Behavioral, Ventilatory, and Metabolic Responses of the Hypogean Amphipod Niphargus virei and the Epigean Isopod Asellus aquaticus to Severe Hypoxia and Subsequent Recovery

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Abstract
The locomotory and ventilatory activities and the intermediary and energy metabolism modifications of the hypogean amphipod Niphargus virei and the epigean isopod Asellus aquaticus were compared during severe hypoxia (<0.03 kPa) and subsequent recovery. The aims of this study were (1) to determine why the subterranean species displayed a greater tolerance of hypoxia than A. aquaticus and numerous other epigean crustaceans, (2) to confirm previous results obtained with the hypogean amphipod Niphargus rhenorhodanensis and the epigean amphipod Gammarus fossarum, (3) to provide an interspecific comparison of epigean species in order to see if responses showed by epigean amphipods during hypoxia and recovery can be extended to epigean isopods, and (4) to better understand the ecological problems of the hypogean organism's survival and perennation in subterranean habitats. Both organisms responded to long-term experimental severe hypoxia with classical anaerobic metabolism, characterized by a decrease in ATP and phosphagen, the use of glycogen and glutamate, and the accumulation of lactate (with some alanine). In addition, some accumulation of succinate was found in N. virei. Lactate (and succinate for N. virei) was also largely excreted by both amphipods, which is unusual for the crustacea in general Compared with A. aquaticus and most other epigean crustaceans, N. virei showed large amounts of stored glycogen and arginine phosphate. These differences in glycogen and phosphagen stores, and the ability to reduce glycolytic flux and energetic expenditures linked to locomotion and ventilation, extended the survival of hypogean crustaceans under experimental anaerobiosis ( was 52.1 h for N. virei and 19. 7 h for A. aquaticus during severe hypoxia at 11° C). During recovery, both species displayed characteristic hyperventilation, slow locomotory activity, and predominantly aerobic metabolism. Asellus aquaticus excreted a large part of the lactate accumulated during severe hypoxia, whereas N. virei remetabolized it, as it had a higher lactate-derived glyconeogenesis capacity. The disposal of endproducts and replenishing of glycogen, ATP, and phosphagen required more than 24 h for both organisms. Niphargus virei showed a faster and more complete replenishment of ATP and arginine phosphate levels than A. aquaticus. Data concerning locomotory, ventilatory, and metabolic responses to hypoxia and subsequent recovery in N. virei and A. aquaticus are similar to those obtained with N. rhenorhodanensis and G. fossarum.