Thermal stress effects on energy resource allocation and oxygen consumption rate in the juvenile sea cucumber, Holothuria scabra (Jaeger, 1833)

Abstract

Water temperature is a key factor in aquaculture production of the commercially valuable sea cucumber Holothuria scabra. Knowledge is scarce about actual energetic costs that can be associated with internal acclimatization processes as a response to thermal extremes. In the present study changes in cellular energy allocation, oxygen consumption rate and energy related enzymes' activity (IDH and LDH) were measured in juvenile H. scabra, held at different temperatures: 21, 27 and 33°C. The results showed that the steady temperature change (1°C/day) to both temperature treatments, until reaching the testing temperatures (day 0), clearly affected cellular energy consumption and available energy reserves, measured in the respiratory tree and muscle tissue, respectively. However, 15 and 30days after acclimation, the initial differences in cellular energy allocation between treatments decreased. In contrast to the variations measured in cellular energy allocation, oxygen consumption was highest at 33°C and lowest at 21°C at all three measurement times. Moreover, a significant positive correlation between oxygen consumption rate and temperature was detected at day 15 and day 30. Likewise, a shift from anaerobic to aerobic energy metabolism, indicated by changes in LDH and IDH activities, was observed in the animals from the warm temperature treatment. Results imply that juvenile H. scabra were able to recover from initial disturbances in energy balance, caused by the incremental temperature change of ±6°C. Over the experimental period of 30days, elevated temperature did however, lead to a metabolic shift and more efficient energy turnover, indicated by changes in oxygen consumption rate, LDH and IDH. The synergy of cellular energy allocation and oxygen consumption proved to be a viable indicator to assess the capability of sea cucumbers like H. scabra to cope with extreme temperature conditions. Surprisingly, juvenile H. scabra were able to sustain their energy balance and oxygen consumption rate within the homeostatic range, even at 33°C. Thus, we assume that rearing temperatures of 33°C might be possible, which could improve aquaculture production of H. scabra. However, further research is required to understand the mechanisms and effects of acclimation under aquaculture conditions. Statement of relevanceThe sea cucumber H. scabra is considered a promising aquaculture candidate in the tropics. The commercial interest in H. scabra has led to a great number of attempts to culture this species e.g. in Madagascar, Tanzania, India and Indonesia, where the farming of this species also showed a great potential to increase the livelihood of the local community. Although, considerable research effort has been put into the advancement of the production cycle, fundamental knowledge, e.g. on physiological adjustments due to sub-optimal rearing conditions, remains scarce for H. scabra. Water temperature has been identified as crucial factor, determining production efficiency. In our manuscript we introduce an innovative approach, for the assessment of shifts in the energy budget as well as in metabolic pathways, to detect thermal stress in juvenile H. scabra. Our results show that the combined application of cellular energy allocation (CEA) and measurement of the oxygen consumption rate (OCR) as well as the activity of two metabolic key enzymes: iso-citrate dehydrogenase (IDH) and lactate dehydrogenase (LDH), is a strong analytical tool to evaluate whole animal homeostasis under thermal extremes. To our knowledge this is the first study in which the method of CEA was optimized for the application on isolated muscle and respiratory tree tissue of a sea cucumber, like H. scabra. Hence, our results provide original insights into the thermal acclimation physiology of H. scabra, which provides crucial knowledge for setting up optimal culture conditions for this highly valuable aquaculture candidate.Moreover, our results show that juvenile H. scabra were strongly affected by rapid temperature changes, exhibiting distinct differences in metabolic adjustments as response to short-term cold and warm acclimation, but were able to restore homeostatic conditions at constant cold and warm temperature extremes. Concerning aquaculture practices, these findings imply that CEA might be a good condition indicator to evaluate the overall metabolic status in sea cucumbers. Moreover, rapid temperature fluctuations seem to provoke much higher energetic costs in juvenile H. scabra than constant extreme temperature conditions, which is important to consider in daily management practices.The OCR revealed an enhanced metabolism at warmer temperature conditions, throughout the entire experimental period. Likewise, the warm exposed animals were shifting their energy turnover from a more anaerobic to a more aerobic state, indicated by changes in LDH and IDH activities, and showed increased foraging activity at all times. The combined outcome of CEA, OCR and activities of energy metabolism related enzymes indicates, that the increased metabolic activity in juvenile H. scabra, as response to warmer temperature, was well within the homeostatic range. Thus, contrary to our expectations, a rearing temperature of up to 33°C might presumably be favourable for the aquaculture of H. scabra.