DOI QR코드

DOI QR Code

Winter Food Resource Partitioning between Sympatric Gadus macrocephalus and G. chalcogrammus in the Northern Coast of East Sea, South Korea Inferred from Stomach Contents and Stable Isotopes Analyses

위내용물 분석과 안정동위원소 분석을 이용한 겨울철 동해 북부 연안에 출현하는 명태(Gadus chalcogrammus)와 대구(G. macrocephalus)의 먹이분할 연구

  • Park, Joo Myun (Institute of Ocean Science and Technology) ;
  • Jung, Hae Kun (Fisheries Resources and Environment Research Division, East Sea Fisheries Research Institute, National Institute of Fisheries Science) ;
  • Lee, Chung Il (Department of Marine Ecology and Environment, Gangneung-Wonju National University) ;
  • Park, Hyun Je (Department of Marine Ecology and Environment, Gangneung-Wonju National University)
  • 박주면 (한국해양과학기술원 독도전문연구센터) ;
  • 정해근 (국립수산과학원 동해수산연구소 자원환경과) ;
  • 이충일 (강릉원주대학교 해양생태환경학과) ;
  • 박현제 (강릉원주대학교 해양생태환경학과)
  • Received : 2022.04.15
  • Accepted : 2022.05.11
  • Published : 2022.06.30

Abstract

This study investigated dietary habits and intra- and inter-specific food resource partitioning of co-occurring walleye pollock (Gadus chalcogrammus) and Pacific cod (G. macrocephalus) from the waters off the north-eastern coast of South Korea using stomach contents and stable isotopes (δ13C and δ15N) analyses. Both species are mesopelagic carnivores that consumed mainly benthopelagic crustaceans, but teleosts were also abundant in the diet of Pacific cod. Non-metric multidimensional scaling (nMDS) ordination and permutational multivariate analysis of variance (PERMANOVA) of dietary data revealed significant intra- and inter-specific dietary differences, i.e., food resource partitioning. Nitrogen stable isotope values (δ15N) were similar between walleye pollock and Pacific cod, but carbon stable isotope values (δ13C) were significant different, suggesting different trophic positioning. Canonical analysis of principal coordinate (CAP) ordination plot further demonstrated that differences in the type and range of prey ingested by the two species contributed such an inter-specific difference in the diet compositions. Ontogenetic changes in diet compositions were evident. As walleye pollock, they preyed more upon carid shrimps and cephalopods, but no such trend was observed in the diets of Pacific cod. While stable isotope values indicated that large-sized specimens of both species were significantly enriched in 15N relative to smaller conspecifics thus supporting these data. Consequently, in this study, both methodologies, i.e., stomach contents and stable isotope analyses, provided evidence of inter- and/or intra-specific dietary segregations and trophic niche partitioning between co-occurring walleye pollock and Pacific cod off eastern Korean waters.

본 연구는 위내용물 분석과 안정동위원소(δ13C and δ15N) 분석을 통하여 우리나라 동해 북부 연안에 출현하는 명태(Gadus chalcogrammus)와 대구(G. macrocephalus)의 종내 및 종간 먹이자원 분할을 조사하였다. 두 종은 중층성 육식성 어종으로 명태는 저서성 및 중층성 갑각류를 주로 섭식하였고, 대구는 어류를 주로 섭식하였다. 위내용물 분석 결과에 대한 Non-metric multidimensional scaling (nMDS) ordination과 permutational multivariate analysis of variance (PERMANOVA)은 두 종의 종내 및 종간 먹이조성의 차이와 먹이자원 분할을 보여줬다. 안정동위원소 분석 결과 δ15N 값은 종간 유사하였지만, δ13C 값은 대구가 높은 값을 나타내어 두 종간 생태지위 차이를 보여줬다. 명태는 체장 증가에 따라 큰 체장군에서 새우류와 두족류를 더 많이 섭식하는 먹이 전환을 나타냈지만, 대구는 체장군 간 먹이조성이 유사하였다. 안정동위원소 분석에서도 체장군 간 차이를 보였는데, 두 종의 큰 체장군은 작은 체장군에 비해 더 높은 δ15N 값을 나타낸다. 결론적으로 본 연구는 명태와 대구의 위내용물 분석과 안정동위원소 분석을 통하여 종내 및 종간 먹이 차이와 생태지위 분할의 증거를 보여줬다.

Keywords

Acknowledgement

이 논문은 한국연구재단 개인기본연구(NRF-2020R1F1A1051773)와 2022년 국립수산과학원 수산과학연구사업(동해 연안어업 및 환경생태 조사, R2022035)의 지원을 받아 수행되었습니다. 본 연구의 시료 채집과 분석에 도움을 준 강릉원주대학교 수산해양학 연구실 학생들에게 감사드립니다.

References

  1. Adams, C.F., A.I. Pinchuk and K.O. Coyle. 2007. Seasonal changes in the diet composition and prey selection of walleye pollock (Theragra chalcogramma) in the northern Gulf of Alaska. Fish. Res., 84: 378-389. https://doi.org/10.1016/j.fishres.2006.11.032.
  2. Albers, W.D. and P.J. Anderson. 1985. Diet of Pacific cod, Gadus macrocephalus, and predation on the northern pink shrimp, Pandalus borealis, in Pavlof Bay, Alaska. Fish. Bull., 83: 601-610.
  3. Alcaraz, C. and E. Garcia-Berthou. 2007. Food of an endangered cyprinodont (Aphanius iberus): ontogenetic diet shift and prey electivity. Environ. Biol. Fish., 78: 193-207. https://doi.org/10.1007/s10641-006-0018-0.
  4. Anderson, M.J., R.N. Gorley and K.R. Clarke. 2008. PERMANOVA for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth Marine Laboratory, Plymouth, UK, 214pp.
  5. Barnes, L.M., M. Leclerc, C.A. Gray and J.E. Williamson. 2011. Dietary niche differentiation of five sympatric species of Platycephalidae. Environ. Biol. Fish., 90: 429-441. https://doi.org/10.1007/S10641-010-9752-4.
  6. Bearhop, S., C.E. Adams, S. Waldron, R.A. Fuller and H. MacLeod. 2004. Determining trophic niche width: a novel approach using stable isotope analysis. J. Anim. Ecol., 73: 1007-1012. https://doi.org/10.1111/j.0021-8790.2004.00861.x.
  7. Buchheister, A. and R.J. Latour. 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can. J. Fish. Aquat. Sci., 67: 445-461. https://doi.org/10.1139/F09-196.
  8. Cha, H.K., S.I. Lee, S.C. Yoon, Y.S. Kim, Y.Y. Chun, D.S. Chang and J.H. Yang. 2007. Maturation and spawning of the Pacific cod, Gadus macrocephalus TILESIUS in East Sea of Korea. J. Korean Soc. Fish. Ocean Technol., 43: 320-328. https://doi.org/10.3796/KSFT.2007.43.4.320.
  9. Chizinski, C.J., C.G. Huber, M. Longoria and K.L. Pope. 2007. Intra-specific resource partitioning by an opportunistic strategist, inland silverside Menidia beryllina. J. Appl. Ichthyol., 23: 147-151. https://doi.org/10.1111/j.1439-0426.2006.00811.x.
  10. Clarke, K. and R. Gorley. 2015. PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth, UK, 296pp.
  11. Cortes, E. 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmo-branch fishes. Can. J. Fish. Aquat. Sci., 54: 726-738. https://doi.org/10.1139/f96-316.
  12. Cresson, P., S. Ruitton, M. Ourgaud and M. Harmelin-Vivien. 2014. Contrasting perception of fish trophic level from stomach content and stable isotope analyses: a Mediterranean artificial reef experience. J. Exp. Mar. Biol. Ecol., 452: 54-62. https://doi.org/10.1016/j.jembe.2013.11.014.
  13. Duarte, L.O. and C.B. Garcia. 1999. Diet of the mutton snapper Lutja-nus analis (Cuvier) from the gulf of Salamanca, Colombia, Caribbean Sea. Bull. Mar. Sci., 65: 453-465.
  14. Elmqvist, T., C. Folke, M. Nystrom, G. Peterson, J. Bengtsson, B. Walker and J. Norberg. 2003. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ., 1: 488-494. https://doi.org/10.1890/1540-9295(2003)001[0488:RDECAR]2.0.CO;2.
  15. Ferry, L.A. and G.M. Cailliet. 1996. Sample size and data analysis: are wecharacterizing and comparing diet properly? In: MacKinlay, D., K. Shearer (eds.), International congress on the biology of fishes. University of California, San Francisco, California, U.S.A., pp. 71-80.
  16. Froese, R. and D. Pauly. Eds. 2022. FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2022).
  17. Fry, B. 2006. Stable Isotope Ecology. Springer-Verlag, New York, U.S.A., 308pp.
  18. Fry, B. and E.B. Sherr. 1984. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib. Mar. Sci., 27: 13-47.
  19. Gerking, S.D. 1994. Feeding ecology of fish, 1st ed. Academic Press, San Diego, U.S.A., 416pp.
  20. Greenstreet, S.P. and S.I. Rogers. 2006. Indicators of the health of the North Sea fish community: identifying reference levels for an ecosystem approach to management. ICES J. Mar. Sci., 63: 573-593. https://doi.org/10.1016/j.icesjms.2005.12.009.
  21. Hesslein, R.H., M.J. Capel, D.E. Fox and K.A. Hallard. 1991. Stable isotopes of sulfur, carbon, and nitrogen as indicators of trophic level and fish migration in the lower Mackenzie River basin, Canada. Can. J. Fish. Aquat. Sci., 48: 2258-2265. https://doi.org/10.1139/f91-265.
  22. Huh, S.H., J.M. Park and G.W. Baeck. 2016. Diet partitioning between co-occurring Amblychaeturichthys hexanema and Amblychaeturichthys sciistius in the southeastern Korean waters. Korean J. Ichthyol., 28: 79-86.
  23. Huveneers, C., N.M. Otway, S.E. Gibbs and R.G. Harcourt. 2007. Quantitative dietassessment of wobbegong sharks (genus orectolobus) in New South Wales, Australia. ICES J. Mar. Sci., 64: 1272-1281. https://doi.org/10.1093/icesjms/fsm111.
  24. Hyslop, E.J. 1980. Stomach contents analysis - a review of methods and their application. J. Fish Biol., 17: 411-429. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x.
  25. Kim, I.S., Y. Choi, C.L. Lee, Y.J. Lee, B.J. Kim and J.H. Kim. 2005. Illustrated book of Korean fishes. Kyo-hak Publ. Co, Seoul, Korea, 615pp.
  26. Kim, Y.S., K.H. Han, C.B. Kang and J.B. Kim. 2004. Commercial fishes of the coastal and offshore waters in Korea. 2nd ed. Hanguel, Busan, Korea, 333pp.
  27. Knickle, D.C. and G.A. Rose. 2014. Dietary niche partitioning in sympatric gadid species in coastal Newfoundland: evidence from stomachs and CN isotopes. Environ. Biol. Fish., 97: 343-355. https://doi.org/10.1007/s10641-013-0156-0.
  28. Krajewski, J.P., R.M. Bonaldo, C. Sazima and I. Sazima. 2006. Foraging activity and behaviour of two goatfish species (Perciformes: Mullidae) at Fernando de Noronha Archipelago, tropical West Atlantic. Environ. Biol. Fish., 77: 1-8. https://doi.org/10.1007/s10641-006-9046-z.
  29. Ko, A.R., S.J. Lee, J.H. Yang and G.W. Baeck. 2020. Diet of the walleye pollock Gadus chalcogrammus in the East Sea, Korea. Korean J. Fish. Aquat. Sci., 53: 456-463. https://doi.org/10.5657/KFAS.2020.0456.
  30. Kwak, S.N., G.W. Baeck and D.W. Klumpp. 2005. Comparative feeding ecology of two sympatric greenling species, Hexagrammos otakii and Hexagrammos agrammus in eelgrass Zostera marina beds. Environ. Biol. Fish., 74: 129-140. https://doi.org/10.1007/s10641-005-7429-1.
  31. Langton, R.W. 1982. Diet overlap between Atlantic cod, Gadus morhua, silver hake Merluccius bilinearis and fifteen other northwest Atlantic finfish. Fish. Bull., 80: 745-759.
  32. Lee, C.I., M.H. Han, H.K. Jung, H.J. Park and J.M. Park. 2019. Spawning season, and factors influencing allometric growth pattern and body condition of walleye pollock Gadus chalcogrammus in the middle East Sea, Korea. Korean J. Ichthyol., 31: 141-149. https://doi.org/10.35399/ISK.31.3.3.
  33. Lin, H.J., W.Y. Kao and Y.T. Wang. 2007. Analyses of stomach contents and stable isotopes reveal food sources of estuarine detritivorous fish in tropical/subtropical Taiwan. Estuar. Coast. Shelf Sci., 73: 527-537. https://doi.org/10.1016/j.ecss.2007.02.013.
  34. MABIK (Marine Biodiversity Institute of Korea). 2021. 2021 National List of Marine Species, I. Marine Vertebrata. Namu Press, Seocheon, Korea, 138pp.
  35. Marshall, A.D., P.M. Kyne and M.B. Bennett. 2008. Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Muller & Henle and Urolophus kapalensis Yearsley & Last): evidence of ontogenetic shifts and possible resource partitioning. J. Fish Biol., 72: 883-898. https://doi.org/10.1111/j.1095-8649.2007.01762.x.
  36. Micheli, F. and B.S. Halpern. 2005. Low functional redundancy in coastal marine assemblages. Ecol. Lett., 8: 391-400. https://doi.org/10.1111/j.1461-0248.2005.00731.x.
  37. O'Shea, O.R., M. Thums, M. Van Keulen, R.M. Kempster and M.G. Meekan. 2013. Dietary partitioning by five sympatric spe- cies of stingray (Dasyatidae) on coral reefs. J. Fish Biol., 82: 1805-1820. https://doi.org/10.1111/jfb.12104.
  38. Park, J.M., H.K. Jung and C.I. Lee. 2021. Factors influencing dietary changes of walleye pollock, Gadus chalcogrammus, inhabiting the East Sea off the Korean coast. J. Mar. Sci. Eng., 9: 1154. https://doi.org/10.3390/jmse9111154.
  39. Park, J.M. and S.H. Huh. 2018. Ontogenetic and seasonal change in the diets of the glowbelly Acropoma japonicum Gunther 1859 in the south-eastern waters of Korea. Indian J. Fish., 65: 7-14. https://doi.org/10.21077/ijf.2018.65.1.67628-02.
  40. Park, J.M., T.F. Gaston and J.E. Williamson. 2017. Resource partitioning in gurnard species using trophic analyses: the importance of temporal resolution. Fish. Res., 186: 301-310. https://doi.org/10.1016/j.fishres.2016.10.005.
  41. Pinnegar, J.K. and N.V.C. Polunin. 1999. Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct. Ecol., 13: 225-231. https://doi.org/10.1046/j.1365-2435.1999.00301.x.
  42. Platell, M.E. and I.C. Potter. 1999. Partitioning of habitat and prey by abundant and similar-sized species of the Triglidae and Pempherididae (Teleostei) in coastal waters. Estuar. Coast. Shelf Sci., 48: 235-252. https://doi.org/10.1006/ecss.1998.0419.
  43. Platell, M.E. and I.C. Potter. 2001. Partitioning of food resources amongst 18 abundant benthic carnivorous fish species in marine waters on the lower west coast of Australia. J. Exp. Mar. Biol. Ecol., 261: 31-54. https://doi.org/10.1016/S0022-0981(01)00257-X.
  44. Qiao, J., J. Hu, Q. Xia, R. Zhu, K. Chen, J. Zhao, Y. Yan, L. Chu and D. He. 2020. Pelagic-benthic resource polymorphism in Schizopygopsis thermalis Herzenstein 1891 (Pisces, Cyprinidae) in a headwater lake in the Salween River system on the Tibetan Plateau. Ecology and evolution, 10(14): 7431-7444. https://doi.org/10.1002/ece3.6470.
  45. Ross, S.T. 1986. Resource partitioning in fish assemblages: a review of field studies. Copeia, 1986: 352-388. https://doi.org/10.2307/1444996.
  46. Smith, J.A., L.J. Baumgartner, I.M. Suthers and M.D. Taylor. 2011. Generalist niche, specialist strategy: the diet of an Australian percichthyid. J. Fish Biol., 78: 1183-1199. https://doi.org/10.1111/j.1095-8649.2011.02926.x.
  47. Stergiou, K.I. and V.S. Karpouzi. 2002. Feeding habits and trophic levels of Mediterranean fish. Rev. Fish Biol. Fish., 11: 217-254. https://doi.org/10.1023/A:1020556722822.
  48. Urban, D. 2012. Food habits of Pacific cod and walleye pollock in the northern Gulf of Alaska. Mar. Ecol. Prog. Ser., 469: 215-222. https://doi.org/10.3354/meps10135.
  49. White, W.T., M.E. Platell and I.C. Potter. 2004. Comparisons between the diets of four abundant species of elasmobranchs in a sub- tropical embayment: implications for resource partitioning. Mar. Biol., 144: 439-448. https://doi.org/10.1007/s00227-003-1218-1.
  50. Yamamura, O., S. Honda, O. Shida and T. Hamatsu. 2002. Diets of walleye pollock Theragra chalcogramma in the Doto area, northern Japan: ontogenetic and seasonal variations. Mar. Ecol. Prog. Ser., 238: 187-198. https://doi.org/10.3354/meps238187.
  51. Yoon, S.C., J.H. Yang, J.H. Park, Y.M. Choi, J.H. Park and D.W. Lee. 2012. Feeding habits of the Pacific cod Gadus macrocephalus in the coastal waters off Jumunjin, Gangwondo of Korea. Korean J. Fish. Aquat. Sci., 45: 379-386. https://doi.org/10.5657/KFAS.2012.0379.