, Volume 794, Issue 1, pp 317–332 | Cite as

Influence of environmental factors and individual traits on the diet of non-native hybrid bigheaded carp (Hypophthalmichthys molitrix × H. nobilis) in Lake Balaton, Hungary

  • Attila MozsárEmail author
  • András Specziár
  • Izabella Battonyai
  • Gábor Borics
  • Judit Görgényi
  • Hajnalka Horváth
  • Mátyás Présing
  • László G.-Tóth
  • Zoltán Vitál
  • Gergely Boros
Primary Research Paper


Planktivorous silver carp and bighead carp (collectively, the bigheaded carps) have been stocked worldwide and their invasion has caused severe impacts on many freshwater ecosystems. Exploiting the chance provided by the specific hybrid bigheaded carp stock in Lake Balaton (Hungary) covering the entire morphological range between the two species (including gill raker morphology), we implemented a comprehensive study (1) to reveal the feeding habits of hybrid bigheaded carps living in a mesotrophic, lacustrine habitat and (2) to assess how biotic and abiotic environmental factors and gill raker morphology affect diet composition. We found that all bigheaded carps utilized primarily zooplankton and neglected the scarce and inefficiently digestible phytoplankton, irrespective of gill raker morphology. Moreover, we observed strikingly high levels of inorganic debris consumption, but the proportion of inorganic matter in the guts was not associated directly with the concentration of suspended inorganic particles. Variance in the diet composition of bigheaded carps was related mostly to environmental factors, including the wind-induced resuspension of inorganic particles and seasonally variable availability of food resources. In conclusion, the effects of abiotic environmental factors and available food resources could overwhelm the effect of gill raker morphology in shaping the feeding habits of bigheaded carps.


Asian carp Filter-feeding Hybrid fishes Introduced fish species Planktivory Zooplankton 



This study was supported by GINOP—2.3.2-15-2016-00004 and OTKA K-83893 projects. We thank I. Mecsnóbel and Z. Poller for their skilful assistance in the laboratory. We also acknowledge the useful comments of J. Syväranta and the helpful contribution of L. Antal to the figure preparation. Bigheaded carps for this study were provided by the Balaton Fish Management Non-Profit Ltd.


  1. Aminot, A. & F. Rey, 2000. Standard Procedure for the Determination of Chlorophyll-a by Spectroscopic Methods. International Council for the Exploration of Sea, Copenhagen: 1–11.Google Scholar
  2. Amundsen, P. A., H. M. Gabler & F. J. Staldvik, 1996. A new approach to graphical analysis of feeding strategy from stomach contents data: modification of the Costello (1990) method. Journal of Fish Biology 48: 607–614.Google Scholar
  3. Baranyai, E. & L. G.-Tóth, 2010. The influence of turbulence on vertical distribution of zooplankton in shallow, kinetic Lake Balaton (Hungary). Verhandlungen der Internationale Vereinigung für Theoretische und Angewandte Limnologie 30: 1505–1508.Google Scholar
  4. Baranyai, E., L. G.-Tóth, Á. Vári & Z. G. Homonnay, 2011. The effect of variable turbulent intensities on the distribution of zooplankton in the shallow, large Lake Balaton (Hungary). Knowledge and Management of Aquatic Ecosystems 400: article No. 07.Google Scholar
  5. Battonyai, I., A. Specziár, Z. Vitál, A. Mozsár, J. Görgényi, G. Borics, L. G.-Tóth & G. Boros, 2015. Relationship between gill raker morphology and feeding habits of hybrid bigheaded carps (Hypophthalmichthys spp.). Knowledge and Management in Aquatic Ecosystems 416: article No. 36.Google Scholar
  6. Bitterlich, G., 1985. Digestive enzyme pattern of two stomachless filter feeders, silver carp, Hypophthalmichthys molitrix Val., and bighead carp, Aristichthys nobilis Rich. Journal of Fish Biology 27: 103–112.CrossRefGoogle Scholar
  7. Borics, G., I. Grigorszky, S. Szabó & J. Padisák, 2000. Phytoplankton associations under changing pattern of bottom-up vs. top-down control in a small hypertrophic fishpond in East Hungary. Hydrobiologia 424: 79–90.CrossRefGoogle Scholar
  8. Boros, G., 2015. A Balatoni busaállomány kutatásának előzményei és fontosabb eredményei a 2010–2015 közötti időszakban. Scientific report of Balaton Limnological Institute (CER, HAS) for The Ministry of Agriculture (in Hungarian).Google Scholar
  9. Boros, G., A. Mozsár, Z. Vitál, S. A. Nagy & A. Specziár, 2014. Growth and condition factor of hybrid (Bighead Hypophthalmichthys nobilis Richardson, 1845× silver carp H. molitrix Valenciennes, 1844) Asian carps in the shallow, oligo-mesotrophic Lake Balaton. Journal of Applied Ichthyology 30: 546–548.CrossRefGoogle Scholar
  10. Britton, J. R., G. D. Davies & C. Harrod, 2010. Trophic interactions and consequent impacts of the invasive fish Pseudorasbora parva in a native aquatic foodweb: a field investigation in the UK. Biological Invasions 12: 1533–1542.CrossRefGoogle Scholar
  11. Calkins, H. A., S. J. Tripp & J. E. Garvey, 2012. Linking silver carp habitat selection to flow and phytoplankton in the Mississippi River. Biological Invasions 14: 949–958.CrossRefGoogle Scholar
  12. Callan, W. T. & S. L. Sanderson, 2002. Feeding mechanisms in carp: cross filtration, palatal protrusion and flow reversals. The Journal of Experimental Biology 206: 883–892.CrossRefGoogle Scholar
  13. Chen, G., Z. Wu, B. Gu, D. Liu, X. Li & Y. Wang, 2011. Isotopic niche overlap of two planktivorous fish in southern China. Limnology 12: 151–155.CrossRefGoogle Scholar
  14. Cooke, S. L., W. R. Hill & K. P. Meyer, 2009. Feeding at different plankton densities alters invasive bighead carp (Hypophthalmichthys nobilis) growth and zooplankton species composition. Hydrobiologia 625: 185–193.CrossRefGoogle Scholar
  15. Costello, M. J., 1990. Predator feeding strategy and prey importance: a new graphical analysis. Journal of Fish Biology 36: 261–263.CrossRefGoogle Scholar
  16. Cremer, M. C. & R. O. Smitherman, 1980. Food habits and growth of silver and bighead carp in cages and ponds. Aquaculture 20: 57–64.CrossRefGoogle Scholar
  17. Cushman, S. A. & K. McGarigal, 2002. Hierarchical, multi-scale decomposition of species-environment relationships. Landscape Ecology 17: 637–646.CrossRefGoogle Scholar
  18. Domaizon, I. & J. Dévaux, 1999. Impact of moderate silver carp biomass gradient on zooplankton communities in a eutrophic reservoir. Consequences for the use of silver carp in biomanipulation. Comptes Rendus de l’Académie des Sciences Paris, Life Sciences 322: 621–628.Google Scholar
  19. Dong, S. & D. Li, 1994. Comparative studies on the feeding selectivity of silver carp Hypophthalmichthys molitrix and bighead carp Aristichthys nobilis. Journal of Fish Biology 44: 621–626.CrossRefGoogle Scholar
  20. Dumont, H. J., I. Van de Velde & S. Dumont, 1975. The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19: 75–97.CrossRefPubMedGoogle Scholar
  21. Finger, T. E., 2008. Sorting food from stones: the vagal taste system in Goldfish. Carassius auratus Journal of Comparative Physiology A 194: 135–143.CrossRefGoogle Scholar
  22. Fukushima, M., N. Takamura, L. Sun, M. Nakagawa, K. Matsushige & P. Xie, 1999. Changes in the plankton community following introduction of filter-feeding planktivorous fish. Freshwater Biology 42: 719–735.CrossRefGoogle Scholar
  23. Gerking, S. D., 1994. Feeding Ecology of Fish. Academic Press, San Diego.Google Scholar
  24. Gophen, M., 2014. Competitive consumption of the Lake Kinneret (Israel) plankton by Hypophthalmichthys molitrix and Sarotherodon galilaeus. Open Journal of Ecology 4: 532–542.CrossRefGoogle Scholar
  25. Görgényi, J., G. Boros, Z. Vitál, A. Mozsár, G. Várbíró, G. Vasas & G. Borics, 2016. The role of filter feeding Asian carps in algal dispersion. Hydrobiologia 764: 115–126.CrossRefGoogle Scholar
  26. Goździejewska, A., E. Paturej & A. Krajewska-Sołtys, 2006. Effect of environmental factors on the occurrence of the Harpacticoida in the zooplankton and in the diet of smelt Osmerus eperlanus (L.) in the Vistula Lagoon. Electronic Journal of Polish Agricultural Universities 9: article No. 16.Google Scholar
  27. G.-Tóth, L., K. V. Balogh & N. Zánkai, 1986. Significance and degree of abioseston consumption in the filter-feeder Daphnia galeata Sars am. Richard (Cladocera) in Lake Balaton. Archiv für Hydrobiologie 106: 45–60.Google Scholar
  28. G.-Tóth, L., L. Parpala, C. Balogh, I. Tátrai & E. Baranyai, 2011. Zooplankton community response to enhanced turbulence generated by water-level decrease in Lake Balaton, the largest shallow lake in Central Europe. Limnology and Oceanography 56: 2211–2222.CrossRefGoogle Scholar
  29. Gu, B. & C. L. Schelske, 1996. Temporal and spatial variations in phytoplankton carbon isotopes in a polymictic subtropical lake. Journal of Plankton Research 18: 2081–2092.CrossRefGoogle Scholar
  30. Hampl, A., J. Jirásek & D. Sirotek, 1983. Growth morphology of the filtering apparatus of silver carp (Hypophthalmichthys molitrix Val.) - II. microscopic anatomy. Aquaculture 31: 153–158.CrossRefGoogle Scholar
  31. Hayer, C.-A., J. J. Breeggemann, R. A. Klumb, B. D. S. Graeb & K. N. Bertrand, 2014a. Population characteristics of bighead and silver carp on the northwestern front of their North American invasion. Aquatic Invasions 9: 289–303.CrossRefGoogle Scholar
  32. Hayer, C.-A., B. D. S. Graeb & K. N. Bertrand, 2014b. Adult, juvenile and young-of-year bighead, Hypophthalmichthys nobilis (Richardson, 1845) and silver carp, H. molitrix (Valenciennes, 1844) range expansion on the northwestern front of the invasion in North America. BioInvasions Records 3: 283–289.CrossRefGoogle Scholar
  33. Herodek, S., L. Laczkó & Á. Virág, 1988. Lake Balaton: Research and Management. Nexus, Budapest.Google Scholar
  34. Herodek, S., I. Tátrai, J. Oláh & L. Vörös, 1989. Feeding experiments with silver carp (Hypophthalmichthys molitrix Val.) fry. Aquaculture 83: 331–344.CrossRefGoogle Scholar
  35. Hillebrand, H., C. D. Dürselen, D. Kirchtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.CrossRefGoogle Scholar
  36. Irons, K. S., G. G. Sass, M. A. McClelland & M. A. Stafford, 2007. Reduced condition factor of two native fish species coincident with invasion of nonnative Asian carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? Journal of Fish Biology 71: 258–273.CrossRefGoogle Scholar
  37. Istvánovics, V., A. Clement, L. Somlyódy, A. Specziár, L. G.-Tóth & J. Padisák, 2007. Updating water quality targets for shallow Lake Balaton (Hungary), recovering from eutrophication. Hydrobiologia 581: 305–318.CrossRefGoogle Scholar
  38. Jayasinghe, U. A. D., E. García-Berthou, Z. Li, W. Li, T. Zhang & J. Liu, 2015. Co-occurring bighead and silver carps show similar food preference but different isotopic niche overlap in different lakes. Environmental Biology of Fishes 98: 1185–1199.CrossRefGoogle Scholar
  39. Ke, Z., P. Xie & L. Guo, 2008. In situ study on effect of food competition on diet shifts and growth of silver and bighead carps in large biomanipulation fish pens in Meiliang Bay, Lake Taihu. Journal of Applied Ichthyology 24: 263–268.CrossRefGoogle Scholar
  40. Khan, M. F. & P. Panikkar, 2009. Assessment of impacts of invasive fishes on the food web structure and ecosystem properties of a tropical reservoir in India. Ecological Modelling 220: 2281–2290.CrossRefGoogle Scholar
  41. Kolar, C. S., D. C. Chapman, W. R. Jr Courtenay, C. M. Housel, J. D. Williams & D. P. Jennings, 2007. Bigheaded carps – a biological synopsis and environmental risk assessment, Bethesda.Google Scholar
  42. Kovács, B., G. Boros, Z. Vitál, A. Mozsár, A. Specziár, V. Józsa, B. Urbányi & I. Lehoczky, 2016. Genetic analysis of filter-feeding Asian carps (Hypophthalmichthys spp.) in Lake Balaton, Hungary. Aquaculture Europe 2016 – Conference of the European Aquaculture Society, 20–23 September, Edinburgh, Scotland. (Abstract 251;
  43. Legendre, P. & L. Legendre, 2012. Numerical Ecology. Elsevier, Amsterdam.Google Scholar
  44. Lepš, J. & P. Šmilauer, 2003. Multivariate Analysis of Ecological Data Using CANOCO. Cambridge University Press, New York.Google Scholar
  45. Lieberman, D. M., 1996. Use of silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) for algae control in a small pond: changes in water quality. Journal of Freshwater Ecology 11: 391–397.CrossRefGoogle Scholar
  46. Lin, Q., X. Jiang, B. P. Han & E. Jeppesen, 2014. Does stocking of filter-feeding fish for production have a cascading effect on zooplankton and ecological state? A study of fourteen (sub)tropical Chinese reservoirs with contrasting nutrient concentrations. Hydrobiologia 736: 115–125.CrossRefGoogle Scholar
  47. Lu, M., P. Xie, H. Tang, Z. Shao & L. Xie, 2002. Experimental study of trophic cascade effect of silver carp (Hypophthalmichthys molitrix) in a subtropical lake, Lake Donghu: on plankton community and underlying mechanisms of changes of crustacean community. Hydrobiologia 487: 19–31.CrossRefGoogle Scholar
  48. Mátyás, K., I. Oldal, J. Korponai, I. Tátrai & G. Palulovits, 2003. Indirect effect of different communities on nutrient chlorophyll relationship in shallow hypertrophic water quality reservoirs. Hydrobiologia 504: 231–239.CrossRefGoogle Scholar
  49. O’Brien, K. R., C. L. Meyer, A. M. Waite, G. N. Ivey & D. P. Hamilton, 2004. Disaggregation of Microcystis aeruginosa colonies under turbulent mixing: laboratory experiments in a drid-stirred tank. Hydrobiologia 519: 143–152.CrossRefGoogle Scholar
  50. Peres-Neto, P. R., P. Legendre, S. Dray & D. Borcard, 2006. Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87: 2614–2625.CrossRefPubMedGoogle Scholar
  51. Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics. 18: 293–320.CrossRefGoogle Scholar
  52. Rellstab, C. & P. Spaak, 2007. Starving with a full gut? Effect of suspended particles on the fitness of Daphnia hyaline. Hydrobiologia 594: 131–139.CrossRefGoogle Scholar
  53. Sampson, S. J., J. H. Chick & M. A. Pegg, 2009. Diet overlap among two Asian carp and three native fishes in backwater lakes on the Illinois and Mississippi rivers. Biological Invasions 11: 483–496.CrossRefGoogle Scholar
  54. Sanderson, S. L., M. C. Stebar, K. L. Ackerman, S. H. Jones, I. E. Batjakas & L. Kaufman, 1996. Mucus entrapment of particles by a suspension-feeding tilapia (Pisces: Cichlidae). The Journal of Experimental Biology 199: 1746–1756.Google Scholar
  55. Sass, G. G., C. Hinz, A. C. Erickson, N. N. McClelland, M. A. McClelland & J. M. Epifanio, 2014. Invasive bighead and silver carp effects on zooplankton communities in the Illinois River, Illinois, USA. Journal of Great Lakes Research 40: 911–921.CrossRefGoogle Scholar
  56. Smith, D. W., 1989. The feeding selectivity of silver carp, Hypophthalmichthys molitrix Val. Journal of Fish Biology 34: 819–828.CrossRefGoogle Scholar
  57. Solomon, L. E., R. M. Pendleton, J. H. Chick & A. F. Casper, 2016. Long term changes in fish community structure in relation to the establishment of Asian carps in a large floodplain river. Biological Invasions 18: 2883–2895.CrossRefGoogle Scholar
  58. Spataru, P., G. W. Wohlfarth & G. Hulata, 1983. Studies on the natural food of different fish species in intensively manured polyculture ponds. Aquaculture 35: 283–298.CrossRefGoogle Scholar
  59. Specziár, A. & E. T. Rezsu, 2009. Feeding guilds and food resource partitioning in a lake fish assemblage: an ontogenetic approach. Journal of Fish Biology 75: 247–267.CrossRefPubMedGoogle Scholar
  60. Specziár, A., T. Erős, Á. I. György, I. Tátrai & P. Bíró, 2009. A comparison between the Nordic gillnet and whole water column gillnet for characterizing fish assemblages in the shallow Lake Balaton. Annales de Limnologie – International. Journal of Limnology 45: 171–180.CrossRefGoogle Scholar
  61. Specziár, A., Á. I. György & T. Erős, 2013. Within-lake distribution patterns of fish assemblages: the relative role of spatial, temporal and random environmental factors in assessing fish assemblages using gillnets in a large and shallow temperate lake. Journal of Fish Biology 82: 840–855.CrossRefPubMedGoogle Scholar
  62. Tátrai, I., G. Paulovits, V. Józsa, G. Boros, Á. I. György & J. Héri, 2009. Halállományok eloszlása és a betelepített halfajok állománya a Balatonban. [Distribution of fish stocks and the stock of the introduced fish species in Lake Balaton.] In Bíró, P. & J. Banczerowski (eds), A Balatonkutatások fontosabb eredményei 1999–2009. MTA, Budapest: 129–141. (in Hungarian).  Google Scholar
  63. ter Braak, C. J. F. & P. Šmilauer, 2002. CANOCO Reference Manual and CanoDraw for Windows user’s Guide: Software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca, New York.Google Scholar
  64. Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilunger der Internationale Vereinigunk für theoretische und angewandte Limnologie 9: 1–38.Google Scholar
  65. van Kleef, H., G. van der Velde, R. S. E. W. Leuven & H. Esselink, 2008. Pumpkinseed sunfish (Lepomis gibbosus) invasions facilitated by introductions and nature management strongly reduce macroinvertebrate abundance in isolated water bodies. Biological Invasions 10: 1481–1490.CrossRefGoogle Scholar
  66. Vitál, Z., A. Specziár, A. Mozsár, P. Takács, G. Borics, J. Görgényi, L. G.-Tóth, S. A. Nagy & G. Boros, 2015. Applicability of gill raker filtrates and foregut contents in the diet assessment of filter-feeding Asian carps. Fundamental and Applied Limnology 187: 79–86.CrossRefGoogle Scholar
  67. Vörös, L., I. Oldal, M. Présing & K. V. Balogh, 1997. Size-selective filtration and taxon-specific digestion of plankton algae by silver carp (Hypophthalmichthys molitrix Val.). Hydrobiologia 342/343: 223–228.CrossRefGoogle Scholar
  68. Xie, P. & J. Liu, 2001. Practical success of biomanipulation using filter-feeding fish to control cyanobacteria blooms. A synthesis of decades of research and application in a subtropical hypereutrophic lake. The Scientific World Journal 1: 337–356.CrossRefPubMedGoogle Scholar
  69. Yang, Y., X. Huang & J. Liu, 1999. Long-therm changes in crustacean zooplankton and water quality in a shallow eutrophic Chinese lake densely stocked with fish. Hydrobiologia 391: 195–203.Google Scholar
  70. Zhang, X., P. Xie & X. Huang, 2008. Review of Nontraditional Biomanipulation. The Scientific World Journal 8: 1184–1196.CrossRefPubMedGoogle Scholar
  71. Zhou, G., X. Thao, Y. Bi & Z. Hu, 2011. Effects of silver carp (Hypophthalmichthys molitrix) on spring phytoplankton community structure of Three-Gorges Reservoir (China): results from an enclosure experiment. Journal of Limnology 70: 26–32.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Attila Mozsár
    • 1
    • 3
    Email author
  • András Specziár
    • 1
  • Izabella Battonyai
    • 1
  • Gábor Borics
    • 2
  • Judit Görgényi
    • 2
  • Hajnalka Horváth
    • 1
  • Mátyás Présing
    • 1
  • László G.-Tóth
    • 1
  • Zoltán Vitál
    • 1
  • Gergely Boros
    • 1
  1. 1.Balaton Limnological InstituteMTA Centre for Ecological ResearchTihanyHungary
  2. 2.Tisza Research DepartmentMTA Centre for Ecological ResearchDebrecenHungary
  3. 3.Research Institute for Fisheries and AquacultureNational Agricultural Research and Innovation CentreSzarvasHungary

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