Under pressure: the extraordinary survival of seal lice in the depth of the sea

Abstract

Lice from pinnipeds – sea lions, seals and walruses – are the only insects capable of surviving marine dives. Throughout their evolutionary history, they have adapted to tolerate hypoxia, high salinity, low temperature and, in particular, to tolerate conditions of high hydrostatic pressure. To understand the limits of the capacity of lice to survive during host deep dives, we conducted a series of controlled experiments in the laboratory. We collected lice from elephant seals and submitted the different life stages to high pressure conditions. Lice were first exposed to one of four hydrostatic pressures: 30, 80, 150 or 200 kg cm−2. They were then exposed a second time to higher or lower hydrostatic pressure conditions to test for the impact of the first experience, which could either be deleterious or trigger physiological adaption, allowing them a better tolerance to high pressure. We found that lice from elephant seals can tolerate hydrostatic pressures higher than 200 kg cm−2 (close to 200 atm), which is equivalent to 2000 m depth. Adults exhibited lower recovery times than nymphs after immersion at high hydrostatic pressure. Our findings show that lice have developed unique adaptations to endure extreme marine conditions. We discuss these extreme performances in relation to the morphological characteristics and physiological responses to diving in these insects.

How Did Seal Lice Turn into the Only Truly Marine Insects?

“…tolerance to high hydrostatic pressure also revealed that adults, which have their bodies fully covered with scales, performed better than nymphs with fewer scales over their bodies [23]. It should be noted, however, that the effects of high hydrostatic pressure would include collapsing air-filled cavities, as tracheal tubes, and, when the pressure is very high, affecting cellular and molecular integrity.…”

“…Secondly, according to Kim (see Figure 343 in [22]), the louse spiracles present an elaborated closing device that could have a double function, i.e., to preserve the atmospheric air into the tracheal system and to prevent the entry of seawater during immersions. However, due to the extremely high hydrostatic pressure seen during deep dives, the tracheal system may entirely collapse [23]; some oxygen could be conserved at a cellular level, either dissolved or associated with (as yet unknown) respiratory pigments. Thus, the elaborated system for closing spiracles would be more related to avoiding the entry of water, rather than retaining air in the tracheal system.…”

“…On the one hand, Leonardi and Lazzari [30] reported that sea lion lice showed higher survival rates and shorter recovery times when they were submerged for variable time periods, between 1 to 15 days, in normoxic rather than in hypoxic water, supporting aquatic respiration and, by extension, Hinton's hypothesis. On the other hand, experiments aimed at determining tolerance to high hydrostatic pressure also revealed that adults, which have their bodies fully covered with scales, performed better than nymphs with fewer scales over their bodies [23]. It should be noted, however, that the effects of high hydrostatic pressure would include collapsing air-filled cavities, as tracheal tubes, and, when the pressure is very high, affecting cellular and molecular integrity.…”

“…The incapacity of N1 to survive underwater was suggested to be associated with the absence of abdominal scales [20,22,27], which are abundantly present in the tolerant instars. When seal lice emerge in seawater, they experience a reduction in oxygen availability, and a rapid and large drop in temperature (20)(21)(22)(23)(24)(25) °C difference between air and water in summer), as well as an increase in hydrostatic pressure. It has been reported that contact with seawater triggers reflex immobility (akinesis) in A. microchir and in L. macrorhini, which is immediate (in seconds) in the former and requires several minutes in the latter [23,30].…”

“…When seal lice emerge in seawater, they experience a reduction in oxygen availability, and a rapid and large drop in temperature (20)(21)(22)(23)(24)(25) °C difference between air and water in summer), as well as an increase in hydrostatic pressure. It has been reported that contact with seawater triggers reflex immobility (akinesis) in A. microchir and in L. macrorhini, which is immediate (in seconds) in the former and requires several minutes in the latter [23,30]. Thus, it seems that the tolerance to immersion depends on a reflex reduction in metabolism and activity (i.e., quiescence) triggered by the physical contact of lice with seawater.…”