long-finned pilot whales, and sperm whales.

Anthropogenic underwater sound in the environment might potentially affect the behavior of marine mammals enough to have an impact on their reproduction and survival. Diving behavior of four killer whales (Orcinus orca), seven long-finned pilot whales (Globicephala melas), and four sperm whales (Physeter macrocephalus) was studied during controlled exposures to naval sonar [low frequency active sonar (LFAS): 1–2 kHz and mid frequency active sonar (MFAS): 6–7 kHz] during three field seasons (2006–2009). Diving behavior was monitored before, during and after sonar exposure using an archival tag placed on the animal with suction cups. The tag recorded the animals vertical movement, and additional data on horizontal movement and vocalizations were used to determine behavioral modes. Killer whales that were conducting deep dives at sonar onset changed abruptly to shallow diving (ShD) during LFAS, while killer whales conducting deep dives at the onset of MFAS did not alter dive mode. When in ShD mode at sonar onset, killer whales did not change their diving behavior. Pilot and sperm whales performed normal deep dives (NDD) during MFAS exposure. During LFAS exposures, long-finned pilot whales mostly performed fewer deep dives and some sperm whales performed shallower and shorter dives. Acoustic recording data presented previously indicates that deep diving (DD) is associated with feeding. Therefore, the observed changes in dive behavior of the three species could potentially reduce the foraging efficiency of the affected animals.

Bubbles in live-stranded dolphins

Bubbles in supersaturated tissues and blood occur in beaked whales stranded near sonar exercises, and post-mortem in dolphins bycaught at depth and then hauled to the surface. To evaluate live dolphins for bubbles, liver, kidneys, eyes and blubber–muscle interface of live-stranded and capture-release dolphins were scanned with B-mode ultrasound. Gas was identified in kidneys of 21 of 22 live-stranded dolphins and in the hepatic portal vasculature of 2 of 22. Nine then died or were euthanized and bubble presence corroborated by computer tomography and necropsy, 13 were released of which all but two did not re-strand. Bubbles were not detected in 20 live wild dolphins examined during health assessments in shallow water. Off-gassing of supersaturated blood and tissues was the most probable origin for the gas bubbles. In contrast to marine mammals repeatedly diving in the wild, stranded animals are unable to recompress by diving, and thus may retain bubbles. Since the majority of beached dolphins released did not re-strand it also suggests that minor bubble formation is tolerated and will not lead to clinically significant decompression sickness.

Bottlenose dolphins modify behavior to reduce metabolic effect of tag attachment.

Attaching bio-telemetry or -logging devices (‘tags’) to marine animals for research and monitoring adds drag to streamlined bodies, thus affecting posture, swimming gaits and energy balance. These costs have never been measured in free-swimming cetaceans. To examine the effect of drag from a tag on metabolic rate, cost of transport and swimming behavior, four captive male dolphins (Tursiops truncatus) were trained to swim a set course, either non-tagged (n=7) or fitted with a tag (DTAG2; n=12), and surface exclusively in a flow-through respirometer in which oxygen consumption () and carbon dioxide production (; ml kg−1 min−1) rates were measured and respiratory exchange ratio (/) was calculated. Tags did not significantly affect individual mass-specific oxygen consumption, physical activity ratios (exercise /resting ), total or net cost of transport (COT; J m−1 kg−1) or locomotor costs during swimming or two-minute recovery phases. However, individuals swam significantly slower when tagged (by ~11%; mean ± s.d., 3.31±0.35 m s−1) than when non-tagged (3.73±0.41 m s−1). A combined theoretical and computational fluid dynamics model estimating drag forces and power exertion during swimming suggests that drag loading and energy consumption are reduced at lower swimming speeds. Bottlenose dolphins in the specific swimming task in this experiment slowed to the point where the tag yielded no increases in drag or power, while showing no difference in metabolic parameters when instrumented with a DTAG2. These results, and our observations, suggest that animals modify their behavior to maintain metabolic output and energy expenditure when faced with tag-induced drag.