How man-made interference might cause gas bubble emboli in deep diving whales

Abstract

Recent cetacean mass strandings in close temporal and spatial association with sonar activity has raised the concern that anthropogenic sound may harm breath-hold diving marine mammals. Necropsy results of the stranded whales have shown evidence of bubbles in the tissues, similar to those in human divers suffering from decompression sickness (DCS). It has been proposed that changes in behavior or physiological responses during diving could increase tissue and blood N2 levels, thereby increasing DCS risk. Dive data recorded from sperm, killer, long-finned pilot, Blainville's beaked and Cuvier's beaked whales before and during exposure to low- (1-2 kHz) and mid- (2-7 kHz) frequency active sonar were used to estimate the changes in blood and tissue N2 tension (PN2 ). Our objectives were to determine if differences in (1) dive behavior or (2) physiological responses to sonar are plausible risk factors for bubble formation. The theoretical estimates indicate that all species may experience high N2 levels. However, unexpectedly, deep diving generally result in higher end-dive PN2 as compared with shallow diving. In this focused review we focus on three possible explanations: (1) We revisit an old hypothesis that CO2, because of its much higher diffusivity, forms bubble precursors that continue to grow in N2 supersaturated tissues. Such a mechanism would be less dependent on the alveolar collapse depth but affected by elevated levels of CO2 following a burst of activity during sonar exposure. (2) During deep dives, a greater duration of time might be spent at depths where gas exchange continues as compared with shallow dives. The resulting elevated levels of N2 in deep diving whales might also make them more susceptible to anthropogenic disturbances. (3) Extended duration of dives even at depths beyond where the alveoli collapse could result in slow continuous accumulation of N2 in the adipose tissues that eventually becomes a liability.

Keywords: cetacean; diving physiology; modeling.

Figure 1

Conceptual model of risk of gas embolism in deep diving mammals. The descent and ascent of deep dives goes through three different depth ranges representing different risk of gas bubble embolism (Kvadsheim et al., 2012). The Shallow N₂ removal region where N₂ is excreted because the partial pressure of N₂ in the tissue is higher than the ambient hydrostatic pressure [P_N2(tiss) > P_N2(amb)], the Intermediate N₂ absorption region where N₂ is absorbed because the ambient partial pressure of N₂ is higher than in the tissue [P_N2(tiss) < P_N2(amb)], and the Deep constant body N₂ region where N₂ is neither absorbed nor excreted in the lungs (no gas exchange) because of alveolar collapse. The gas exchange model used in this paper suggests that the Deep constant body N₂ region starts when the alveoli are completely collapsed at 180–220 m, depending on species, and extend downward as deep as the animal might dive. The depth range of the Shallow N₂ removal region (decompression zone) will constantly vary depending on the P_N2 level of the tissue, and thus the dive history of the animal. It might be restricted to just the surface or extend down to depths of 20–30 m if the animal has a high P_N2 level built up during previous dives. The risk of gas bubble embolism depends on the saturation level, which is determined by the P_N2in the tissue and the hydrostatic pressure. N₂ levels in the tissue will increase if more time is spent in the Intermediate N₂ absorption region and less time in the Shallow N₂ removal region. Time spent in the Deep constant body N₂ region, does not add to the total body nitrogen, but the extended duration of the deep dives allows for transfer of N₂ into poorly perfused slow tissues such as blubber, where it might accumulate to dangerous levels. Gas embolism will only occur in supersaturated tissues and because this requires a low hydrostatic pressure, it only occurs in the Shallow N₂ removal region, including the surface. Thus, the Intermediate N₂ absorption region is where N₂ is absorbed, but the Shallow N₂ removal region is what represents the immediate risk of gas embolism. See text for further details Illustration IAN, FFI.

Figure 2

Average (Δ) and maximum (o) change in risk {risk = [P_venN2 − P_N2(amb)]} during 1–2 kHz LFAS (left) or 6–7 kHz MFAS (right) sonar exposure compared to control in behaviorally responding sperm whales. Data are modified from Kvadsheim et al. (2012).