The influence of lipid-extraction on the δ<sup>13</sup>C of mesopelagic and demersal fish in the South China Sea: modification and application of lipid normalization models

Linyu Wang; Fuqiang Wang; Zuozhi Chen; Ying Wu

doi:10.1007/s13131-022-2045-x

Volume 42 Issue 1

Jan. 2023

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Article Navigation > Acta Oceanologica Sinica > 2023 > 42(1): 35-43

Linyu Wang, Fuqiang Wang, Zuozhi Chen, Ying Wu. The influence of lipid-extraction on the δ13C of mesopelagic and demersal fish in the South China Sea: modification and application of lipid normalization models[J]. Acta Oceanologica Sinica, 2023, 42(1): 35-43. doi: 10.1007/s13131-022-2045-x

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Linyu Wang, Fuqiang Wang, Zuozhi Chen, Ying Wu. The influence of lipid-extraction on the δ¹³C of mesopelagic and demersal fish in the South China Sea: modification and application of lipid normalization models[J]. Acta Oceanologica Sinica, 2023, 42(1): 35-43. doi: 10.1007/s13131-022-2045-x

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The influence of lipid-extraction on the δ¹³C of mesopelagic and demersal fish in the South China Sea: modification and application of lipid normalization models

doi: 10.1007/s13131-022-2045-x

Linyu Wang¹,
Fuqiang Wang^{1, 2},
Zuozhi Chen³,
Ying Wu^{1
,
,}

1.
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200241, China
2.
Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
3.
South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 100141, China

Funds: the National Natural Science Foundation of China under contract Nos 42090043 and 41876074; the National Basic Research Program (973 Program) of China under contract No. 2014CB441502.

More Information

Corresponding author: E-mail: wuying@sklec.ecnu.edu.cn
Received Date: 2021-12-31
Accepted Date: 2022-04-06

Available Online: 2022-10-28

Publish Date: 2023-01-25

Abstract

Abstract

Mesopelagic fish, the most important daily vertically migrating community in the oceans, are characterized by high lipid content which may obscure the interpretation of stable isotopes analysis. Demersal fish, which are important consumers in the food web dominated by mesopelagic fish, also have a high lipid content. Here we collected 127 fish samples from the South China Sea and evaluated the effect of lipid contents on δ¹³C of mesopelagic and demersal fish. In lipid-extracted mesopelagic fish, the C/N content ratio (<5.5) shows a clear correlation with Δδ¹³C (the offset of bulk and lipid-extracted δ¹³C values), especially in non-migratory and semi-migratory species; these values were less correlation in demersal fish. Based on our results, we suggest that mesopelagic and demersal fish in different regions of the South China Sea should be studied separately using appropriate correction models and less fit for the traditional model. Moreover, the C/N content ratio should be used cautiously for establishing the lipid normalization model, especially for the fish in migratory mesopelagic fish and demersal fish. Our results also reveal that mesopelagic fish across nearby regions could be analyzed together. The new models described here can be applied in future studies of mesopelagic and demersal fish in the South China Sea.
- mesopelagic fish,
- demersal fish,
- lipid normalization model,
- C/N content ratio,
- lipid content,
- δ¹³C,
- South China Sea

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References

Abrantes K G, Semmens J M, Lyle J M, et al. 2012. Normalisation models for accounting for fat content in stable isotope measurements in salmonid muscle tissue. Marine Biology, 159(1): 57–64. doi: 10.1007/s00227-011-1789-1

Bowen W D, Boness D J, Oftedal O T. 1987. Mass transfer from mother to pup and subsequent mass loss by the weaned pup in the hooded seal, Cystophora cristata. Canadian Journal of Zoology, 65(1): 1–8. doi: 10.1139/z87-001

Catul V, Gauns M, Karuppasamy P K. 2011. A review on mesopelagic fishes belonging to family Myctophidae. Reviews in Fish Biology and Fisheries, 21(3): 339–354. doi: 10.1007/s11160-010-9176-4

Chen Suzhi. 2002. Fauna Sinica: Ostichthyes (Myctophiformmes, Cetomimiformes and Osteoglossiformes) (in Chinese). Beijing: Science Press, 1–304

Chen Dagang, Zhang Meizhao. 2015. Marine Fishes of China (in Chinese). Qingdao: China Ocean University Press, 1–2152

Cherel Y, Fontaine C, Richard P, et al. 2010. Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnology & Oceanography, 55(1): 324–332. doi: 10.4319/lo.2010.55.1.0324

Cloyed C S, Dacosta K P, Hodanbosi M R, et al. 2020. The effects of lipid extraction on δ¹³C and δ¹⁵N values and use of lipid-correction models across tissues, taxa and trophic groups. Methods in Ecology and Evolution, 11(6): 751–762. doi: 10.1111/2041-210x.13386

Cloyed C S, Eason P K. 2016. Different ecological conditions support individual specialization in closely related, ecologically similar species. Evolutionary Ecology, 30(3): 379–400. doi: 10.1007/s10682-016-9825-8

Colaço A, Giacomello E, Porteiro F, et al. 2013. Trophodynamic studies on the Condor seamount (Azores, Portugal, North Atlantic). Deep-Sea Research Part II: Topical Studies in Oceanography, 98: 178–189. doi: 10.1016/j.dsr2.2013.01.010

Cui Ying, Wu Ying, Xu Zhaoli, et al. 2015. Potential dietary influence on the stable isotopes and fatty acid composition of migratory anchovy (Coilia mystus) around the Changjiang Estuary. Journal of the Marine Biological Association of the United Kingdom, 95(1): 193–205. doi: 10.1017/S0025315414000873

De Lecea A M, De Charmoy L. 2015. Chemical lipid extraction or mathematical isotope correction models: Should mathematical models be widely applied to marine species?. Rapid Communications in Mass Spectrometry, 29(21): 2013–2025. doi: 10.1002/rcm.7310

DeNiro M J, Epstein S. 1977. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science, 197(4300): 261–263. doi: 10.1126/science.327543

Eduardo L N, Bertrand A, Mincarone M M, et al. 2021. Distribution, vertical migration, and trophic ecology of lanternfishes (Myctophidae) in the Southwestern Tropical Atlantic. Progress in Oceanography, 199: 102695. doi: 10.1016/j.pocean.2021.102695

Fagan K A, Koops M A, Arts M T, et al. 2011. Assessing the utility of C:N ratios for predicting lipid content in fishes. Canadian Journal of Fisheries and Aquatic Sciences, 68(2): 374–385. doi: 10.1139/f10-119

Fanelli E, Cartes J E, Papiol V. 2011. Food web structure of deep-sea macrozooplankton and micronekton off the Catalan slope: Insight from stable isotopes. Journal of Marine Systems, 87(1): 79–89. doi: 10.1016/j.jmarsys.2011.03.003

Flynn A J, Kloser R J. 2012. Cross-basin heterogeneity in lanternfish (family Myctophidae) assemblages and isotopic niches (δ¹³C and δ¹⁵N) in the southern Tasman Sea abyssal basin. Deep-Sea Research Part I: Oceanographic Research Papers, 69: 113–127. doi: 10.1016/j.dsr.2012.07.007

Folch J, Lees M, Stanley G H S. 1957. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry, 226(1): 497–509. doi: 10.1016/S0021-9258(18)64849-5

Gong Yuyan, Chen Zuozhi, Zhang Jun, et al. 2015a. Feeding habits of Diaphus chrysorhynchus from continental slope region in northern South China Sea in autumn. South China Fisheries Science, 11(5): 90–99. doi: 10.3969/j.issn.2095-0780.2015.05.011

Gong Chenglin, Wang Yingmin, Xu Shang, et al. 2015b. The northeastern South China Sea margin created by the combined action of down-slope and along-slope processes: Processes, products and implications for exploration and paleoceanography. Marine & Petroleum Geology, 64: 233–249. doi: 10.1016/j.marpetgeo.2015.01.016

Hoffman J C, Sierszen M E, Cotter A M. 2015. Fish tissue lipid-C:N relationships for correcting δ¹³C values and estimating lipid content in aquatic food-web studies. Rapid Communications in Mass Spectrometry, 29(21): 2069–2077. doi: 10.1002/rcm.7367

Hoffman J C, Sutton T T. 2010. Lipid correction for carbon stable isotope analysis of deep-sea fishes. Deep-Sea Research Part I: Oceanographic Research Papers, 57(8): 956–964. doi: 10.1016/j.dsr.2010.05.003

Hu Jianyu, Kawamura H, Hong Huasheng, et al. 2000. A review on the currents in the South China Sea: seasonal circulation, South China Sea warm current and Kuroshio intrusion. Journal of Oceanography, 56(6): 607–624. doi: 10.1023/A:1011117531252

Hudson J M, Steinberg D K, Sutton T T, et al. 2014. Myctophid feeding ecology and carbon transport along the northern Mid-Atlantic Ridge. Deep-Sea Research Part I: Oceanographic Research Papers, 93: 104–116. doi: 10.1016/j.dsr.2014.07.002

Irigoien X, Klevjer T A, Røstad A, et al. 2014. Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nature Communications, 5: 3271. doi: 10.1038/ncomms4271

Jin Haiwei, Xue Lijian, Pan Guoliang, et al. 2011. Feeding habits of Benthosema pterotum in the East China Sea and southern part of Yellow Sea. Marine Fisheries, 33(4): 368–377. doi: 10.3969/j.issn.1004-2490.2011.04.002

Jónasdóttir S H, Visser A W, Richardson K, et al. 2015. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. Proceedings of the National Academy of Sciences of the United States of America, 112(39): 12122–12126. doi: 10.1073/pnas.1512110112

Kong Xiaolan, Jiang Yane, Gong Yuyan, et al. 2016. A preliminary study on fishery biology of Ceratoscopelus warmingii in the central and northern South China Sea. South China Fisheries Science, 12(4): 117–124. doi: 10.3969/j.issn.2095-0780.2016.04.015

Layman C A, Arrington D A, Montaña C G, et al. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure?. Ecology, 88(1): 42–48. doi: 10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2

Li Kaizhi, Yin Jianqiang, Huang Liangmin, et al. 2011. Distribution and abundance of thaliaceans in the northwest continental shelf of South China Sea, with response to environmental factors driven by monsoon. Continental Shelf Research, 31(9): 979–989. doi: 10.1016/j.csr.2011.03.004

Lin Mao, Lin Rongcheng. 2006. Seasonal abundance and distribution of pelagic tunicates (Chordata: Thaliacea) in the central South China Sea. Acta Oceanologica Sinica, 25(3): 148–156

Logan J M, Jardine T D, Miller T J, et al. 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology, 77(4): 838–846. doi: 10.1111/j.1365-2656.2008.01394.x

Masuda H, Amaoka K, Araga C, et al. 1984. The Fishes of the Japanese Archipelago. Tokyo: Tokal University Press, 1–374

McClain-Counts J P, Demopoulos A W J, Ross S W. 2017. Trophic structure of mesopelagic fishes in the Gulf of Mexico revealed by gut content and stable isotope analyses. Marine Ecology, 38(4): e12449. doi: 10.1111/maec.12449

McConnaughey T, Mcroy C P. 1979. Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Marine Biology, 53(3): 257–262. doi: 10.1007/bf00952434

Molina-Valdivia V, Bustos C A, Castillo M I, et al. 2021. Oceanographic influences on the early life stages of a mesopelagic fish across the Chilean Patagonia. Progress in Oceanography, 195: 102572. doi: 10.1016/j.pocean.2021.102572

Newsome S D, Chivers S J, Kowalewski M B. 2018. The influence of lipid-extraction and long-term DMSO preservation on carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values in cetacean skin. Marine Mammal Science, 34(2): 277–293. doi: 10.1111/mms.12454

Newsome S D, Clementz M T, Koch P L. 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science, 26(3): 509–572. doi: 10.1111/j.1748-7692.2009.00354.x

Olivar M P, Bernal A, Molí B, et al. 2012. Vertical distribution, diversity and assemblages of mesopelagic fishes in the western Mediterranean. Deep-Sea Research Part I: Oceanographic Research Papers, 62: 53–69. doi: 10.1016/j.dsr.2011.12.014

Olivar M P, Bode A, López-Pérez C, et al. 2019. Trophic position of lanternfishes (Pisces: Myctophidae) of the tropical and equatorial Atlantic estimated using stable isotopes. ICES Journal of Marine Science, 76(3): 649–661. doi: 10.1093/icesjms/fsx243

Park H J, Park T H, Lee C I, et al. 2018. Ontogenetic shifts in diet and trophic position of walleye pollock, Theragra chalcogramma, in the western East Sea (Japan Sea) revealed by stable isotope and stomach content analyses. Fisheries Research, 204: 297–304. doi: 10.1016/j.fishres.2018.03.006

Patterson H K, Carmichael R H. 2016. The effect of lipid extraction on carbon and nitrogen stable isotope ratios in oyster tissues: Implications for glycogen-rich species. Rapid Communications in Mass Spectrometry, 30(24): 2594–2600. doi: 10.1002/rcm.7759

Peterson B J, Fry B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology & Systematics, 18(1): 293–320. doi: 10.1146/annurev.es.18.110187.001453

Post D M. 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology, 83(3): 703–718. doi: 10.1890/0012-9658(2002)083[0703:Usitet]2.0.Co;2

Post D M, Layman C A, Arrington D A, et al. 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152(1): 179–189. doi: 10.1007/s00442-006-0630-x

Quintana-Rizzo E, Torres J J, Ross S W, et al. 2015. δ¹³C and δ¹⁵N in deep-living fishes and shrimps after the Deepwater Horizon oil spill, Gulf of Mexico. Marine Pollution Bulletin, 94(1–2): 241–250. doi: 10.1016/j.marpolbul.2015.02.002

Richards T M, Gipson E E, Cook A, et al. 2019. Trophic ecology of meso- and bathypelagic predatory fishes in the Gulf of Mexico. ICES Journal of Marine Science, 76(3): 662–672. doi: 10.1093/icesjms/fsy074

Saito H, Murata M. 1998. Origin of the monoene fats in the lipid of midwater fishes: relationship between the lipids of myctophids and those of their prey. Marine Ecology Progress Series, 168: 21–33. doi: 10.3354/meps168021

Satterfield F R, Finney B P. 2002. Stable isotope analysis of Pacific salmon: insight into trophic status and oceanographic conditions over the last 30 years. Progress in Oceanography, 53(2–4): 231–246,

Shen Shih-chieh. 1993. Fishes of Taiwan (in Chinese). Taipei: National Taiwan University, 1–960

Stowasser G, McAllen R, Pierce G J, et al. 2009a. Trophic position of deep-sea fish—Assessment through fatty acid and stable isotope analyses. Deep-Sea Research Part I: Oceanographic Research Papers, 56(5): 812–826. doi: 10.1016/j.dsr.2008.12.016

Stowasser G, Pond D W, Collins M A. 2009b. Using fatty acid analysis to elucidate the feeding habits of Southern Ocean mesopelagic fish. Marine Biology, 156(11): 2289–2302. doi: 10.1007/s00227-009-1256-4

Su Jilan. 2004. Overview of the South China Sea circulation and its influence on the coastal physical oceanography outside the Pearl River Estuary. Continental Shelf Research, 24(16): 1745–1760. doi: 10.1016/j.csr.2004.06.005

Sun Dianrong, Chen Zheng. 2013. Review of Fishes of South China Sea: Volume One (in Chinese). Beijing: China Ocean Press, 1–606

Sutton T T. 2013. Vertical ecology of the pelagic ocean: classical patterns and new perspectives. Journal of Fish Biology, 83(6): 1508–1527. doi: 10.1111/jfb.12263

Svensson E, Freitas V, Schouten S, et al. 2014. Comparison of the stable carbon and nitrogen isotopic values of gill and white muscle tissue of fish. Journal of Experimental Marine Biology & Ecology, 457: 173–179. doi: 10.1016/j.jembe.2014.04.014

Tocher D R. 2003. Metabolism and functions of lipids and fatty acids in teleost fish. Reviews in Fisheries Science, 11(2): 107–184. doi: 10.1080/713610925

Valls M, Olivar M P, Fernández de Puelles M L, et al. 2014. Trophic structure of mesopelagic fishes in the western Mediterranean based on stable isotopes of carbon and nitrogen. Journal of Marine Systems, 138: 160–170. doi: 10.1016/j.jmarsys.2014.04.007

Wan Ruijing, Wu Ying, Huang Liang, et al. 2010. Fatty acids and stable isotopes of a marine ecosystem: study on the Japanese anchovy (Engraulis japonicus) food web in the Yellow Sea. Deep-Sea Research Part II: Topical Studies in Oceanography, 57(11–12): 1047–1057,

Wang Fuqiang, Wu Ying, Chen Zuozhi, et al. 2019a. Trophic interactions of mesopelagic fishes in the South China Sea illustrated by stable isotopes and fatty acids. Frontiers in Marine Science, 5: 522. doi: 10.3389/fmars.2018.00522

Wang Fuqiang, Wu Ying, Cui Ying, et al. 2019b. δ¹³C and fatty acid composition of mesopelagic fishes in the South China Sea and their influence factors. Chemistry and Ecology, 35(9): 788–804. doi: 10.1080/02757540.2019.1651844

Wang Na, Wu Ying, Zhang Jing. 2009. Comparison and unification of carbon stable isotope ratios in specific aquatic biota. Communications in Nonlinear Science and Numerical Simulation, 14(5): 2502–2506. doi: 10.1016/j.cnsns.2008.05.015

Weldrick C K, Trebilco R, Swadling K M. 2019. Can lipid removal affect interpretation of resource partitioning from stable isotopes in Southern Ocean pteropods?. Rapid Communications in Mass Spectrometry, 33(6): 569–578. doi: 10.1002/rcm.8384

Yu Jie, Chen Guobao, Zhang Kui, et al. 2016. Vertical distribution of summer chlorophyll a concentration in the middle South China Sea. South China Fisheries Science, 12(4): 1–8

Yurkowski D J, Hussey N E, Semeniuk C, et al. 2015. Effects of lipid extraction and the utility of lipid normalization models on δ¹³C and δ¹⁵N values in Arctic marine mammal tissues. Polar Biology, 38(2): 131–143. doi: 10.1007/s00300-014-1571-1

Zhang Yi, Li Jie, Cheng Xuhua, et al. 2018. Community differentiation of bacterioplankton in the epipelagic layer in the South China Sea. Ecology and Evolution, 8(10): 4932–4948. doi: 10.1002/ece3.4064

Zhang Jun, Wang Xinliang, Jiang Yane, et al. 2019. Species composition and biomass density of mesopelagic nekton of the South China Sea continental slope. Deep-Sea Research Part II: Topical Studies in Oceanography, 167: 105–120. doi: 10.1016/j.dsr2.2018.06.008

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