Benthic-pelagic relations of aquatic organisms in various water masses of the Chukchi Sea by the data of δ¹⁵N and δ¹³С

To compare trophic characteristics for pelagic and benthic communities of zooplankton and zoobenthos in the Chukchi Sea, isotopic composition of carbon and nitrogen (δ¹⁵N and δ¹³С) was measured in two different water masses: i) the Bering Sea water with relatively high δ¹³С and low δ¹⁵N values that occupied the southern part of the sea (south of 71^о N), and ii) the cold Arctic water prevailed in its northern part were δ¹³С value was considerably lower and δ¹⁵N value was higher in 1–3 %. Stable difference in the isotopic composition of carbon is found between zooplankton and benthic invertebrates in the southern Chukchi Sea that means that benthic organisms base mainly on the benthic trophic chain and role of organic matter from the upper layer is not significant. About 90 % of the studied species of benthic fish are locked into the benthic trophic web there. In the northern Chukchi Sea, the benthic community consumes mainly the suspended organic matter produced in the water column, with prevalence of ice algae. All samples of benthic fish collected in this area have minimum content of heavy carbon δ¹³С with the values comparable to pelagic fish that indicates the main role of pelagic objects (60–80 %) in their feeding. The δ¹⁵N value reflects predatory habits of the animals. These values vary over a wide range both in the southern and northern areas that corresponds to the diet of the first, second or third order consumers.

1. Arashkevich, E.G., The food and feeding of copepods in the northwestern pacific, Oceanology, 1969, vol. 9, no. 5, pp. 857–873.

2. Yavnov, S.V., Atlas morskikh zvezd dal’nevostochnyy morey Rossii (Atlas of sea stars of the Far Eastern seas of Russia), Rakov, V.A., ed., Vladivostok: Russkiy Ostrov, 2010.

3. Yavnov, S.V., Atlas kishechnopolostnykh dal’nevostochnyy morey Rossii (Atlas of the coelenterates of the Far Eastern seas of Russia), Chuchukalo, V.I., ed., Vladivostok: Vladivostok: Russkiy Ostrov, 2010.

4. Brodskiy, K.A., Vyshkvartseva, N.V., Kos Ye.S., amd Markhaseva, Ye.L., Veslonogiye rakoobraznyye (Copepoda: Calanoida) morey SSSR i sopredel’nykh vod (Copepods (Copepoda: Calanoida) of the seas of the USSR and adjacent waters), Leningrad: Nauka, 1983, vol. 1.

5. Volkov, A.F. and Murphy, J.M., Plankton and diet of fish in the Chukchi Sea and the northern Bering Sea, in Byull. no. 2 realizatsii “Kontseptsii dal’nevostochnoi basseinovoi programmy izucheniya tikhookeanskikh lososei” (Bull. No. 2 Implementation “Concept of the Far Eastern Basin Program for the Study of Pacific Salmon”), Vladivostok: TINRO-Tsentr, 2007, pp. 70–80.

6. Geynrikh, A.K., Nutrition of marine copepods in the boreal and tropical regions of the Pacific Ocean, Tr. Inst. Okeanol. im. P.P. Shirshova, Akad. Nauk SSSR, 1963, vol. 71, pp. 60–71.

7. Golenkevich, A.V., Species composition and biology of bottom octopuses on the shelf of the north-western Japan Sea, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 1998, vol. 124, pp. 178–211.

8. Golikov, A.N., Buccininae mollusks of the World Ocean, Fauna SSSR. T. 5: Mollyuski (Fauna of the USSR, vol. 5: Mollusks), Leningrad: Nauka, 1980, no. 2.

9. Golikov, A.N. and Kusakin, O.G., Opredeliteli po faune SSSR, izdavaemye zoologicheskim institutom akademii nauk SSSR. T. 116. Rakovinnyye bryukhonogiye mollyuski litorali morey SSSR (Keys to Fauna Published by the Zoological Institute, USSR Academy of Sciences, vol. 116: Conch gastropods of the littoral of the seas of the USSR), Leningrad: Nauka, 1978.

10. Gorbatenko, K.M., Trophodynamics of aquatic organisms in the Sea of Okhotsk, Extended Abstract of Doctoral (Biol.) Dissertation, Vladivostok: TINRO-Tsentr, 2018.

11. Gorbatenko, K.M., Zavolokin, A.V., Merzlyakov, A.Yu., and Kiyashko, S.I., Trophic status of medusas (Cnidaria) of the Okhotsk Sea and their feeding habits in spring, Izv. Tikhookean. NauchnoIssled. Inst. Rybn. Khoz. Okeanogr., 2005, vol. 143, pp. 240–248.

12. Gorbatenko, K.M., Kiyashko, S.I., Lazhentsev, A.E., Nadtochiy, V.A., and Savin, A.B., Trophic benthic-pelagic interactions of the fish community in the shelf zone of western Bering sea revealed by analysis of stomach contents and stable isotopes of carbon and nitrogen, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2008, vol. 153, pp. 283–294.

13. Gorbatenko, K.M., Kiyashko, S.I., Lazhentsev, A.E., Emelin, P.O., and Grishan, R.P., Bentho-pelagic relations in the deep-water part of the Okhotsk sea by the data of stable isotopes C and N analysis, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2015, vol. 183, pp. 200–216. doi 10.26428/1606-9919-2015-183-200-216

14. Gorbatenko, K.M., Lazhentsev, A.E., and Loboda, S.V., Distribution, feeding, and some physiological parameters of the Pacific herring from the Gizhigin and Okhotsk populations in the north part of the Sea of Okhotsk in the spring season, Russ. J. Mar. Biol., 2004, vol. 30, no. 5, pp 298–305.

15. Gutel’makher, V.L., Sadchikov, A.P., and Filippova, T.G., Zooplankton Nutrition, Itogi nauki i tekhniki. Ser.: obshchaya ekologiya, biotsenologiya, gidrobiologiya (Results of Science and Technology. Ser.: general ecology, biocenology, hydrobiology), Moscow: Vseros. Inst. nauch. i tekh. inf., 1988, vol. 6.

16. Dogel, V.A., Uchebnik zoologii bespozvonochnykh (Textbook of Invertebrate Zoology), Leningrad: Biomedgiz, 1934.

17. Kosikhina, O.V., Studies in Chaetognatha nutrition, Ekol. Morya, 1982, vol. 11, pp. 79–83.

18. Kuznetsova, N.A., Features of plankton community in the Chukchi sea in august-september, 2017, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2018, vol. 194, pp. 153–166. doi 10.26428/1606-9919-2018-194-153-166

19. Kuznetsova, N.A., Pitaniye i pishchevye otnosheniya nektona v epipelagiali severnoi chasti Okhotskogo morya (Diet and Feeding Interactions of Nekton in the Epipelagic Zone of the Northern Sea of Okhotsk), Vladivostok: TINRO-Tsentr, 2005.

20. Kuznetsova, N.A. and Slabinsky, A.M., Hydrobiological studies in the western Bering and Chukchi seas and the Pacific waters off the Commander Islands in 2007 by the BASIS program, in Byull. no. 2 realizatsii “Kontseptsii dal’nevostochnoi basseinovoi programmy izucheniya tikhookeanskikh lososei” (Bull. No. 2 Implementation “Concept of the Far Eastern Basin Program for the Study of Pacific Salmon”), Vladivostok: TINRO-Tsentr, 2007, pp. 282–293.

21. Lomakina, N.B., Eufauziidy Mirovogo okeana (Euphausiacea) (Euphausiids of the World Ocean (Euphausiacea), Leningrad: Nauka, 1983.

22. Nadtochiy, V.A., Chuchukalo, V.I., and Koblikov, V.N., On the feeding of snow crab (Chionoecetes opilio) in the Anadyr Bay in the Bering Sea, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2001, vol. 128, pp. 432–435.

23. Odintsov, V.S. and Kiyashko, S.I., Variations in the carbon and nitrogen isotope composition of the crabs Chionoecetes opilio (Fabricius, 1788) and Hyas coarctatus Leach, 1816 (Crustacea: Decapoda) from the Chukchi sea, Russ. J. Mar. Biol., 2018, vol. 44, no. 1, pp. 68–74. doi 10.1134/S106307401801008X

24. Orlov, A.М., Benzik, A.N., Vedishcheva, Е.V., Gorbatenko, K.M., Goryanina, S.V., Zubarevich, V.L., Kodryan, K.V., Nosov, М.A., Orlova, S.Yu., Pedchenko, A.P., Rybakov, М.О., and Sokolov, А.М., Preliminary results of fisheries research in the Laptev Sea at RV “Professor Levanidov” in September 2019, Tr. Vses. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2020, vol. 179, pp. 206–225. doi 10.36038/2307-3497-2020-179-206-225

25. Ponomareva, L.A., Weight characteristics of euphausiids in the Sea of Japan, Dokl. Akad. Nauk SSSR, 1954, vol. 99, no. 1, pp. 169–171.

26. Ponomareva, L.A., Diet and distribution of euphausiids in the Sea of Japan, Zool. Zh., 1955, vol. 34, no. 1, pp. 85–97.

27. Raymont, D.E.G., Plankton and productivity in the oceans, vol. 1: Zooplankton, Pergamon press, 1983.

28. Raymont, D.E.G., Plankton and productivity in the oceans, vol. 2: Zooplankton, Pergamon press, 1983.

29. Sirenko, B.I. and Gagaev, S.Y., Unusual abundance of macrobenthos and biological invasions in the Chukchi Sea, Russ. J. Mar. Biol., 2007, vol. 33, no. 6, pp. 355–364. doi 10.1134/S1063074007060016

30. Skarlato, O.A., Dvustvorchatye mollyuski umerennykh vod severo-zapadnoi chasti Tikhogo okeana (Bivalve Mollusks in Temperate Waters of the Northwestern Pacific Ocean), Leningrad: Nauka, 1981. [Opredeliteli po faune SSSR (Keys to the USSR fauna), Zool. Inst. Akad Nauk SSSR, vol. 126]

31. Slabinsky, A.M. and Figurkin, A.L., Structure of planktonic community in the southern part of the Chukchi Sea in summer period, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2014, vol. 178, pp. 135–147. doi 10.26428/1606-9919-2014-178-135-147

32. Slizkin, A.G., Atlas-opredelitel’ krabov i krevetok dal’nevostochnykh morey Rossii (Atlasdeterminant of crabs and shrimps of the Far Eastern seas of Russia), Vladivostok: TINRO-Tsentr, 2010.

33. Sokolova, M.N., Nutrition of deep-sea benthic invertebrate detritivores, Tr. Inst. Okeanol. im. P. P. Shirshova, Akad. Nauk SSSR, 1958, vol. 27, pp. 123–153.

34. Turpaeva, E.P., Nutrition and food groups of marine benthic invertebrates, Tr. Inst. Okeanol. im. P. P. Shirshova, Akad. Nauk SSSR, 1953, vol. 7, pp. 259–299.

35. Issledovaniya Fauny Morei. T. 61(69): Fauna i zoogeografiya bentosa Chukotskogo morya (Explorations of the Fauna of the Seas, vol. 61(69): Fauna and Zoogeography of the Benthos of the Chukchi Sea), Sirenko, B.I. and Vasilenko, S.V., eds, St. Petersburg: Zool. Inst. Ross. Akad. Nauk, 2008.

36. Figurkin, A.L. and Slabinskiy, A.M., Oceanological conditions and plankton in the southern part of the Chukchi Sea in the summer of 1997–2010, Vopr. Promysl. Okeanol., 2012, vol. 1, no. 9, pp. 134–152.

37. Tsikhon-Lukanina, E.A., Trofologiya vodnykh mollyuskov (Trophology of aquatic molluscs), Moscow: Nauka, 1987.

38. Chuchukalo, V.I., Pitanie i pishchevye otnosheniya nektona i nektobentosa v dal’nevostochnykh moryakh (Diet and Feeding Interactions among Nekton and Nektobenthos in the Far Eastern Seas), Vladivostok: TINRO-Tsentr, 2006.

39. Chuchukalo, V.I., Nadtochiy, V.A., and Shebanova, M.A., Distribution and nutrition of the blacktailed chillim in the Olyutorsky Bay in September 2001, Vopr. Rybolov., 2003, vol. 4, no. 1(13), pp. 64–73.

40. Chuchukalo, V.I. and Napazakov, V.V., Feeding and trophology status of some skate species (Rajidae) of the western Bering Sea, Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2002, vol. 130, pp. 422–428.

41. Issledovaniya Fauny Morei. T. 64(72): Ekosistemy i bioresursy Chukotskogo morya i sopredel’nykh akvatoriy (Explorations of the Fauna of the Seas, vol. 64(72): Ecosystems and bioresources of the Chukchi Sea and adjacent waters), Sirenko, B.I., ed., St. Petersburg: Zool. Inst. Ross. Akad. Nauk, 2009.

42. Barton, M.B., Moran, J.R., Vollenweider, J.J., Heintz, R.A., and Boswell, K.M., Latitudinal dependence of body condition, growth rate, and stable isotopes of juvenile capelin (Mallotus villosus) in the Bering and Chukchi Seas, Polar Biol., 2017, vol. 40, no. 7, pp. 1465–1466. doi 10.1007/s00300-016-2041-8

43. Belkin, I.M., Rapid warming of Large Marine Ecosystems, Prog. Oceanogr., 2009, vol. 81, no. 1–4, pp. 207–213. doi 10.1016/j.pocean.2009.04.011

44. Boutillier, J.A. and Nguyen, H., Pandalus hypsinotus Humpback shrimp: A review of the biology and a recommended assessment framework for a directed fishery, Canadian Stock Assessment Secretariat Research Document 99/067, 1999.

45. Cahoon, L.В. and Cooke, J.E., Benthic microalgal production in Onslow Bay, North Carolina, U.S.A., Mar. Ecol. Prog. Ser., 1992, vol. 84, pp. 185–196.

46. Fauchald, K. and Jumars, P.A., The diet of worms: a study of polychaete fiding guilds, Oceanogr. Mar. Biol. Ann. Rev., 1979, vol. 17, pp. 193–284.

47. France, R.L., Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications, Mar. Ecol. Prog. Ser., 1995, vol. 124, pp. 307–312.

48. Grebmeier, J.M., McRoy, C.P., and Feder, H.M., Pelagic-benthic coupling on the shelf of the northern Bering and Chukchi Seas. I. Food supply source and benthic biomass, Mar. Ecol. Prog. Ser., 1988, vol. 48, pp. 57–67.

49. Grebmeier, J.M., Studies of pelagic-benthic coupling extended onto the Soviet continental shelf in the northern Bering and Chukchi Seas, Cont. Shelf Res., 1993, vol. 13, pp. 653‒668.

50. Hill, V. and Cota, G., Spatial patterns of primary production on the shelf, slope and basin of the Western Arctic in 2002, Deep-Sea Res. Part II, 2005, vol. 52, no. 24–26. doi 10.1016/j.dsr2.2005.10.001

51. Hobson, K.A., Fisk, A., Karnovsky, N., Holst, M., Gagnon, J.-M., and Fortier M., A stable isotope (δ13С, δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants, Deep-Sea Res. Part II, 2002, vol. 49, no. 22–23, pp. 5131–5150. doi 10.1016/S0967-0645(02)00182-0

52. Hobson, K.A. and Welch, H.E., Determination of trophic relationship within a high Arctic marine food web using δ13C and δ15N analysis, Mar. Ecol. Prog. Ser., 1992, vol. 84, pp. 9–18. doi 10.3354/meps084009

53. Howell, K.L., Pond, D.W., Billett, D.S.M., and Tyler, P.A., Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty-acid bimarker approach, Mar. Ecol. Prog. Ser., 2003, vol. 255, pp. 193–206. doi 10.3354/meps255193

54. Iken, K., Bluhm, B., and Dunton, K., Benthic food-web structure under differing water mass properties in the southern Chukchi Sea, Deep-Sea Res. Part II, 2010, vol. 57, no. 1–2, pp. 71–85. doi 10.1016/j.dsr2.2009.08.007

55. Iken, K., Bluhm, B.A., and Gradinger, R., Food web structure in the high Arctic Canada Basin: evidence from δ13C and δ15N analysis, Polar Biol., 2005, vol. 28, no 3, pp. 238–249. doi 10.1007/s00300-004-0669-2

56. Jackson, A.L., Inger, R., Parnell, A.C., and Bearhop, S., Comparing isotopic niche widths among and within communities: SIBER — Stable Isotope Bayesian Ellipses in R, J. Animal Ecol., 2011, vol. 80, no. 3, pp. 595–602. doi 10.1111/j.1365-2656.2011.01806.x

57. Lovvorn, J.R., Cooper, L.W., Brooks, M.L., De Ruyck, C.C., Bump, J.K., and Grebmeier, J.M., Organic matter pathways to zooplankton and benthos under pack ice in late winter and open water in later summer in the north-central Bering Sea, Mar. Ecol. Prog. Ser., 2005, vol. 291, pp. 135–150. doi 10.3354/meps291135

58. McTigue, N.D. and Dunton, K.H., Trophodynamics and organic matter assimilation pathways in the northeast Chukchi Sea, Alaska, Deep-Sea Res. Part II, 2014, vol. 102, pp. 84–96. doi 10.1016/j.dsr2.2013.07.016

59. McTigue, N.D. and Dunton, K.H., Trophodynamics of the Hanna Shoal Ecosystem (Chukchi Sea, Alaska): Connecting multiple end-members to a rich food web, Deep-Sea Res. Part II, 2017, vol. 144, pp. 175–189. doi 10.1016/j.dsr2.2017.08.010

60. Melnikov, I.A., Kolosova, E.G., Welch, H.E., and Zhitina, L.S., Sea ice biological communities and nutrient dynamics in the Canadian Basin of the Arctic Ocean, Deep-Sea Res. Part I, 2002, vol. 49, no. 9, pp. 1623–1649. doi 10.1016/S0967-0637(02)00042-0

61. Minagawa, M. and Wada, E., Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age, Geochim. Cosmochim. Acta, 1984, vol. 48, no. 5, pp. 1135–1140. doi 10.1016/0016-7037(84)90204-7

62. Morris, D.J., O’Connell, M.T., and Macko, S.A., Assessing the importance of terrestrial organic carbon in the Chukchi and Beaufort seas, Estuarine, Coastal and Shelf Science, 2015, vol. 164, pp. 28–38. doi 10.1016/j.ecss.2015.06.011

63. Pasquaud, S., Pillet, M., David, V., Sautour, B., and Elie, P., Determination of fish trophic levels in an estuarine system, Estuarine, Coastal and Shelf Science, 2010, vol. 86, no. 2, pp. 237–246. doi 10.1016/j.ecss.2009.11.019

64. Petersen, G.H. and Curtis, M.A., Differences in energy flow through major components of subarctic, temperature and tropical marine shelf ecosystems, Dana, 1980, vol. 1, pp. 53–64.

65. Pinnegar, J.K. and Polunin, N.V.C., Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes, Oecologia, 2000, vol. 122, no. 3, pp. 399–409. doi 10.1007/s004420050046

66. Post, D.M., Using stable isotopes to estimate trophic position: models, methods, and assumptions, Ecology, 2002, vol. 83, no. 3, pp. 703–718. doi 10.2307/3071875

67. Takai, N., Hirose, N., Osawa, T., Hagiwara, K., Kojima, T., Okazaki, Yu., Kuwae, T., Taniuchi, T., and Yoshihara, K., Carbon source and trophic position of pelagic fish in coastal waters of south-eastern Izu Peninsula, Japan, identified by stable isotope analysis, Fish. Sci., 2007, vol. 73, no. 3, pp. 593–608. doi 10.1111/j.1444-2906.2007.01372.x

68. Takai, N., Mishima, Y., Yorozu, A., and Hoshika, A., Carbon sources for demersal fish in the western Seto Inland Sea, Japan, examined by δ13C and δ15N analyses, Limnol. Oceanogr., 2002, vol. 47, no. 3, pp. 730–741. doi 10.4319/lo.2002.47.3.0730

69. Tatara, K., Relation between the primary production and the commercial fishery production in the fishing ground utilization of the primary production by the boat fishery, Bull. Nansei Reg. Fish. Res. Lab., 1981, vol. 13, pp. 111–133 (in Japanese with English abstract).

70. Wolff, W.J., The estuary as a habitat: an analysis of data on the soft-bottom macrofauna of the Estuarine area of the rivers Rhine, Meuse, and Scheldt, Zool. Verh., 1973, no. 126.