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Effects of Rearing Temperature on Growth, Metabolism and Thermal Aquaculture Research, 2013, 44, 1550–1559 doi:10.1111/j.1365-2109.2012.03162.x Effects of rearing temperature on growth, metabolism and thermal tolerance of juvenile sea cucumber, Apostichopus japonicus Selenka: critical thermal maximum (CTmax) and hsps gene expression Qing-Lin Wang1, Yun-Wei Dong2, Chuan-Xin Qin3, Shan-Shan Yu1, Shuang-Lin Dong1 & Fang Wang1 1The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao, China 2State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, China 3South China Sea Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China Correspondence: Y-W Dong, State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen 361005, China. E-mail: [email protected] Abstract Introduction Effects of different rearing temperatures (16, 21 and Sea cucumber Apostichopus japonicus (Selenka) is 26°C) on growth, metabolic performance and ther- distributed along the Asian coast from 35°Ntoat mal tolerance of juvenile sea cucumber Apostichopus least 44°N including Russia, China, Japan and japonicus (initial body weight 7.72 ± 0.96 g, mean Korea (Sloan 1984; Liao 1997). Due to demand ±SD) were investigated in this study. During the 40- and high price, it has been exploited as an impor- day experiment, growth, metabolic performance, tant fishery resource for a long time. With the food intake and energy budget at different reared rapid increase in demand of beche-de-mer and sig- temperatures were determined. Sea cucumbers rear- nificantly declining wild caught stocks form overf- ing at 16°C obtained better growth (final body ishing, aquaculture of sea cucumber has become weight 11.96 ± 0.35 g) than those reared at 21 more economically viable. (10.33 ± 0.41 g) and 26°C (8.31 ± 0.19 g) Water temperature plays an important role in (P < 0.05), and more energy was allocated for growth and physiological performance of the sea growth at 16°C (162.73 ±11.85 J gÀ1 dÀ1) than cucumber (Li, Yang, Zhang, Zhou & Zhang 2002; those at 21(79.61 ± 6.76 J gÀ1 dÀ1) and 26°C Dong & Dong 2006; Dong, Dong, Tian, Wang & (27.07 ± 4.30 J gÀ1 dÀ1)(P < 0.05). Critical ther- Zhang 2006), and the low thermotolerance of A. mal maxima (CTmax) values of juvenile sea cucum- japonicus limits the national wide aquaculture bers reared at 16, 21 and 26°C were 33.1, 34.1 (Wang, Dong, Dong & Wang 2011). According to and 36.6°C, respectively, and the upregulation of our record, the water temperature in the field hsps in sea cucumbers reared at 26°C was higher aquaculture pond was À0.4 to 31.8°C in Jiaonan, than those acclimated at lower temperatures (16 Qingdao (35°53′N, 120°00′E), and frequently and 21°C), indicating that temperature acclimation exceeded 30°C in summer (from June to Septem- could change the thermal tolerance of the sea ber) (Dong Y. W. & Meng X. L, unpublished data). cucumber, and CTmax and hsps were sensitive indi- An, Dong and Dong (2007) found that the assimi- cators of the sea cucumber’s thermal tolerance. lation efficiency of sea cucumber decreased with temperature increasing, and adult A. japonicus Keywords: rearing temperature, sea cucumber, becomes inactive when water temperature exceeds growth, metabolic performance, thermal toler- 18°C and will aestivate at water temperatures ance, critical thermal maxima about 20–24.5°C (Liu, Li, Song, Sun, Zhang and Gu 1550 © 2012 John Wiley & Sons Ltd Aquaculture Research, 2013, 44, 1550–1559 Effects of rearing temperature on sea cucumber Q -L Wang et al. 1996; Yang, Zhou, Zhang, Yuan, Li, Liu & Zhang Materials and methods 2006). Aestivation can last for 4 months in some regions in China (Liu et al. 1996). Therefore, it is Collection and acclimation of animals essential to study the thermal limits of this species. Previous studies used upper or lower incipient Six-month old sea cucumbers were collected at lethal temperature (ILT) as an index reflecting 12°C in April from Jimo Aquatic Seeding Breeding thermal tolerance of sea cucumber (Meng, Ji, Farm, Qingdao, China. In the laboratory, water Dong, Wang & Dong 2009; Dong, Ji, Meng, Dong temperature was gradually increased to 16°C and & Sun 2010). The measurement of ILT involves maintained at 16°C for 2 weeks, before placing the abrupt transfer of samples to baths maintained animals in acclimatization conditions. at a sequence of constant, lethally high tempera- tures. However, critical thermal maxima (CTmax) Experimental protocol refers to the thermal point at which the locomo- tory activity of an animal becomes disorganized To acclimatize the experimental animals, water and the animal loses its ability to escape from con- temperature gradually increased at a rate of ditions which will promptly lead to its death when 1°CdÀ1 heated by 300 W electric heaters until heated from a previous acclimation temperature at the designated temperature, and kept at the desig- a constant rate just fast enough to allow deep nated temperature for 1 week. After acclimatiza- body temperatures to follow environmental tem- tion, the sea cucumbers were starved for 48 h and peratures without a significant time lag (Cox weighed by a balance of 0.001 g sensitivity. Forty- 1974; Becker & Genoway 1979). In the method of five sea cucumbers (wet weight of 7.72 ± 0.96 g) CTmax, samples are placed in an environment of were randomly selected and allocated into nine steadily increasing temperature. The ILT method glass aquarium (450 9 250 9 350 mm, about measures only mortification and, regrettably per- 40 L water). This allowed three treatments to be haps, the trauma of handling and transfer. How- tested in triplicates with five animals in each ever, the CTmax measures mortification and aquarium. The three treatments were setup at partial acclimation (Kilgour & McCauley 1986). three temperatures: 16, 21 and 26°C. The experi- To evaluate the capability of A. japonicus facing an ment lasted for 40 days. increasing thermal stress, therefore CTmax value was used in this study. Rearing conditions Thermal history can affect the upper thermal limit of aquatic animals, such as sea cucumber (Meng During acclimatization and throughout the experi- et al. 2009), fish (Das, Pala, Chakrabortyb, Manu- ment, sea cucumbers were fed to excess with a sha, Sahua & Mukherjeea 2004) and shrimp (Sel- laboratory-made formulated diet (9.94 ± 0.17% vakumar & Geraldine 2005). Acting as molecular moisture, 18.58 ± 0.23% crude protein, 2.67 ± chaperones, heat shock proteins (hsps) are extremely 0.06% fat, 42.66 ± 0.54% ash and 8.16 ± 0.00 sensitive to temperature (Frydman & Ho¨held 1997; kJ gÀ1 energy), containing powders of Sargassum Morimoto 1998; Feder & Hofmann 1999; Picard spp., fish meal, sea mud, wheat, vitamin and 2002), and are closely related to organisms’ thermal mineral premixes. Seawater was filtered using a history (Tomanek & Somero 1999; Hochachka & So- sand filter and the salinity was 30–32 psu. One- mero 2002). The responses of hsp70 in the sea half or two-thirds of the rearing water was cucumber to acute thermal and osmotic stress have exchanged by fresh equi-temperature seawater been determined (Dong, Dong & Ji 2007, 2008; daily. Aeration was provided continuously, and Dong & Dong 2008; Dong, Dong & Meng 2008; Ji, the photoperiod was 12:12 h light:dark. Seawater Dong & Dong 2008). However, the responses of pH was about 7.8–8.2 and the concentration of hsp70 and hsp90 of A. japonicus to a long-term ammonia was less than 0.24 mg LÀ1. Water tem- chronic thermal stress have not been assessed. perature, salinity, pH and ammonia concentration In this study, we want to test the hypothesis were determined with mercury thermometer that thermal history can change the thermal limits (accuracy ±0.2°C), salinity refractometer (AIAGO, of the sea cucumber A. japonicus, and the modifica- Kyoto, Japan), pH metre (PH3150i; WTW, tions of thermal tolerance are closely relate to the Munich, Germany) and hypobromite oxidation changes in expression of hsps. methods (Wu 2007) respectively. © 2012 John Wiley & Sons Ltd, Aquaculture Research, 44, 1550–1559 1551 Effects of rearing temperature on sea cucumber Q -L Wang et al. Aquaculture Research, 2013, 44, 1550–1559 8.23 ± 0.87 g were measured every 8 days. Prior Sample collection and data calculation to the test of oxygen consumption, sea cucumbers Five sea cucumbers were simultaneously sampled were starved for 24 h to reduce associated meta- from the acclimatized animals to determine the ini- bolic responses. The tested animal was put into a tial body composition. During the experiment, sea 330 mL conical flask with a rubber plug individu- cucumbers were fed once a day at about ally, which was immersed into a water bath (Shuniu, 17:00 hour, faeces and uneaten feed were col- Chengdu, China) for temperature control. There lected by syphon 23–24 h later and then dried at were three replicates and two blank controls to 65°C to constant weight. The sea cucumbers were correct for the respiration of bacteria in the water. weighed every 20 days and the daily food supply Oxygen content of water samples was determined was precisely weighed and recorded. At the end of using the dissolved oxygen analyser (YSI 5000; experiment, the sea cucumbers were starved for YSI, Yellow Springs, OH, USA), and the OCR of 48 h, weighed and then dried at 65°C until con- the sea cucumber was calculated from the follow- stant weight achieved. ing equation: The energy content of the diets, faeces and ani- À1 À1 mal samples were measured by a calorimeter OCRðlgO2h g Þ¼ðDtVt À D0V0Þ=WT (PARR Instrument Company, Moline, IL, USA).
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