Cite this paper:
LIU Chao, WU Fucun, QUE Huayong, ZHANG Guofan. Relationships of growth and mortality to enzymatic activity, and the relative mRNA expression of cultured scallops Patinopecten yessoensis in the Yellow Sea, China[J]. Journal of Oceanology and Limnology, 2019, 37(4): 1409-1422

Relationships of growth and mortality to enzymatic activity, and the relative mRNA expression of cultured scallops Patinopecten yessoensis in the Yellow Sea, China

LIU Chao1,2,3,4, WU Fucun1,3,4, QUE Huayong1,3,4, ZHANG Guofan1,3,4
1 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
4 National & Local Joint Engineering Laboratory of Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
Abstract:
The bottom aquaculture of yesso scallop (Patinopecten yessoensis) has developed rapidly in the north of Yellow Sea, China, but not without accompanying productivity problems. We, therefore, conducted field surveys to investigate factors related to growth and mortality rates of bottom-cultured scallops after release. Specifically, we focused on the effects of total antioxidant capacity (TAOC) and three key enzymes involved in antioxidant and metabolic function:glutamic pyruvic transaminase (GPT), lactic dehydrogenase (LDH), and superoxide dismutase (SOD). Across summer and winter, we also measured the relative mRNA expression of GPT and SOD to understand their seasonal variation in the scallops, along with how such variation correlated to growth and mortality. Results show that bottom cultured scallops experienced mass mortality during the first six months post-release. During winter (December), scallops grew more rapidly and suffered less mortality than in summer (August). The observed lower performance probably resulted from less advantageous environmental factors during the summer seasons, such as high temperature and low dissolved oxygen. These environmental stressors enhance protein consumption while decreasing energetic resources in scallops. Furthermore, scallops in summer exhibited high antioxidant levels that probably competed for energy with process integral to growth and survival. These negative factors combined to elevate mortality rates. In conclusion, we provided evidence suggesting correlations between metabolic/antioxidant activity and growth and mortality of bottom-cultured yesso scallops. These correlations implied us an accurate method to estimate the performance of bottom culture system. Suggestions about innovative aquaculture techniques were also discussed in the study. Our results might provide a possible guideline to the improvement of bottom culture techniques for this commercially valuable seafood species.
Key words:    yesso scallop (Patinopecten yessoensis)|bottom culture|growth and mortality rate|antioxidant and metabolic activity|relative mRNA expression   
Received: 2017-09-06   Revised: 2017-12-03
Tools
PDF (705 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LIU Chao
Articles by WU Fucun
Articles by QUE Huayong
Articles by ZHANG Guofan
References:
Abele D, Puntarulo S. 2004. Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 138(4):405-415.
Bedaiwy M A, Agarwal A, Said T M, Worley S, Thornton J, Falcone T. 2004. Differential growth of human embryos in vitro:role of total antioxidant capacity. Fertility and Sterility, 82(S2):S195-S196.
Bell J D, Leber K M, Blankenship H L, Loneragan N R, Masuda R. 2008. A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources. Reviews in Fisheries Science, 16(1-3):1-9.
Berthelin C, Kellner K, Mathieu M. 2000. Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West Coast of France). Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 125(3):359-369.
Brand A R. 2016. Scallop ecology:distributions and behaviour.Developments in Aquaculture and Fisheries Science, 40:469-533.
Brucet S, Boix D, Nathansen L W, Quintana X D, Jensen E, Balayla D, Meerhoff M, Jeppesen E. 2012. Effects of temperature, salinity and fish in structuring the macroinvertebrate community in shallow lakes:implications for effects of climate change. PLoS One, 7(2):e30877.
Burton R S, Feldman M W. 1983. Physiological effects of an allozyme polymorphism:Glutamate-pyruvate transaminase and response to hyperosmotic stress in the copepod Tigriopus californicus. Biochemical Genetics, 21(3-4):239-251.
Cabaud P G, Wróblewski F. 1958. Colorimetric measurement of lactic dehydrogenase activity of body fluids. American Journal of Clinical Pathology, 30(3):234-236.
Chen M Y, Yang H S, Delaporte M, Zhao S J. 2007. Immune condition of Chlamys farreri in response to acute temperature challenge. Aquaculture, 271(1-4):479-487.
Cheng P Z, Liu X, Zhang G F, He J G. 2007. Cloning and expression analysis of a HSP70 gene from Pacific abalone(Haliotis discus hannai). Fish & Shellfish Immunology, 22(1-2):77-87.
Choi Y K, Jo P G, Choi C Y. 2008. Cadmium affects the expression of heat shock protein 90 and metallothionein mRNA in the Pacific oyster, Crassostrea gigas.
Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 147(3):286-292.
Cliche G, Giguère M, Vigneau S. 1994. Dispersal and mortality of sea scallops, Placopecten magellanicus (Gmelin 1791), seeded on the sea bottom off Îles-de-la-Madeleine.Journal of Shellfish Research, 13(2):565-570.
Cotter E, Malham S K, O'Keeffe S, Lynch S A, Latchford J W, King J W, Beaumont A R, Culloty S C. 2010. Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea:the influence of growth, biochemistry and gametogenesis. Aquaculture, 303(1-4):8-21.
di Giulio R T, Washburn P C, Wenning R J, Winston G W, Jewell C S. 1989. Biochemical responses in aquatic animals:a review of determinants of oxidative stress.Environmental Toxicology and Chemistry, 8(12):1 103-1 123.
Dickie L M. 1958. Effects of high temperature on survival of the Giant Scallop. Journal of the Fisheries Research Board of Canada, 15(6):1 189-1 211.
Dyrynda E A, Pipe R K, Burt G R, Ratcliffe N A. 1998.Modulations in the immune defences of mussels (Mytilus edulis) from contaminated sites in the UK. Aquatic Toxicology, 42(3):169-185.
Grefsrud E S, Strand Ø, Haugum G A. 2003. Handling time and predation behaviour by the crab, Cancer pagurus, preying on cultured scallop, Pecten maximus. Aquaculture Research, 34(13):1 191-1 200.
Grieshaber M, Gäde G. 1977. Energy supply and the formation of octopine in the adductor muscle of the scallop, Pecten jacobaeus (Lamarck). Comparative Biochemistry and Physiology Part B:Comparative Biochemistry, 58(3):249-252.
Grizzle R E, Lutz R A. 1989. A statistical model relating horizontal seston fluxes and bottom sediment characteristics to growth of Mercenaria mercenaria.Marine Biology, 102(1):95-105.
Guerra C, Zenteno-Savín T, Maeda-Martínez A N, Philipp E E R, Abele D. 2012. Changes in oxidative stress parameters in relation to age, growth and reproduction in the shortlived catarina scallop Argopecten ventricosus reared in its natural environment. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 162(4):421-430.
Guo X M, Ford S E, Zhang F S. 1999. Molluscan aquaculture in China. Journal of Shellfish Research, 18(1):19-31.
Hao Z L, Liu J Z, Tang X J, Zhan Y Y, Tian Y, Ding J, Yang L M, Chang Y Q. 2015. A comparative study of survival, metabolism, immune indi-cators and HSP70 expression in three kinds of shell colors Japanese scallop Mizuhopecten yessoensis under high tem-perature stress.Marine Sciences, 39(11):108-115. (in Chinese with English abstract)
Hatcher B G, Scheibling R E, Barbeau M A, Hennigar A W, Taylor L H, Windust A J. 1996. Dispersion and mortality of a population of sea scallop (Placopecten magellanicus)seeded in a tidal channel. Canadian Journal of Fisheries and Aquatic Sciences, 53(1):38-54.
Hermes-Lima M, Storey J M, Storey K B. 1998. Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 120(3):437-448.
Hilton J W, Cho C Y, Brown R G, Slinger S J. 1979. The synthesis, half-life and distribution of ascorbic acid in rainbow trout. Comparative Biochemistry and Physiology Part A:Physiology, 63(3):447-453.
Houle-Leroy P, Garland Jr T, Swallow J G, Guderley H. 2000.Effects of voluntary activity and genetic selection on muscle metabolic capacities in house mice Mus domesticus. Journal of Applied Physiology, 89(4):1 608-1 616.
Hsieh K M, Suntzeff V, Cowdry E V. 1955. Serum lactic dehydrogenase activity as indication of neoplastic growth and regression. Experimental Biology and Medicine, 89(4):627-629.
Jaenisch R, Bird A. 2003. Epigenetic regulation of gene expression:how the genome integrates intrinsic and environmental signals. Nature Genetics, 33(3S):245-254.
Ji L Q, Sun G X, Li J, Wang Y, Du Y S, Li X, Liu Y. 2017.Effect of dietary β-glucan on growth, survival and regulation of immune processes in rainbow trout(Oncorhynchus mykiss) infected by Aeromonas salmonicida. Fish & Shellfish Immunology, 64:56-67.
Jo P G, Choi Y K, Choi C Y. 2008. Cloning and mRNA expression of antioxidant enzymes in the Pacific oyster, Crassostrea gigas in response to cadmium exposure.Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 147(4):460-469.
Kader M A, Koshio S, Ishikawa M, Yokoyama S, Bulbul M, Honda Y, Mamauag R E, Laining A. 2011. Growth, nutrient utilization, oxidative condition, and element composition of juvenile red sea bream Pagrus major fed with fermented soybean meal and scallop by-product blend as fishmeal replacement. Fisheries Science, 77(1):119-128.
Konstantinov A S, Pushkar V Y, Aver Yanova O V. 2003.Effects of fluctuations of abiotic factors on the metabolism of some hydrobionts. Biology Bulletin of the Russian Academy of Sciences, 30(6):610-616.
Labreuche Y, Lambert C, Soudant P, Boulo V, Huvet A, Nicolas J L. 2006. Cellular and molecular hemocyte responses of the Pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Microbes and Infection, 8(12-13):2 715-2 724.
Laing I. 2007. Scallop farming-2nd edition by David Hardy.Aquaculture Research, 38(6):668-669.
Lauzon-Guay J S, Dionne M, Barbeau M A, Hamilton D J. 2005. Effects of seed size and density on growth, tissueto-shell ratio and survival of cultivated mussels (Mytilus edulis) in Prince Edward Island, Canada. Aquaculture, 250(3-4):652-665.
Leach G J, Taylor M H. 1982. The effects of cortisol treatment on carbohydrate and protein metabolism in fundulus heteroclitus. General and Comparative Endocrinology, 48(1):76-83.
Lenihan H S. 1999. Physical-biological coupling on oyster reefs:how habitat structure influences individual performance. Ecological Monographs, 69(3):251-275.
Li Q, Zhao X L, Kong L F, Yu H. 2013. Transcriptomic response to stress in marine bivalves. ISJ-Invertebrate Survival Journal, 10(1):84-93.
Li W J, Xue Z F. 2005. Healthy sustainable proliferation & cultivation of scallop Patinopecten yessoensis. Fisheries Science, 24(9):49-51. (in Chinese with English abstract)
Lin C, Ning X, Su J, Lin Y, Xu B. 2005. Environmental changes and the responses of the ecosystems of the Yellow Sea during 1976-2000. Journal of Marine Systems, 55(3-4):223-234.
Liu J, Pan L Q, Zhang L, Miao J J, Wang J. 2009. Immune responses, ROS generation and the haemocyte damage of scallop Chlamys farreri exposed to Aroclor 1254. Fish & Shellfish Immunology, 26(3):422-428.
Liu Q, Basu N, Goetz G, Jiang N, Hutz R J, Tonellato P J, Carvan Ⅲ M J. 2013a. Differential gene expression associated with dietary methylmercury (MeHg) exposure in rainbow trout (Oncorhynchus mykiss) and zebrafish(Danio rerio). Ecotoxicology, 22(4):740-751.
Liu R, Qiu L M, Yu Z A, Zi J, Yue F, Wang L L, Zhang H, Teng W M, Liu X F, Song L S. 2013b. Identification and characterisation of pathogenic Vibrio splendidus from Yesso scallop (Patinopecten yessoensis) cultured in a low temperature environment. Journal of Invertebrate Pathology, 114(2):144-150.
Livingstone D R, de Zwaan A, Leopold M, Marteijn E. 1983.Studies on the phylogenetic distribution of pyruvate oxidoreductases. Biochemical Systematics and Ecology, 11(4):415-425.
Livingstone D R, de Zwaan A, Thompson R J. 1981. Aerobic metabolism, octopine production and phosphoarginine as sources of energy in the phasic and catch adductor muscles of the giant scallop placopecten magellanicus during swimming and the subsequent recovery period.Comparative Biochemistry and Physiology Part B:Comparative Biochemistry, 70(1):35-44.
Long S M, Ryder K J, Holdway D A. 2003. The use of respiratory enzymes as biomarkers of petroleum hydrocarbon exposure in Mytilus edulis planulatus.Ecotoxicology and Environmental Safety, 55(3):261-270.
Lu X, Wang C, Liu B Z. 2015. The role of Cu/Zn-SOD and Mn-SOD in the immune response to oxidative stress and pathogen challenge in the clam Meretrix meretrix. Fish & Shellfish Immunology, 42(1):58-65.
Lu Y T, Blake N J. 1997. The culture of the southern bay scallop in Tampa Bay, an urban Florida estuary.Aquaculture International, 5(5):439-450.
Malham S K, Cotter E, O'Keeffe S, Lynch S, CUlloty S C, King J W, Latchford J W, Beaumont A R. 2009. Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea:the influence of temperature and nutrients on health and survival. Aquaculture, 287(1-2):128-138.
Matoo O B, Ivanina A V, Ullstad C, Beniash E, Sokolova I M. 2013. Interactive effects of elevated temperature and CO2 levels on metabolism and oxidative stress in two common marine bivalves (Crassostrea virginica and Mercenaria mercenaria). Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 164(4):545-553.
McMahon T E, Matter W J. 2006. Linking habitat selection, emigration and population dynamics of freshwater fishes:a synthesis of ideas and approaches. Ecology of Freshwater Fish, 15(2):200-210.
Meng Q L, Bao Z M, Wang Z P, Wang S, Hu J J, Hu X L, Huang X T. 2012. Growth and reproductive performance of triploid yesso scallops (Patinopecten yessoensis)induced by hypotonic shock. Journal of Shellfish Research, 31(4):1 113-1 123.
Minchin D. 1992. Biological observations on young scallops, Pecten maximus. Journal of the Marine Biological Association of the United Kingdom, 72(4):807-819.
Minchin D. 2002. The potential for ranching the scallop, Pecten maximus-past, present, and future:problems and opportunities.-Proceedings of ICES Marine Science Symposia 215:416-423
Morel G M, Bossy S F. 2001. A seeding experiment of juvenile great scallops (Pecten maximus (L.)) off the Island of Jersey. Aquaculture International, 9(5):367-377.
Nordberg J, Arnér E S J. 2001. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system.Free Radical Biology and Medicine, 31(11):1 287-1 312.
Park Y J. 1998. Biological Studies on Aquaculture of the Scallop, Patinopecten Yessoensis (Jay). Cheju National University, Korea.
Patrick S, Faury N, Goulletquer P. 2006. Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of pacific oyster Crassostrea gigas(Thunberg) in Marennes-Oléron bay (France).Aquaculture, 252(2-4):328-338.
Pohle D G, Bricelj V M, García-Esquivel Z. 1991. The eelgrass canopy an above-bottom refuge from benthic predators for juvenile bay scallops Argopecten irradians. Marine Ecology Progress Series, 74:47-59.
Pörtner H O. 2002. Climate variations and the physiological basis of temperature dependent biogeography:systemic to molecular hierarchy of thermal tolerance in animals.Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 132(4):739-761.
Reitman S, Frankel S. 1957. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. American Journal of Clinical Pathology, 28(1):56-63.
Richardson C A. 1992. Scallops:biology, ecology and aquaculture:edited by S.E. Shumway; Elsevier; 1991; 116 pp.; NLG 300.00; ISBN 0-444-88954-X. Journal of Experimental Marine Biology and Ecology, 164(2):280-281.
Rong Y F, Wu W C, Ni X L, Kuang T T, Jin D Y, Wang D S, Lou W H. 2013. Lactate dehydrogenase A is overexpressed in pancreatic cancer and promotes the growth of pancreatic cancer cells. Tumor Biology, 34(3):1 523-1 530.
Sakamoto S, Yone Y. 1978. Effect of starvation on hematological characteristics, and the contents of chemical components and activities of enzymes in blood serum of red sea bream.Journal of the Faculty of Agriculture, Kyushu University, 23(1-2):63-69.
Shao B, Zhu L S, Dong M, Wang J, Wang J H, Xie H, Zhang Q M, Du Z K, Zhu S Y. 2012. DNA damage and oxidative stress induced by endosulfan exposure in zebrafish (Danio rerio). Ecotoxicology, 21(5):1 533-1 540.
Smith I, Fonseca M S, Rivera J A, Rittmaster K A. 1988.Habitat value of natural versus recently transplanted eelgrass, Zostera marina, for the bay scallop, Argopecten irradians. Fishery Bulletin, 87:189-196.
Soletchnik P, Lambert C, Costil K. 2005. Summer mortality of crassostrea gigas (Thunberg) in relation to environmental rearing conditions. Journal of Shellfish Research, 24(1):197-208.
Soletchnik P, Le Moine O, Faury N, Razet D, Geairon P, Goulletquer P. 1999. Summer mortality of the oyster in the Bay Marennes-Oléron:spatial variability of environment and biology using a geographical information system (GIS). Aquatic Living Resources, 12(2):131-143.
Soletchnik P, Ropert M, Mazurié J, Gildas Fleury P, Le Coz F. 2007. Relationships between oyster mortality patterns and environmental data from monitoring databases along the coasts of France. Aquaculture, 271(1-4):384-400.
Strahl J, Dringen R, Schmidt M M, Hardenberg S, Abele D. 2011. Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 158(4):513-519.
Sultana M S, Koshio S, Ishikawa M, Yokoyama S, Ikemura T. 2015. Effects on dietary supplement of Shochu Distillery By-Product (SDBP) on the growth of red sea bream.Aquaculture Science, 61(1):47-54.
Wang J, Green P S, Simpkins J W. 2001. Estradiol protects against ATP depletion, mitochondrial membrane potential decline and the generation of reactive oxygen species induced by 3-nitroproprionic acid in SK-N-SH human neuroblastoma cells. Journal of Neurochemistry, 77(3):804-811.
Wang X Q, Wang L L, Yao C, Qiu L M, Zhang H, Zhi Z, Song L S. 2012. Alternation of immune parameters and cellular energy allocation of Chlamys farreri under ammonia-N exposure and Vibrio anguillarum challenge. Fish & Shellfish Immunology, 32(5):741-749.
Wenming R J, di Giulio R T. 1988. Microsomal enzyme activities, superoxide production, and antioxidant defenses in ribbed mussels (Geukensia demissa) and wedge clams (Rangia cuneata). Comparative Biochemistry and Physiology Part C:Comparative Pharmacology, 90(1):21-28.
Wong M C, Barbeau M A, Hennigar A W, Robinson S M. 2005. Protective refuges for seeded juvenile scallops(Placopecten magellanicus) from sea star (Asterias spp.)and crab (Cancer irroratus and Carcinus maenas)predation. Canadian Journal of Fisheries and Aquatic Sciences, 62(8):1 766-1 781.
Wong M C, Barbeau M A. 2003. Effects of substrate on interactions between juvenile sea scallops (Placopecten magellanicus Gmelin) and predatory sea stars (Asterias vulgaris Verrill) and rock crabs (Cancer irroratus Say).Journal of Experimental Marine Biology and Ecology, 287(2):155-178.
Xiao J, Ford S E, Yang H S, Zhang G F, Zhang F S, Guo X M. 2005. Studies on mass summer mortality of cultured Zhikong scallops (Chlamys farreri Jones et Preston) in China. Aquaculture, 250(3-4):602-615.
Xiu M, Pan L Q, Jin Q. 2016. Toxic effects upon exposure to polycyclic aromatic hydrocarbon (chrysene) in scallop Chlamys farreri during the reproduction period.Environmental Toxicology and Pharmacology, 44:75-83.
Yin H C, Huang J, Yang D H, Zhao H Y, Jia F, Zhang Y. 2015.Effects of yeast nucleotide on growth performance, serum immune index and muscle composition of Ancherythroculter nigrocauda Yih & Wu. Iranian Journal of fisheries Sciences, 14(3):646-659.
Yu Z H, Yang H S, Liu B Z, Xing K, Zhang L B, Xu Q. 2010.Survival, growth and immune activity of scallop Chlamys farreri cultured at different depths in Haizhou Bay(Yellow Sea, China) during hot season. Chinese Journal of Oceanology and Limnology, 28(3):498-507.
Yuan L X, Li M, Meng F X, Gong Y F, Qian Y X, Shi G, Wang R X. 2017. Growth, blood health, antioxidant status, immune response and resistance to Aeromonas hydrophila of juvenile yellow catfish exposed to di-2-ethylhexyl phthalate (DEHP). Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 202:79-84.
Zang Y Q, Tian X L, Dong S L, Dong Y W. 2012. Growth, metabolism and immune responses to evisceration and the regeneration of viscera in sea cucumber, Apostichopus japonicus. Aquaculture, 358-359:50-60.
Zhen H, Wen M, Yang Y, Can Z, Hui G, Li X, Liu D L. 2014.Toxic effects of HgCl2 on activities of SOD, AchE and relative expression of SOD, AChE, CYP1A1 of zebrafish.Ecotoxicology, 23(10):1 842-1 845.
Copyright © Haiyang Xuebao