Academic Scientific JournalsCorrelation between δ13C and δ15N in flying fish (Exocoetus volitans) muscle and scales from the South China Sea
Keywords:
flying fish, muscle, scales, stable isotope analysis, South China SeaAbstract
We collected flying fish (Exocoetus volitans) from the South China Sea to determine whether fish scale isotope values correlate with those from muscle, and discuss relevant eco-environmental implications. A significant positive correlation was determined between fish scales and muscle δ13C and δ15N, rendering a fish scale an alternative to muscle tissue for stable isotope analysis. However, muscle and scale isotopic offsets should be fully considered when using δ13C and δ15N to analyze the actual trophic level of fish and their food source. The average offsets of δ13C and δ15N between muscles and scales are -2.1 ± 0.5‰ and 2.3 ± 0.6‰, respectively, though these values vary slightly with fish mass. Weak correlations were found between δ13C and δ15N, both in the flying fish muscle and scales, suggesting that other factors are influencing δ13C and δ15N. Fish δ15N also correlates with the size of individuals, while δ13C reflects the marine habitat. Based on our data, it appears that more eco-environmental processes can be revealed from modern or ancient flying fish scales.
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Amezcua, F., Muro-Torres, V. & Soto-Jiménez, M.F. (2015). Stable isotope analysis versus TROPH: a comparison of methods for estimating fish trophic positions in a subtropical estuarine system. Aquatic Ecology 49: 235-250. DOI: 10.1007/s10452-015-9517-4.
Blanco, A., Deudero, S. & Box, A. (2009). Muscle and scale isotopic offset of three fish species in the Mediterranean Sea: Dentex dentex, Argyrosomus regius and Xyrichtys novacula. Rapid Communications in Mass Spectrometry 23: 2321-2328. DOI: 10.1002/rcm.4154.
Cano-Rocabayera, O., Maceda-Veiga, A. & de Sostoa, A. (2015). Fish fins and scales as non-lethally sampled tissues for stable isotope analysis in five fish species of north-eastern Spain. Environmental Biology of Fishes 98: 925-932. DOI: 10.1007/s10641-014-0328-6.
Cao, L., Wang, Q.S., Yang, J.P. & Cheng, Y.Y. (2003). Staged investigation report of waterbirds on Xisha Archipelago: Macroscopic ecology researches on Red-footed Booby on Dongdao Island. School of Life Sciences, University of Science and Technology of China, Hefei (In Chinese).
Cao, L. (2005). Population ecology of the Red-footed Booby on the Xisha archipelago. Unpublished doctoral dissertation. Lanzhou University.
DeNiro, M.J. & Epstein, S. ( 1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495-506. DOI: 10.1016/0016-7037(78)90199-0.
DeNiro, M.J. & Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341-351. DOI: 10.1016/0016-7037(81)90244-1.
Estep, M.L.F. & Vigg, S. (1985). Stable carbon and nitrogen isotope tracers of trophic dynamics in natural populations and fisheries of the Lahontan Lake system, Nevada. Canadian Journal of Fisheries and Aquatic Sciences, 42: 1712-1719. DOI: 10.1139/f85-215.
Field, J.C., Baltz, K., Phillips, A.J. & Walker, W.A. (2007). Range expansion and trophic interactions of the jumbo squid, Dosidicus gigas, in the California Current. California Cooperative Oceanic Fisheries Investigations Report, 48: 131.
Gerdeaux, D. & Perga, M.E. (2006). Changes in whitefish scales 13C during eutrophication and reoligotrophication of subalpine lakes. Limnology and Oceanography 51: 772-780. DOI: 10.4319/lo.2006.51.1_part_2.0772.
Hawke, D.J. & Holdaway, R.N. (2005). Avian assimilation and dispersal of carbon and nitrogen brought ashore by breeding Westland petrels (Procellaria westlandica): a stable isotope study. Journal of Zoology 266: 419-426. DOI: 10.1017/S0952836905007065.
Hobson, K.A. (1999). Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120: 314-326. DOI: 10.1007/s004420050865.
Hobson, K.A., Wassenaar, L.I., Milá, B., Lovette, I., Dingle, C. et al. (2003). Stable isotopes as indicators of altitudinal distributions and movements in an Ecuadorean hummingbird community. Oecologia 136: 302-308. DOI: 10.1007/s00442-003-1271-y.
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: 2069-2077. DOI: 10.1002/rcm.7367.
Inamura, O., Zhang, J. & Minagawa, M. (2012). δ13C and δ15N values in scales of Micropterus salmoides largemouth bass as a freshwater environmental indicator. Rapid Communications in Mass Spectrometry 26: 17-24. DOI: 10.1002/rcm.5288.
Jardine, T.D., Hunt, R.J., Pusey, B.J. & Bunn, S.E. (2011). A nonlethal sampling method for stable carbon and nitrogen isotope studies of tropical fishes. Marine and Freshwater Research, 62: 83-90. DOI: 10.1071/MF10211.
Kaehler, S., Pakhomov, E.A. & McQuaid, C.D. (2000). Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by δ13C and δ15N analysis. Marine Ecology Progress Series 208: 13-20. DOI: 10.3354/meps208013.
Logan, J.M. & Lutcavage, M.E. (2008). A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems. Rapid Communications in Mass Spectrometry 22: 1081-1086. DOI: 10.1002/rcm.3471.
Minagawa, M. & Wada, E. (1984). Stepwise enrichment of 15N along food chains: further evidence and the relations between δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135-1140. DOI: 10.1016/0016-7037(84)90204-7.
Navarro, J., Coll, M., Somes, C.J. & Olson, R.J. (2013). Trophic niche of squids: Insights from isotopic data in marine systems worldwide. Deep Sea Research Part II: Topical Studies in Oceanography 95: 93-102. DOI: 10.1016/j.dsr2.2013.01.031.
Perga, M.E. & Gerdeaux, D. (2003). Using the δ13C and δ15N of whitefish scales for retrospective ecological studies: changes in isotope signatures during the restoration of Lake Geneva, 1980-2001. Journal of Fish Biology 63: 1197-1207. DOI: 10.1046/j.1095-8649.2003.00239.x.
Pinnegar, J.K. & Polunin, N.V.C. (1999). Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13: 225-231. DOI: 10.1046/j.1365-2435.1999.00301.x.
Post, D.M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718. DOI: 10.2307/3071875.
Pruell, R.J., Taplin, B.K. & Cicchelli, K. (2003). Stable isotope ratios in archived striped bass scales suggest changes in trophic structure. Fisheries Management and Ecology 10: 329-336. DOI: 10.1046/j.1365-2400.2003.00369.x.
Ramsay, A.L., Milner, N.J., Hughes, R.N. & Mccarthy, I.D. (2012). Fish scale δ15N and δ13C values provide biogeochemical tags of fish comparable in performance to element concentrations in scales and otoliths. Hydrobiologia 694: 183-196. DOI: 10.1007/s10750-012-1143-8.
Roussel, J.M., Perrier, C., Erkinaro, J., Niemelä, E., Cunjak, R.A. et al. (2014). Stable isotope analyses on archived fish scales reveal the long-term effect of nitrogen loads on carbon cycling in rivers. Global Change Biology, 20: 523-530. DOI: 10.1111/gcb.12293.
Saito, L., Johnson, B.M., Bartholow, J. & Hanna, R.B. (2011). Assessing ecosystem effects of reservoir operations using food web-energy transfer and water quality models. Ecosystems, 4: 105–125. DOI: 10.1007/s100210000062.
Schoeninger, M.J. & DeNiro, M.J. (1984). Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta, 48: 625-639. DOI: 10.1016/0016-7037(84)90091-7.
Schoeninger, M.J., Jim, M. & Sept, J.M. (1999). Subsistence strategies of two “savanna” chimpanzee populations: the stable isotope evidence. American Journal of Primatology 49: 297-314. DOI: 10.1111/j.1095-8649.2007.01434.x.
Sinnatamby, R.N., Bowman, J.E., Dempson, J.B. & Power, M. (2007). An assessment of de-calcification procedures for δ13C and δ15N analysis of yellow perch, walleye and Atlantic salmon scales. Journal of Fish Biology 70: 1630-1635. DOI: 10.1111/j.1095-8649.2007.01434.x.
Sisma-Ventura, G., Yam, R., Kress, N. & Shemesh, A. (2016). Water column distribution of stable isotopes and carbonate properties in the South-eastern Levantine basin (Eastern Mediterranean): Vertical and temporal change. Journal of Marine Systems 158: 13-25. DOI: 10.1016/j.jmarsys.2016.01.012.
Smith, A., Marty, J. & Power, M. (2015). Non-lethal sampling of lake sturgeon for stable isotope analysis: comparing pectoral fin-clip and dorsal muscle for use in trophic studies. Journal of Great Lakes Research 41: 292-297. DOI: 10.1016/j.jglr.2014.11.014.
Syväranta, J., Vesala, S., Rask, M., Ruuhijärvi, J. & Jones, R.I. (2008). Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 600: 121-130. DOI: 10.1007/s10750-007-9181-3.
Takai, N., Onaka, S., Ikeda, Y., Yatsu, A., Kidokoro, H. et al. (2000). Geographical variations in carbon and nitrogen stable isotope ratios in squid. Journal of the Marine Biological Association of the UK 80: 675-684. DOI: 10.1017/S0025315400002502.
Vander Zanden, M.J., Cabana, G. & Rasmussen, J.B. (1997). Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literaturę dietary data. Canadian Journal of Fisheries and Aquatic Sciences 54: 1142-1158. DOI: 10.1139/f97-016.
Vašek, M., Vejrík, L., Vejríková, I., Šmejkal, M., Baran, R. et al. (2017). Development of non-lethal monitoring of stable isotopes in asp (Leuciscus aspius): a comparison of muscle, fin and scale tissues. Hydrobiologia 785: 327-335. DOI: 10.1007/s10750-016-2940-2.
Vaughn, B.H., Evans, C.U., White, J.W., Still, C.J., Masarie, K.A. et al. (2010). Global network measurements of atmospheric trace gas isotopes. In J.B. West, G.J. Bowen, T.E. Dawson, K.P. Tu (Eds.), Isoscapes (pp. 3-31). Springer Netherlands.
Ventura, M. & Jeppesen, E. (2010). Evaluating the need for acid treatment prior to δ13C and δ15N analysis of freshwater fish scales: effects of varying scale mineral content, lake productivity and CO2 concentration. Hydrobiologia 644: 245-259. DOI: 10.1007/s10750-010-0121-2.
Wada, E., Mizutani, H. & Minagawa, M. (1991). The use of stable isotopes for food web analysis. Critical
Reviews in Food Science and Nutrition 30: 361-371. DOI: 10.1080/10408399109527547.
Wang, L.J. (2011). Animals in South China Sea. Guangxi Normal University Press, Guilin (In Chinese).
Wu, L.B., Liu, X.D., Fu, P.Q., Xu, L.Q., Li, D.N. et al. ( 2017). Dietary change in seabirds on Guangjin Island, South China Sea, over the past 1200 years inferred from stable isotope analysis. The Holocene 27: 331-338. DOI: 0959683616660163.
Xu, J., Zhang, M. & Xie, P. (2007). Size-related shifts in reliance on benthic and pelagic food webs by lake anchovy. Ecoscience 14: 170-177. DOI: 10.2980/1195-6860(2007)14[170:SSIROB]2.0.CO;2.
Xu, L.Q., Liu, X.D., Sun, L.G., Yan, H., Liu, Y. et al. (2011). Geochemical evidence for the development of coral Island ecosystem in the Xisha Archipelago of South China Sea from four ornithogenic sediment profiles. Chemical Geology, 286: 135-145. DOI: 10.1016/j.chemgeo.2011.04.015.
Xu, L,Q., Liu, X.D. & Jiang, S. (2014). Late-Holocene seabird palaeodietary record from Ganquan Island, South China Sea. Quaternary International 333: 139-145. DOI: 10.1016/j.quaint.2014.01.001.
Zhang, R.Q. (1956). Flying fish. Popular Science-Middle School Edition 8: 019 (In Chinese).
