Cite this paper:
LI Qiao, ZHANG Fang, WANG Minxiao, LI Mengna, SUN Song. Effects of hypoxia on survival, behavior, and metabolism of Zhikong scallop Chlamys farreri Jones et Preston 1904[J]. Journal of Oceanology and Limnology, 2020, 38(2): 351-363

Effects of hypoxia on survival, behavior, and metabolism of Zhikong scallop Chlamys farreri Jones et Preston 1904

LI Qiao1,2, ZHANG Fang1, WANG Minxiao1, LI Mengna1,2, SUN Song1
1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China
Abstract:
Hypoxia, a frequent occurring threat in coastal regions, often results in mass mortalities of marine organisms and brings a serious ecological problem. The commercially important Zhikong scallop Chlamys farreri is being under such a threat as the risks of eutrophication and hypoxia have risen in their culture areas. However, little information has been known concerning their tolerance to hypoxia and their strategy for survival. In the present study, a 20-day experiment was conducted to determine the effects of hypoxia on the survival, behavior, and metabolism of Zhikong scallop. With the LC50 for dissolved oxygen (DO) being estimated as 1.8 mg/L, the survival of Zhikong scallop can be greatly challenged even under the moderate hypoxic condition of around 2.0 mg/L DO. The survival rate ranged from 69% to 59% when DO dropped from 3.0 to 2.0 mg/L, and it was further reduced to 47% at 1.5 mg/L DO. In hypoxic conditions, the scallops became significantly active, which may be explained as escape attempts to avoid hypoxic water. To save energy, Zhikong scallop would depress their respiration. However, when DO dropped from 3.0 to 2.0 mg/L, the oxygen consumption rate hardly changed. The upregulation of lactate dehydrogenase activity and the unrepressed phosphofructokinase activity, which often result in the unbalanced cellular homeostasis and energy budget, may account for the observed increase in the mortality rate of Zhikong scallops. In general, Zhikong scallop is sensitive to hypoxia events, though possible escape attempts, depressed respiration, and oxaloacetate-pathway may increase their survival chance.
Key words:    hypoxia|Zhikong scallop|survival|behavior|metabolism   
Received: 2019-03-19   Revised: 2019-05-12
Tools
PDF (1254 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by LI Qiao
Articles by ZHANG Fang
Articles by WANG Minxiao
Articles by LI Mengna
Articles by SUN Song
References:
Aguirre-Velarde A, Jean F, Thouzeau G, Flye-Sainte-Marie J. 2018. Feeding behaviour and growth of the Peruvian scallop (Argopecten purpuratus) under daily cyclic hypoxia conditions. J. Sea Res., 131:85-94.
Artigaud S, Lacroix C, Pichereau V, Flye-Sainte-Marie J. 2014. Respiratory response to combined heat and hypoxia in the marine bivalves Pecten maximus and Mytilus spp.Comp. Biochem. Physiol. Part A:Mol. Integr. Physiol., 175:135-140.
Brand A R, Roberts D. 1973. The cardiac responses of the scallop Pecten maximus (L.) to respiratory stress. J. Exp.Mar. Biol. Ecol., 13(1):29-43.
Breitburg D, Levin L A, Oschlies A, Grégoire M, Chavez F P, Conley D J, Garçon V, Gilbert D, Gutiérrez D, Isensee K, Jacinto G S, Limburg K E, Montes I, Naqvi S W A, Pitcher G C, Rabalais N N, Roman M R, Rose K. A, Seibel B A, Telszewski M, Yasuhara M, Zhang J. 2018. Declining oxygen in the global ocean and coastal waters. Science, 359(6371):eaam7240.
Chen J H, Mai K S, Ma H M, Wang X J, Deng D, Liu X W, Xu W, Liufu Z G, Zhang W B, Tan B P, Ai Q H. 2007a. Effects of dissolved oxygen on survival and immune responses of scallop (Chlamys farreri Jones et Preston). Fish Shellfish Immunol., 22(3):272-281.
Chen M Y, Yang H S, Delaporte M, Zhao S J, Xing K. 2007c.Immune responses of the scallop Chlamys farreri after air exposure to different temperatures. J. Exp. Mar. Biol.Ecol., 345(1):52-60.
Chen M Y, Yang H S, Delaporte M, Zhao S J. 2007b.Immune condition of Chlamys farreri in response to acute temperature challenge. Aquaculture, 271(1-4):479-487.
Diaz R J, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science, 321(5891):926-929.
Domenici P, Lefrançois C, Shingles A. 2007. Hypoxia and the antipredator behaviours of fishes. Philos. Trans. Roy. Soc.B:Biol. Sci., 362(1487):2 105-2 121.
Finney D. 2009. Probit Analysis. Cambridge University Press, Cambridge, UK. 272p.
Foss A, Evensen T H, Øiestad V. 2002. Effects of hypoxia and hyperoxia on growth and food conversion efficiency in the spotted wolffish Anarhichas minor (Olafsen).Aquacult. Res., 33(6):437-444.
Gao J G, Gao X J, Hao Y H. 2002. Inhabition of albendazole and oxfendazole on the activity of fumaric reductase in Cysticercus cellulosae. Heilongjiang J. Anim. Sci. Vet.Med., (8):8-9. (in Chinese with English abstract)
Gobler C J, Baumann H. 2016. Hypoxia and acidification in ocean ecosystems:coupled dynamics and effects on marine life. Biol. Lett., 12(5):20150976.
Grieshaber M K, Hardewig I, Kreutzer U, Pörtner H O. 1993.Physiological and metabolic responses to hypoxia in invertebrates. In:Reviews of Physiology, Biochemistry and Pharmacology. Springer, Berlin, Heidelberg. p.43-147.
Guo X M, Luo Y S. 2006. Scallop culture in China. Dev.Aquacult. Fish. Sci., 35:1 143-1 161.
Hagerman L, Uglow R F. 1985. Effects of hypoxia on the respiratory and circulatory regulation of Nephrops norvegicus. Mar. Biol. 87(3):273-278.
Howarth R, Chan F, Conley D J, Garnier J, Doney S C, Marino R, Billen G. 2011. Coupled biogeochemical cycles:eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front. Ecol. Environ., 9(1):18-26.
Hughes G M, Sunders R L. 1970. Responses of the respiratory pumps to hypoxia in the rainbow trout (Salmo gairdneri).J. Exp. Biol., 53(3):529-545.
Ivanina A V, Nesmelova I, Leamy L, Sokolov E P, Sokolova I M. 2016. Intermittent hypoxia leads to functional reorganization of mitochondria and affects cellular bioenergetics in marine molluscs. J. Exp. Biol., 219(11):1 659-1 674.
Joyce W, Ozolina K, Mauduit F, Ollivier H, Claireaux G, Shiels H A. 2016. Individual variation in whole-animal hypoxia tolerance is associated with cardiac hypoxia tolerance in a marine teleost. Biol Lett., 12(1):20150708.
Kong H, Jiang X Y, Clements J C, Wang T, Huang X Z, Shang Y Y, Chen J F, Hu M H, Wang Y J. 2019. Transgenerational effects of short-term exposure to acidification and hypoxia on early developmental traits of the mussel Mytilus edulis.Mar. Environ. Res., 145:73-80.
Larade K, Storey K B. 2002. A profile of the metabolic responses to anoxia in marine. Cell Mol. Response Stress, 3:27-46.
Laudien J, Schiedek D, Brey T, Pörtner H O, Arntz W E. 2002. Survivorship of juvenile surf clams Donax serra (Bivalvia, Donacidae) exposed to severe hypoxia and hydrogen sulphide. J. Exp. Mar. Biol. Ecol., 271(1):9-23.
Leverone J R. 1995. Diurnal dissolved oxygen in two Tampa Bay seagrass meadows:ramifications for the survival of adult bay scallops (Argopectin irradians concentricus).Fla. Sci., 58:141-152.
Livingstone D R, Stickle W B, Kapper M A, Wang S, Zurburg W. 1990. Further studies on the phylogenetic distribution of pyruvate oxidoreductase activities. Comp. Biochem.Physiol. Part B:Comp. Biochem., 97(4):661-666.
Lombardi S A, Harlan N P, Paynter K T. 2013. Survival, acid-base balance, and gaping responses of the Asian oyster Crassostrea ariakensis and the eastern oyster Crassostrea virginica during clamped emersion and hypoxic immersion. J. Shellfish Res. 32(2):409-416.
Long W C, Brylawski B J, Seitz R D. 2008. Behavioral effects of low dissolved oxygen on the bivalve Macoma balthica.J. Exp. Mar. Biol. Ecol., 359(1):34-39.
McGladdery S E, Bower S M, Getchell R G. 2006. Diseases and parasites of scallops. Dev. Aquacult. Fish. Sci. 35:595-650.
Ripley J L, Foran C M. 2007. Influence of estuarine hypoxia on feeding and sound production by two sympatric pipefish species (Syngnathidae). Mar. Environ. Res., 63(4):350-367.
Seibel B A. 2011. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J. Exp.Biol., 214(2):326-336.
Smolinski M B. 2016. Regulation of Pyruvate Kinase in Hypometabolic States. Carleton University, Ottawa, Ontario, Canada.
Sui Y M, Kong H, Shang Y Y, Huang X Z, Wu F L, Hu M H, Lin D H, Lu W Q, Wang Y J. 2016. Effects of short-term hypoxia and seawater acidification on hemocyte responses of the mussel Mytilus coruscus. Mar. Pollut. Bull., 108(1-2):46-52.
Tang B J, Liu B Z, Wang X M, Yue X, Xiang J H. 2010.Physiological and immune responses of zhikong scallop Chlamys farreri to the acute viral necrobiotic virus infection. Fish Shellfish Immunol., 29(1):42-48.
Vaquer-Sunyer R, Duarte C M. 2008. Thresholds of hypoxia for marine biodiversity. Proc. Natl. Acad. Sci. USA, 105(40):15 452-15 457.
Wang M Q, Wang B J, Jiang K Y, Liu M, Shi X M, Wang L. 2018. A mitochondrial manganese superoxide dismutase involved in innate immunity is essential for the survival of Chlamys farreri. Fish Shellfish Immunol., 72:282-290.
Wang Y J, Hu M H, Cheung S G, Shin P K S, Lu W Q, Li J L. 2013. Antipredatory responses of Perna viridis (Linnaeus, 1758) under acute hypoxia and low salinity. J. Molluscan Stud., 79(1):42-50.
Wang Y J, Hu M H, Wong W H, Cheung S G, Shin P K S. 2011.Combined effects of dissolved oxygen and salinity on growth and body composition of juvenile green-lipped mussel Perna viridis. J. Shellfish Res., 30(3):851-857.
Wu R S S, Lam P K S, Wan K L. 2002. Tolerance to, and avoidance of, hypoxia by the penaeid shrimp (Metapenaeus ensis). Environ. Pollut., 118(3):351-355.
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.
Yan T, Zhou M J, Fu M, Wang Y F, Yu R C, Li J. 2001.Inhibition of egg hatching success and larvae survival of the scallop, Chlamys farreri, associated with exposure to cells and cell fragments of the dinoflagellate Alexandrium tamarense. Toxicon, 39(8):1 239-1 244.
Yang H S, Wang J, Zhou Y, Wang P, He Y C, Zhang F S. 2001.Impact of starvation on survival, meat condition and metabolism of Chlamys farreri. Chin. J. Oceanol. Limnol., 19(1):51-56.
Yang S, Yang Q, Song X L, Liu S, Qu K M, Sun Y. 2018. A novel approach to evaluate potential risk of organic enrichment in marine aquaculture farms:a case study in Sanggou Bay. Environ. Sci. Pollut. Res., 25(17):16 842-16 851.
Zhang F S, Yang H S. 1999. Analysis of the causes of mass mortality of farming Chlamys farreri in summer in coastal areas of Shandong, China. Mar. Sci., (1):44-47. (in Chinese with English abstract)
Zhang Y, Wu H F, Wei L, Xie Z P, Guan B. 2017. Effects of hypoxia in the gills of the Manila clam Ruditapes philippinarum using NMR-based metabolomics. Mar.Pollut. Bull., 114:84-89.
Copyright © Haiyang Xuebao