Skip to main content
Log in

Partitioning of food resources among three sympatric scorpionfish (Scorpaeniformes) in coastal waters of the northern Yellow Sea

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The partitioning of food resources among three abundant co-occurring reef-associated scorpionfish, Hexagrammos agrammus, Hexagrammos otakii and Sebastes schlegelii, was determined on an artificial reef zone in nearshore and offshore coastal waters of northern China, using stomach content and stable isotope analyses (δ13C and δ15N). The three species consumed similar prey items, mainly a variety of crustaceans, teleosts, polychaetes and macroalgae, but the proportions of the items differed among species. The dietary composition of all three scorpionfish differed significantly in nearshore waters, but not between H. otakii and S. schlegelii in offshore waters, where both species fed predominantly on carideans, penaeids and brachyurans. The δ13C values varied significantly among the three scorpionfish in nearshore waters, and tended towards significance (P = 0.053) between H. otakii and S. schlegelii in offshore waters, suggesting that they partition food resources. Bayesian mixing models further confirmed that all scorpionfish were generalist carnivorous and that the main food sources were assimilated in different proportions. In the nearshore waters, resource partitioning occurs among the three scorpionfish, reducing the potential for competition and the feeding ecology implies that they have dietary plasticity, which facilitates their coexistence and maintains local benthic fish community stability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alfaro, A. C., F. Thomas, L. Sergent & M. Duxbury, 2006. Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuarine, Coastal and Shelf Science 70: 271–286.

    Article  Google Scholar 

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth.

    Google Scholar 

  • Balanov, A. A., A. I. Markevich, D. V. Antonenko & K. D. Crow, 2001. The first occurrence of hybrids of Hexagrammos otakii × H. octogrammus and description of H. otakii (Hexagrammidae) from Peter the Great Bay (the Sea of Japan). Journal of Ichthyology 41: 728–738.

    Google Scholar 

  • Buchheister, A. & R. J. Latour, 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Canadian Journal of Fisheries and Aquatic Sciences 67: 445–461.

    Article  CAS  Google Scholar 

  • Cai, D., F. Meng, Y. Han & S. Gao, 1999. Studies on 13C/12C ratios as a tracer for food web in a marine ecosystem-the trophic relations in pelagic food webs in Laoshan Bay. Oceanologia Et Limnologia Sinica 30: 671–678.

    Google Scholar 

  • Chin, B.S., M. Nakagawa, T. Noda, T. Wada & Y. Yamashita, 2013. Determining optimal release habitat for black rockfish, Sebastes schlegelii: examining growth rate, feeding condition, and return rate. Reviews in Fisheries Science 21: 286–298.

    Article  Google Scholar 

  • Clark, S. & A. Edwards, 1999. An evaluation of artificial reef structures as tools for marine habitat rehabilitation in the Maldives. Aquatic Conservation 9: 5–21.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2015. PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth.

    Google Scholar 

  • Clarke, K. R., R. N. Gorley, P. J. Somerfield & R. M. Warwick, 2014a. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 3rd ed. PRIMER-E Ltd, Plymouth.

    Google Scholar 

  • Clarke, K. R., J. R. Tweedley & F. J. Valesini, 2014b. Simple shade plots aid better long-term choices of data pre-treatment in multivariate assemblage studies. Journal of the Marine Biological Association of the United Kingdom 94: 1–16.

    Article  Google Scholar 

  • Costanzo, S. D., M. J. O’Donohue, W. C. Dennison, N. R. Loneragan & M. Thomas, 2001. A new approach for detecting and mapping sewage impacts. Marine Pollution Bulletin 42: 149–156.

    Article  CAS  Google Scholar 

  • Coulson, P.G., M. E. Platell, K. R. Clarke & I. C. Potter, 2015. Dietary variations within a family of ambush predators (Platycephalidae) occupying different habitats and environments in the same geographical region. Journal of Fish Biology 86: 1046–1077.

    Article  CAS  Google Scholar 

  • Cresson, P., S. Ruitton & M. Harmelin-Vivien, 2014a. Artificial reefs do increase secondary biomass production: mechanisms evidenced by stable isotopes. Marine Ecology Progress Series 509: 15–26.

    Article  Google Scholar 

  • Cresson, P., S. Ruitton, M. Ourgaud & M. Harmelin-Vivien, 2014b. Contrasting perception of fish trophic level from stomach content and stable isotope analyses: a Mediterranean artificial reef experience. Journal of Experimental Marine Biology and Ecology 452: 54–62.

    Article  Google Scholar 

  • Dromard, C. R., Y. Bouchon-Navaro, S. Cordonnier, M. F. Fontaine, M. Verlaque, M. Harmelin-Vivien & C. Bouchon, 2013. Resource use of two damselfishes, Stegastes planifrons and Stegastes adustus, on Guadeloupean reefs (Lesser Antilles): inference from stomach content and stable isotope analysis. Journal of Experimental Marine Biology and Ecology 440: 116–125.

    Article  Google Scholar 

  • Franca, S., R. P. Vasconcelos, S. Tanner, C. Maguas, M. J. Costa & H. N. Cabral, 2011. Assessing food web dynamics and relative importance of organic matter sources for fish species in two Portuguese estuaries: a stable isotope approach. Marine Environmental Research 72: 204–215.

    Article  CAS  Google Scholar 

  • Froese, R. & D. Pauly, 2014. Fishbase. World Wide Web electronic publication, version (08/2014). www.fishbase.org.

  • Fry, B., 1988. Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnology and Oceanography 33: 1182–1190.

    Article  CAS  Google Scholar 

  • García-Charton, J. A., Á. Pérez-Ruzafa, P. Sánchez-Jerez, J. T. Bayle-Sempere, O. Reñones & D. Moreno, 2004. Multi-scale spatial heterogeneity, habitat structure, and the effect of marine reserves on Western Mediterranean rocky reef fish assemblages. Marine Biology 144: 161–182.

    Article  Google Scholar 

  • Green, K.M., A.P. Greenley & R.M. Starr, 2014. Movements of Blue rockfish (Sebastes mystinus) off Central California with comparisons to similar species. PLoS One 9: e98976.

    Article  Google Scholar 

  • Guelinckx, J., J. Maes, P. Van Den Driessche, B. Geysen, F. Dehairs & F. Ollevier, 2007. Changes in δ13C and δ15N in different tissues of juvenile sand goby Pomatoschistus minutus: a laboratory diet-switch experiment. Marine Ecology Progress Series 341: 205–215.

    Article  CAS  Google Scholar 

  • Heaton, T.H.E., 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chemical Geology 59: 87–102.

    Article  CAS  Google Scholar 

  • Helfman, G., 1978. Patterns of community structure in fishes: summary and overview. Environmental Biology of Fishes 3: 129–148.

    Article  Google Scholar 

  • Hobson, K. A., W. G. Ambrose & P. E. Renaud, 1995. Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13Cand δ15N analysis. Marine Ecology Progress Series 128: 1–10.

    Article  Google Scholar 

  • Hoshika, A., M. J. Sarker, S. Ishida, Y. Mishima & N. Takai, 2006. Food web analysis of an eelgrass (Zostera marina L.) meadow and neighbouring sites in Mitsukuchi Bay (Seto Inland Sea, Japan) using carbon and nitrogen stable isotope ratios. Aquatic Botany 85: 191–197.

    Article  CAS  Google Scholar 

  • Jacob, U., K. Mintenbeck, T. Brey, R. Knust & K. Beyer, 2005. Stable isotope food web studies: a case for standardized sample treatment. Marine Ecology Progress Series 287: 251–253.

    Article  Google Scholar 

  • Ji, D., X. Bian, N. Song & T. Gao, 2015. Feeding ecology of Hexagrammos agrammus in Lidao Rongcheng, China. Journal of Fishery Sciences of China 22: 88–98. (in Chinese).

    CAS  Google Scholar 

  • Jiang, R., S. Zhang, K. Wang, X. Zhou & J. Zhao, 2014. Stable isotope analysis of the offshore food web of Gouqi Island. Chinese Journal of Ecology 33: 930–938. (in Chinese).

    Google Scholar 

  • Jorgensen, S.J., D.M. Kaplan, A.P. Klimley, S.G. Morgan, M.R. O'Farrell & L.W. Botsford, 2006. Limited movement in blue rockfish Sebastes mystinus: internal structure of home range. Marine Ecology Progress Series 327: 157–170.

    Article  Google Scholar 

  • Kanamoto, Z., 1979. On the ecology of Hexagrammid fish V: food items of Agrammus agrammus (Temminck et Schlegel) and Hexagrammos otakii Jordan et Starks sampled from different habitats around a small reef. Japanese Journal of Ecology 29: 265–271. (in Japanese).

    Google Scholar 

  • Kang, C. K., E. J. Choy, Y. Son, J. Y. Lee, J. K. Kim, Y. Kim & K. S. Lee, 2008. Food web structure of a restored macroalgal bed in the eastern Korean peninsula determined by C and N stable isotope analyses. Marine Biology 153: 1181–1198.

    Article  Google Scholar 

  • Kikuchi, T., 1966. An ecological study on animal communities of the Zostera marina belt in Tomioka Bay, Amakusa, Kyushu. Publications from the Amakusa Marine Biological Laboratory 1: 1–106.

    Google Scholar 

  • Kiyashko, S. I., T. A. Velivetskaya & A. V. Ignatiev, 2011. Sulfur, carbon, and nitrogen stable isotope ratios in soft tissues and trophic relationships of fish from the near-shore waters of the peter the great bay in the Sea of Japan. Russian Journal of Marine Biology 37: 297–302.

    Article  CAS  Google Scholar 

  • Kolpakov, N., E. Barabanshchikov & Y. D. Valuev, 2005. First findings of the fat greenling Hexagrammos otakii (Hexagrammidae) in waters off northern primorye. Journal of Ichthyology 45: 682–684.

    Google Scholar 

  • Kusakari, M., 1991. Mariculture of kurosoi, Sebastes schlegeli. Environmental Biology of Fishes 30: 245–251.

    Article  Google Scholar 

  • Kwak, S., G. Baeck & D. Klumpp, 2005. Comparative feeding ecology of two sympatric greenling species, Hexagrammos otakii and Hexagrammos agrammus in eelgrass Zostera marina beds. Environmental Biology of Fishes 74: 129–140.

    Article  Google Scholar 

  • Lebreton, B., P. Richard, R. Galois, G. Radenac, A. Brahmia, G. Colli, M. Grouazel, C. André, G. Guillou & G. F. Blanchard, 2012. Food sources used by sediment meiofauna in an intertidal Zostera noltii seagrass bed: a seasonal stable isotope study. Marine Biology 159: 1537–1550.

    Article  Google Scholar 

  • Lei, J., 2005. Marine fish culture theory and techniques. China Agriculture Press, Beijing.

    Google Scholar 

  • Lek, E., D. V. Fairclough, M. E. Platell, K. R. Clarke, J. R. Tweedley & I. C. Potter, 2011. To what extent are the dietary compositions of three abundant, co-occurring labrid species different and related to latitude, habitat, body size and season? Journal of Fish Biology 78: 1913–1943.

    Article  CAS  Google Scholar 

  • Lepoint, G., P. Dauby & S. Gobert, 2004. Applications of C and N stable isotopes to ecological and environmental studies in seagrass ecosystems. Marine Pollution Bulletin 49: 887–891.

    Article  CAS  Google Scholar 

  • Letourneur, Y., T. Lison de Loma, P. Richard, M. L. Harmelin-Vivien, P. Cresson, D. Banaru, M. F. Fontaine, T. Gref & S. Planes, 2013. Identifying carbon sources and trophic position of coral reef fishes using diet and stable isotope (δ15N and δ13C) analyses in two contrasted bays in Moorea, French Polynesia. Coral Reefs 32: 1091–1102.

    Article  Google Scholar 

  • Lin, D. T. & P. Fong, 2008. Macroalgal bioindicators (growth, tissue N, δ15N) detect nutrient enrichment from shrimp farm effluent entering Opunohu Bay, Moorea, French Polynesia. Marine Pollution Bulletin 56: 245–249.

    Article  CAS  Google Scholar 

  • Linke, T., M. Platell & I. Potter, 2001. Factors influencing the partitioning of food resources among six fish species in a large embayment with juxtaposing bare sand and seagrass habitats. Journal of Experimental Marine Biology and Ecology 266: 193–217.

    Article  Google Scholar 

  • Lorrain, A., Y. M. Paulet, L. Chauvaud, N. Savoye, A. Donval & C. Saout, 2002. Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology. Journal of Experimental Marine Biology and Ecology 275: 47–61.

    Article  CAS  Google Scholar 

  • Love, M.S., M. Yoklavich & L.K. Thorsteinson, 2002. The rockfishes of the northeast Pacific. University of California Press, Berkeley.

    Google Scholar 

  • Mablouké, C., J. Kolasinski, M. Potier, A. Cuvillier, G. Potin, L. Bigot, P. Frouin & S. Jaquemet, 2013. Feeding habits and food partitioning between three commercial fish associated with artificial reefs in a tropical coastal environment. African Journal of Marine Science 35: 323–334.

    Article  Google Scholar 

  • MacNeil, M. A., K. G. Drouillard & A. T. Fisk, 2006. Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Canadian Journal of Fisheries and Aquatic Sciences 63: 345–353.

    Article  CAS  Google Scholar 

  • Matley, J. K., A. T. Fisk, A. J. Tobin, M. R. Heupel & C. A. Simpfendorfer, 2016. Diet-tissue discrimination factors and turnover of carbon and nitrogen stable isotopes in tissues of an adult predatory coral reef fish, Plectropomus leopardus. Rapid Communications in Mass Spectrometry 30: 29–44.

    Article  CAS  Google Scholar 

  • Matyushin, V.M. & P.A. Fedotov, 1993. Feeding of masked greenling in a Zostera community in Vityaz Bay of the Sea of Japan. Russian Journal of Marine Biology 18: 33–37.

    Google Scholar 

  • Michener, R. & K. Lajtha, 2008. Stable isotopes in Ecology and Environmental Science. Blackwell Publishing, Oxford.

    Google Scholar 

  • Minagawa, M. & E. Wada, 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140.

    Article  CAS  Google Scholar 

  • Nagasawa, T., 2001. Early life history of rockfishes (genus Sebastes) in the Sea of Japan. Bulletin of the Japan Sea National Fisheries Research Institute. (in Japanese).

  • Nagasawa, T. & K. Domon, 1997. The early life history of kurosoi, Sebastes schlegeli (Scorpaenidae), in the Sea of Japan. Ichthyological Research 44: 237–248.

    Article  Google Scholar 

  • Nelson, J., J. Chanton, F. Coleman & C. Koenig, 2011. Patterns of stable carbon isotope turnover in gag, Mycteroperca microlepis, an economically important marine piscivore determined with a non-lethal surgical biopsy procedure. Environmental Biology of Fishes 90: 243–252.

    Article  Google Scholar 

  • Newsome, S. D., C. M. del Rio, S. Bearhop & D. L. Phillips, 2007. A niche for isotopic ecology. Frontiers in Ecology and the Environment 5: 429–436.

    Article  Google Scholar 

  • Parnell, A. C., R. Inger, S. Bearhop & A. L. Jackson, 2010. Source partitioning using stable isotopes: coping with too much variation. PloS One 5: e9672.

    Article  Google Scholar 

  • Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.

    Article  Google Scholar 

  • Pianka, E. R., 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4: 53–74.

    Article  Google Scholar 

  • Platell, M.E. & 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. Journal of Experimental Marine Biology and Ecology 261: 31–54.

    Article  Google Scholar 

  • Quan, W., L. Shi & Y. Chen, 2010. Stable isotopes in aquatic food web of an artificial lagoon in the Hangzhou Bay, China. Chinese Journal of Oceanology and Limnology 28: 489–497.

    Article  CAS  Google Scholar 

  • Ross, S. T., 1986. Resource partitioning in fish assemblages: a review of field studies. Copeia 1986: 352–388.

    Article  Google Scholar 

  • Santos, M. N. & C. C. Monteiro, 2007. A fourteen-year overview of the fish assemblages and yield of the two oldest Algarve artificial reefs (southern Portugal). Hydrobiologia 580: 225–231.

    Article  Google Scholar 

  • Schoener, T. W., 1974. Resource partitioning in ecological communities. Science 185: 27–39.

    Article  CAS  Google Scholar 

  • Schoener, T. W., 1983. Field experiments on interspecific competition. American Naturalist 122: 240–285.

    Article  Google Scholar 

  • Seo, I. S. & J. S. Hong, 2007. Comparative feeding ecology of sympatric greenling Hexagrammos otakii and Schlegel’s black rockfish Sebastes schlegeli in the Jnngbong Tidal Flat, Incheon, Korea. Korean Journal of Fisheries and Aquatic Sciences 40: 84–94. (in Korean).

    Article  Google Scholar 

  • Tong, Y. & X. Guo, 2009. Feeding competition between two rockfish Sebastes schlegeli and Hexagrammos otakii. Journal of Fishery Sciences of China 16: 541–549. (in Chinese).

    Google Scholar 

  • Tu, Z., X. Zhang, P. Zhang & T. Gao, 2007. Artificial fish reef near Lidao Island in Rongcheng—early assessment on resource and environment in sea area for artificial fish reef. Marine Fisheries Information 22: 1–7. (in Chinese).

    CAS  Google Scholar 

  • Wang, K., S. Zhang, Z. Wang, J. Zhao, M. Xu & J. Xu, 2012. Dietary composition and food competition of six main fish species in rocky reef habitat off Gouqi Island. Chinese Journal of Applied Ecology 23: 536–544. (in Chinese).

    PubMed  Google Scholar 

  • Wu, Z., L. Zhang, X. Zhang, P. Zhang & W. Li, 2012. Nekton community structure and its relationship with the main environmental variables in Lidao artificial reef zones of Rongcheng. Acta Ecologica Sinica 32: 6737–6746. (in Chinese).

    Article  Google Scholar 

  • Wu, Z., X. Zhang, H. M. Lozano & N. R. Loneragan, 2016. Trophic flows, kelp culture and fisheries in the marine ecosystem of an artificial reef zone in the Yellow Sea. Estuarine, Coastal and Shelf Science 182: 86–97.

    Article  CAS  Google Scholar 

  • Ye, Q., 1992. Feeding habits of Greenling from coastal waters off Qingdao. Transactions of Oceanology and Limnology 4: 50–55. (in Chinese).

    Google Scholar 

  • Yoon, C. H., 2002. Fishes of Korea with Pictorial Key and Systematic List. Academy Publishing Company, Seoul.

    Google Scholar 

  • Zhang, X., X. Wang, Z. Tu, P. Zhang, Y. Wang, T. Wang & X. Wang, 2009. Current status and prospect of fisheries resource enhancement in Shandong Province. China Fisheries Economics 2: 51–58. (in Chinese).

    Google Scholar 

  • Zhang, B., Z. Li & X. Jin, 2014. Food composition and prey selectivity of Sebastes schlegeli. Journal of Fishery Sciences of China 21: 134–141. (in Chinese).

    Google Scholar 

  • Zhang, Y., Q. Xu, J. Alós, H. Liu, Q. Xu & H. Yang, 2015. Short-term fidelity, habitat use and vertical movement behavior of the black rockfish Sebastes schlegelii as determined by acoustic telemetry. PloS One 10: e0134381.

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the support of research grant provided by funds from the national program on key basic research project (973 Program) (2015CB453302) and the public science and technology research funds projects of ocean of China (201405010). We also thank Xiaoqi Zeng, Ying Xue and Dongyan Han for the generous and invaluable guidance in the identification of taxa in the stomach contents. We gratefully appreciate the advice and technique assistance provided by Xingliang He and Lilei Chen from Qingdao Institute of Marine Geology. Members from the lab of marine stock enhancement and conservation, Ocean University of China, are thanked for their help during the fieldwork. The China Scholarship Council provided financial support for ZW to study at Murdoch University to develop this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiumei Zhang.

Additional information

Handling editor: David J. Hoeinghaus

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 72 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Z., Zhang, X., Dromard, C.R. et al. Partitioning of food resources among three sympatric scorpionfish (Scorpaeniformes) in coastal waters of the northern Yellow Sea. Hydrobiologia 826, 331–351 (2019). https://doi.org/10.1007/s10750-018-3747-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3747-0

Keywords

Navigation