Abstract
We collected samples of Pacific saury Cololabis saira (249–331 mm in knob length; ages 0 and 1) in the North Pacific Ocean from 154°E to 165°W during their northward migration in the early summers of 2013, 2014, and 2015, and measured the stable nitrogen and carbon isotope ratios (δ15N and δ13C) of their muscle tissues. A hierarchical cluster analysis based on δ15N and δ13C yielded three groups (G1–G3). G1 (mean δ15N: 12.9%; mean δ13C: –20.3%) had the highest δ15N and occurred only in the eastern area of 170° W in 2013 and 2015. G2 (δ15N: 9.3%; δ13C: −20.1%) and G3 (δ15N: 7.3%, δ13C: −20.9%) occurred in all years mainly in eastern and western areas of 170° W, respectively. The latter two groups presented reasonable δ15N and δ13C considering the trophic enrichment and potential prey such as Neocalanus copepods that exist in each area. In contrast, the substantially enriched δ15N of G1 was characteristic of organisms at higher trophic levels in the same area. Thus, this group is most likely an immigrant from outside the survey area. This study showed that Pacific saury utilize different ecosystems east and west of 170° W during their northward migration.
Similar content being viewed by others
References
Baitaliuk AA, Orlov AM, Ermakov YK (2013) Characteristic features of ecology of the Pacific saury Cololabis saira (Scomberesocidae, Beloniformes) in open waters and in the northeast Pacific Ocean. J Ichthyol 53:899–913
Carle RD, Beck JN, Calleri DM, Hester MM (2015) Temporal and sex-specific variability in Rhinoceros Auklet diet in the central California Current system. J Mar Syst 146:99–108
Chiba S, Sugisaki H, Kuwata A, Tadokoro K, Kobari T, Yamaguchi A, Mackas DL (2012) Pan-North Pacific comparison of long-term variation in Neocalanus copepods based on stable isotope analysis. Prog Oceanogr 97–100:63–75
Chow S, Suzuki N, Brodeur RD, Ueno Y (2009) Little population structuring and recent evolution of the Pacific saury (Cololabis saira) as indicated by mitochondrial and nuclear DNA sequence data. J Exp Mar Biol Ecol 369:17–21
Choy CA, Popp BN, Hannides CCS, Drazen JC (2015) Trophic structure and food resources of epipelagic and mesopelagic fishes in the North Pacific Subtropical Gyre ecosystem inferred from nitrogen isotopic compositions. Limnol Oceanogr 60:1156–1171
Davies WE, Hipfner JM, Hobson KA, Ydenberg RC (2009) Seabird seasonal trophodynamics: isotopic patterns in a community of Pacific alcids. Mar Ecol Prog Ser 382:211–219
Favorite F, Dodimead AJ, Nasu K (1976) Oceanography of the subarctic Pacific region, 1960–1971. Int North Pac Fish Comm Bull 33:1–187
Fuji T, Kurita Y, Suyama S, Ambe D (2020) Estimating the spawning ground of Pacific saury Cololabis saira by using the distribution and geographical variation in maturation status of adult fish during the main spawning season. Fish Oceanogr. https://doi.org/10.1111/fog.12525
Fukushima S (1979) Synoptic analysis of migration and fishing conditions of saury in the northwest Pacific Ocean. Bull Tohoku Reg Fish Res Lab 41:1–70 ((In Japanese with English abstract))
Glaser SM, Waechter KE, Bransome NC (2015) Through the stomach of a predator: regional patterns of forage in the diet of albacore tuna in the California Current system and metrics needed for ecosystem-based management. J Mar Syst 146:38–49
Gould P, Ostrom P, Walker W (2000) Foods, trophic relationships, and migration of sooty and short-tailed shearwaters associated with squid and large-mesh driftnet fisheries in the North Pacific Ocean. Waterbirds 23:165–186
Graham BS, Grubbs D, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar Biol 150:647–658
Horii S, Takahashi K, Shiozaki T, Hashihama F, Furuya K (2018) Stable isotopic evidence for the differential contribution of diazotrophs to the epipelagic grazing food chain in the mid-Pacific Ocean. Global Ecol Biogeogr 27:1467–1480
Hubbs CL, Wisner RL (1980) Revision of the saury (Pisces, Scomberescocidae) with descriptions of two new species. US Fish Bull 77:521–566
Iwahashi M, Isoda Y, Ito S, Oozeki Y, Suyama S (2006) Estimation of seasonal spawning ground locations and ambient sea surface temperatures for eggs and larvae of Pacific saury (Cololabis saira) in the western North Pacific. Fish Oceanogr 15:125–138. https://doi.org/10.1111/j.1365-2419.2005.00384.x
Kaeriyama M, Nakamura M, Edpalina R, Bower JR, Yamaguchi H, Walker RV, Myers KW (2004) Change in feeding ecology and trophic dynamics of Pacific salmon (Oncorhynchus spp.) in the central Gulf of Alaska in relation to climate events. Fish Oceanogr 13:197–207
Kimura K (1956) The standard length of the Pacific saury, Cololabis saira (Brevoort). Bull Tohoku Reg Fish Res Lab 7:1–11 ((In Japanese with English abstract))
Kosaka S (2000) Life history of the Pacific saury Cololabis saira in the northwest Pacific and considerations on resource fluctuations based on it. Bull Tohoku Natl Fish Res Inst 63:1–96 ((In Japanese with English abstract))
Kosaka S, Watanabe Y, Tanino Y, Takahashi S (1985) Ecology of the Pacific saury Cololabis saira BREVOORT determined by the distribution of its parasite Pennella sp. Bull Tohoku Reg Fish Res Lab 47:79–91 ((In Japanese with English abstract))
Kurita Y, Nemoto Y, Oozeki Y, Hayashizaki K, Ida H (2004) Variations in patterns of daily changes in otolith increment widths of 0+ Pacific saury, Cololabis saira, off Japan by hatch date in relation to the northward feeding migration during spring and summer. Fish Oceanogr 13(Suppl. 1):54–62
Laws EA, Popp BN, Bidigare RR, Kennicutt MC, Macko SA (1995) Dependence of hytoplankton carbon isotopic composition on growth rate and [CO2]aq: Theoretical considerations and experimental results. Geochim Cosmochim Acta 59:1131–1138
Madigan DJ, Carlisle AB, Dewar H, Snodgrass OE, Litvin SY, Micheli F, Block BA (2012) Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem. Sci Rep 2:654
Matsubayashi J, Osada Y, Tadokoro K, Abe Y, Yamaguchi A, Shirai K, Honda K, Yoshikawa C, Ogawa ON, Ohkouchi N, Ishikawa FN, Nagata T, Miyamoto H, Nishino S, Tayasu I (2020) Tracking long-distance migration of marine fishes using compound-specific stable isotope analysis of amino acids. Ecol Lett 23:881–890
Miller TW, Brodeur RD, Rau G, Omori K (2010) Prey dominance shapes trophic structure of the northern California Current pelagic food web: evidence from stable isotopes and diet analysis. Mar Ecol Prog Ser 420:15–26
Miller TW, Van der Lingen C, Brodeur R, Omori K, Hamaoka H, Isobe T (2011) Understanding what drives food web structure in marine pelagic ecosystems. In: Omori K, Guo X, Yoshie N, Fujii N, Handoh IC, Isobe A, Tanabe S (eds) Interdisciplinary studies on environmental chemistry—marine environmental modeling and analysis. TERRA-PUB, Tokyo, pp 125−131
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochem Cosmochem Acta 48:1135–1140
Minagawa M, Ohashi M, Kuramoto T, Noda N (2001) δ15N of PON and nitrate as a clue to the origin and transformation of nitrogen in the subarctic North Pacific and its marginal sea. J Oceanogr 57:285–300
Minami H, Ogi H (1997) Determination of migratory dynamics of the sooty shearwater in the Pacific using stable carbon and nitrogen isotope analysis. Mar Ecol Prog Ser 158:249–256
Minami H, Minagawa M, Ogi H (1995) Changes in stable carbon and nitrogen isotope ratios in sooty and short-tailed shearwaters during their northward migration. Condor 97:565–574
Mitani Y, Bando T, Takai N, Sakamoto W (2006) Patterns of stable carbon and nitrogen isotopes in the baleen of common minke whale Balaenoptera acutorostrata from the western North Pacific. Fish Sci 72:69–76
Miyamoto H, Suyama S, Vijai D, Kidokoro H, Naya M, Fuji T, Sakai M (2019) Predicting the timing of Pacific saury (Cololabis saira) immigration to Japanese fishing grounds: A new approach based on natural tags in otolith annual rings. Fish Res 209:167–177
Miyamoto H, Vijai D, Kidokoro H, Tadokoro K, Watanabe T, Fuji T, Suyama S (2020) Geographic variation in feeding of Pacific saury Cololabis saira in June and July in the North Pacific Ocean. Fish Oceanogr 29:558–571
Morinville GR, Rasmussen JB (2006) Marine feeding patterns of anadromous brook trout (Salvelinus fontinalis) inhabiting an estuarine river fjord. Can J Fish Aquat Sci 63:2011–2027
Nagasawa K, Ishida K, Nakamura S (1984) Occurrence of Pennella sp. (Copepoda: Pennellidae) on the saury, Cololabis saira, in Japanese and central North Pacific waters in 1983. J Hokkaido Fish Exp Stat (hokusuishi Geppo) 41:221–236 ((In Japanese))
Navarro J, Coll M, Somes CJ, Olson RJ (2013) Trophic niche of squids: Insights from isotopic data in marine systems worldwide. Deep-Sea Res II 95:93–102
Odate K (1977) On the feeding habits of the Pacific saury, Cololabis saira (Brevoort). Bull Tohoku Reg Fish Res Lab 38:75–88 ((In Japanese with English abstract))
Ohshimo S, Madigan DJ, Kodama T, Tanaka H, Komoto K, Suyama S, Ono T, Yamakawa T (2019) Isoscapes reveal patterns of δ13C and δ15N of pelagic forage fish and squid in the Northwest Pacific Ocean. Prog Oceanogr 175:124–138
Parry M (2008) Trophic variation with length in two ommastrephid squids: Ommastrephes bartramii and Sthenoteuthis oualaniensis. Mar Biol 153:249–256
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718
Saino T, Hattori A (1987) Geographical variation of the water column distribution of suspended particulate organic nitrogen and its 15N natural abundance in the Pacific and its marginal seas. Deep-Sea Res 34:807–827
Shiomoto A, Hashimoto S (2000) Comparison of east and west chlorophyll a standing stock and oceanic habitat along the Transition Domain of the North Pacific. J Plankton Res 22:1–14
Somes CJ, Schmittner A, Galbraith ED, Lehmann MF, Altabet MA, Montoya JP, Letelier RM, Mix AC, Bourbonnais A, Eby M (2010) Simulating the global distribution of nitrogen isotopes in the ocean. Global Biogeochem Cycl 24:GB4019
Spero HJ, Bijma J, Lea DW, Bemis BE (1997) Effect of seawater carbonate concentration of foraminiferal carbon and oxygen isotopes. Nature 390:497–500
Sugisaki H, Kurita Y (2004) Daily rhythm and seasonal variation of feeding habit of Pacific saury (Cololabis saira) in relation to their migration and oceanographic conditions off Japan. Fish Oceanogr 13(Suppl. 1):63–73
Suyama S, Kurita Y, Ueno Y (2006) Age structure of Pacific saury Cololabis saira based on observations of the hyaline zones in the otolith and length frequency distributions. Fish Sci 72:742–749
Suyama S, Nakagami M, Naya M, Ueno Y (2012a) Migration route of Pacific saury Cololabis saira inferred from the otolith hyaline zone. Fish Sci 78:1179–1186
Suyama S, Nakagami M, Naya M, Ueno Y (2012b) Comparison of the growth of age-1 Pacific saury Cololabis saira in the Western and the Central North Pacific. Fish Sci 78:277–285
Suyama S, Ozawa H, Shibata Y, Fuji T, Nakagami M, Shimizu A (2019) Geographical variation in spawning histories of age-1 Pacific saury Cololabis saira in the North Pacific Ocean during June and July. Fish Sci 85:495–507
Taka S, Kitakata M, Wada T (1982) The relations between the saury, Cololabis saira (BREVOORT) and the food organisms on especially Calanus plumchrus, in the southeast waters of the Kuril islands during the summer. Bull Hokkaido Reg Fish Res Lab 47:41–55
Takahashi K, Wada E, Sakamoto M (1991) Relation between carbon isotope dis-crimination and the specific growth rate of green algae, Chlamydomonas reinhardtii. Jpn J Limnol 52:105–112
Takai N, Onaka S, Ikeda Y, Yatsu A, Kidokoro H, Sakamoto W (2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. J Mar Biol Ass UK 80:675–684
Tanaka H, Takasuka A, Aoki I, Ohshimo S (2008) Geographical variations in the trophic ecology of Japanese anchovy, Engraulis japonicus, inferred from carbon and nitrogen stable isotope ratios. Mar Biol 154:557–568
Tawa A, Ishihara T, Uematsu Y, Ono T, Ohshimo S (2017) Evidence of westward transoceanic migration of Pacific bluefin tuna in the Sea of Japan based on stable isotope analysis. Mar Biol 164:94
Ueno Y, Suyama S, Kurita Y, Kumazawa T (2004) Design and operation methods of a mid-water trawl for quantitative sampling of a surface pelagic fish, Pacific saury (Cololabis saira). Fish Res 66:3–17
Ueno Y, Suyama S, Nakagami M, Naya M, Sakai M, Kurita Y (2017) Direct estimation of stock abundance of Pacific saury Cololabis saira in the northwestern Pacific Ocean using a mid-water trawl. Fish Sci 83:23–33
Watanabe Y, Kosaka S, Tanino Y, Takahashi S (1985) Occurrence of parasitic copepod Pennella sp. on the Pacific saury Cololabis saira in 1983. Bull Tohoku Reg Fish Res Lab 47:37–46 ((In Japanese with English abstract))
Watanabe Y, Butler JL, Mori T (1988) Growth of Pacific saury, Cololabis saira, in the northeastern and northwestern Pacific Ocean. Fish Bull 86:489–498
Welch DW, Parsons TR (1993) δ13C-δ15N values as indicators of trophic position and competitive overlap for Pacific salmon (Oncorhynchus spp.). Fish Oceanogr 2(1):11–23
Yasuda I, Kitagawa D (1996) Locations of early fishing grounds of saury in the north-western Pacific. Fish Oceanogr 5:63–69
Yasunaka S, Nojiri Y, Nakaoka S, Ono T, Mukai H, Usui N (2013) Monthly maps of sea surface dissolved inorganic carbon in the North Pacific: basin-wide distribution and seasonal variation. J Geophys Res Oceans 118:3843–3850
Yatsu A (2019) Review of population dynamics and management of small pelagic fishes around the Japanese Archipelago. Fish Sci 85:611–639
Yoshikawa C, Makabe A, Matusi Y, Nunoura T, Ohkouchi N (2018) Nitrate isotope distribution in the subarctic and subtropical North Pacific. Geochem Geophys Geosys 19:2212–2224
Zanden MJV, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015) Stable isotope turnover and half-life in animal tissues: A literature synthesis. PLoS ONE 10:e0116182. https://doi.org/10.1371/journal.pone.0116182
Acknowledgements
The authors thank the crew of the Hokuho-maru and Hokko-maru for their cooperation and Mss. Junko Momosawa, Naoko Kubo, and Kanae Okabori for otolith extraction, light microscope photography, and stable isotope analysis. The authors also thank Drs. Dharmamony Vijai, Tsuyoshi Watanabe, and Seiji Ohshimo for their constructive comments and informative discussions. This work was partially supported by the Fisheries Agency of Japan.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fuji, T., Nakagami, M., Suyama, S. et al. Geographical differences in the stable isotope ratios of Pacific saury in the North Pacific Ocean. Fish Sci 87, 529–540 (2021). https://doi.org/10.1007/s12562-021-01528-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-021-01528-3