Hypoxia Tolerance in the Epaulette Shark (Hemiscyllium ocellatum)

The epaulette shark, Hemiscyllium ocellatum, is a tropical reef shark that can live in an environment with cyclic periods of low oxygen concentration, suggesting that it has a well-developed capacity for anaerobic metabolism. Most investigations of hypoxia-tolerant teleosts and reptiles have focused on species that inhabit cold environments. This study was carried out on a tropical reef shark in order to determine whether similar strategies for hypoxia survival are used at higher environmental temperatures. We studied the effects of a single exposure to mild hypoxia and cyclic exposure to extreme hypoxia on blood-lactate concentration and key indicators of neurological function. The basal blood-lactate concentration for the epaulette shark was determined as 0.37 mM and showed a graded increase during hypoxia. After a single exposure to mild hypoxia (20% of normoxia for 4 h), the mean blood-lactate level rose to 3.07 mM (P < 0.01). After cyclic exposure to extreme hypoxia (eight repetitions of a 120-min exposure at 5% of normoxia), there was a rise in mean blood-lactate concentration to 5.43 mM (P < 0.0001). During both hypoxic regimens, there were no observed changes in key indicators of neurological function. We conclude that the epaulette shark is tolerant to both mild hypoxia and to cyclic exposure to extreme hypoxia. J. Exp. Zool. 281:1–5, 1998. © 1998 Wiley-Liss, Inc. The epaulette shark, Hemiscyllium ocellatum (Bonnaterre, 1877), is an Australasian benthic reef shark that inhabits the shallow reef flats surrounding the islands of the Great Barrier Reef and the Torres Strait (Dingerkus and DeFino, ’83; Last and Stevens, ’94). This shark was studied at Heron Island, which is located in the Capricorn Bunker group of islands, on the Great Barrier Reef, situated off the northeastern coast of Australia. During a low tide at night, the water on the reef flat immediately surrounding the island does not mix with the surrounding ocean. Consequently, the respiration of coral, algae, and reef animals can lower the oxygen concentration from the normoxic level of 6.8 mg O2/L to a hypoxic level of 2.1 mg O2/L (Kinsey and Kinsey, ’67). The survival of the epaulette shark on the reef flat in a naturally cycling hypoxic environment indicates that this shark may have a large capacity for anaerobic metabolism to avoid hypoxic damage. The metabolic and neurological responses of teleost fish to hypoxia and anoxia have been examined in the hypoxia-susceptible rainbow trout (Oncorhynchus mykiss) and in the hypoxia-tolerant crucian carp (Carassius carassius). The brain of rainbow trout loses its neuronal ion-gradients after 30 min of anoxia (Nilsson et al., ’93), whereas *Correspondence to: Dr. Gillian Renshaw, Vertebrate Neurobiology and Cell Biology Laboratory, Department of Anatomical Sciences, The University of Queensland, St. Lucia 4072, QLD, Australia. E-mail: [email protected] Received 3 June 1997; Accepted 16 December 1997 the crucian carp can survive anoxia for several days (Nilsson et al., ’91). The differences between tolerant and nontolerant species are in part due to the increased capacity for anaerobic metabolism of tolerant species. Most investigations into the hypoxia-tolerance of teleost fishes and turtles have focused on species that inhabit cold environments. The crucian carp can survive hypoxic periods of up to 5.5 months in ice-locked lakes (Blazka, ’58). Similarly, the freshwater turtle, Chrysemys picta bellii, overwinters beneath frozen water-courses for up to 3.5 months (Ultsch, ’89). However, hypoxia tolerance is reduced with increasing temperature (Herbert and Jackson, ’85a,b; Kam and Lillywhite, ’94). Many tolerant species show a preference for lower temperatures when they are placed in a hypoxic environment (Branco et al., ’93; O’Connor et al., ’88). The survival of the epaulette shark in a hypoxic tropical environment indicates that it may provide a useful model for examining the physiological mechanisms underlying hypoxia-tolerance.