Bioenergetics of diapause and quiescence in aquatic animals

Abstract

With one exception, all major animal phyla contain species that possess dormant states, a feature that affords tolerance to extreme environmental conditions. Diapause is an obligate, developmentally-programmed form of dormancy that precedes the onset of environmental insult. Calorimetric and respirometric studies reveal that a major metabolic depression accompanies entry into diapause in vertebrates and invertebrates. Under fully aerobic conditions, embryos of the annual fish Austrofundulus limnaeus depress metabolism by approximately 90% over a period of several days as they enter diapause. This metabolic shift is achieved without alteration in ATP:ADP ratio. Breakage of diapause involves a lengthened photoperiod and is accompanied by a 200-fold increase in metabolic rate. Similarly, gemmules of the freshwater sponge Eunapius fragilis display developmental arrest and exhibit low heat dissipation and respiration when in diapause. Upon diapause breakage, germination occurs within 48–72 h. Across this period metabolic rate increases 12-fold, while adenylate status is unchanged; constant adenylates are also noted during diapause in embryos of the brine shrimp, Artemia franciscana. In contrast to diapause, quiescence is a form of dormancy that is a direct response to environmental stress. During anoxia-induced quiescence in A. franciscana embryos, heat dissipation rate drops below 0.2% of the aerobic value within hours of anoxic exposure, and ATP declines by 80% or more during this period. Transcription and translation are markedly depressed in the nucleo-cytoplasmic compartment and within the mitochondrion, and these represent two events in a suite of energy-saving measures. Coordinated depression of catabolic and anabolic processes is a hallmark feature of both diapause and quiescence. However, the adenylate energy status and time interval required for achieving metabolic depression are markedly different between the two conditions.