Temperature increases induce metabolic adjustments in the early developmental stages of bigfin reef squid (Sepioteuthis lessoniana)

Abstract

Climate changes, such as extreme temperature shifts, can have a direct and significant impact on animals living in the ocean system. Ectothermic animals may undergo concerted metabolic shifts in response to ambient temperature changes. The physiological and molecular adaptations in cephalopods during their early life stages are largely unknown due to the challenge of rearing them outside of a natural marine environment. To overcome this obstacle, we established a pelagic bigfin reef squid (Sepioteuthis lessoniana) culture facility, which allowed us to monitor the effects of ambient thermal elevation and fluctuation on cephalopod embryos/larvae. By carefully observing embryonic development in the breeding facility, we defined 23 stages of bigfin reef squid embryonic development, beginning at stage 12 (blastocyst; 72 h post-egg laying) and continuing through hatching (~1 month post-egg laying). Since temperature recordings from the bigfin reef squid natural habitats have shown a steady rise over the past decade, we examined energy substrate utilization and cellular/metabolic responses in developing animals under different temperature conditions. As the ambient temperature increased by 7 °C, hatching larvae favored aerobic metabolism by about 2.3-fold. Short-term environmental warming stress inhibited oxygen consumption but did not affect ammonium excretion in stage (St.) 25 larvae. Meanwhile, an aerobic metabolism-related marker (CoxI) and a cellular stress-responsive marker (HSP70) were rapidly up-regulated upon acute warming treatments. In addition, our simulations of temperature oscillations mimicking natural daily rhythms did not result in significant changes in metabolic processes in St. 25 animals. As the ambient temperature increased by 7 °C, referred to as heatwave conditions, CoxI, HSP70, and antioxidant molecule (SOD) were stimulated, indicating the importance of cellular and metabolic adjustments. As with other aquatic species with high metabolic rates, squid larvae in the tropical/sub-tropical climate zone undergo adaptive metabolic shifts to maintain physiological functions and prevent excessive oxidative stress under environmental warming.

Keywords: Adaptive metabolic shift; Antioxidation; Climate change; Developmental stages; Environmental warming; Squid.