Hydrobiologia

, Volume 764, Issue 1, pp 115–126 | Cite as

The role of filter-feeding Asian carps in algal dispersion

  • Judit Görgényi
  • Gergely Boros
  • Zoltán Vitál
  • Attila Mozsár
  • Gábor Várbíró
  • Gábor Vasas
  • Gábor Borics
PHYTOPLANKTON & SPATIAL GRADIENTS

Abstract

The gut contents of filter-feeding fish often contain considerable amounts of viable phytoplankton cells; thus, these animals can act as vectors in the horizontal and vertical transport of algae. In this study, the potential role of the introduced filter-feeding Asian carps (hybrids of silver carp Hypophthalmichthys molitrix and bighead carp H. nobilis) in algal dispersion was studied in the oligo-mesotrophic Lake Balaton (Hungary). We examined the algal composition in the lake water, gut contents (foregut and hindgut), and occasionally in the filtered suspensions collected directly from the gill rakers (filtering apparatus) of fish. Microscopic analyses revealed that the phytoplankton composition of the ingested food differed considerably from what we found in the lake water. Cryptophytes, dinoflagellates, and euglenophytes were observed in both the lake water and foregut samples but were absent in the hindgut samples. However, in the cultured hindgut samples, we found viable cells of several phytoplankton taxa (e.g., diatoms, blue-greens, desmids, volvocalean and chlorococcalean green algae), which managed to survive the physical and chemical digestion. These results imply that the presence of these filter-feeding fish can alter the phytoplankton species composition and promote the dominance of taxa that are able to resist digestion.

Keywords

Phytoplankton Digestibility Biogeography Asian carps 

Supplementary material

10750_2015_2285_MOESM1_ESM.docx (35 kb)
Supplementary material 1 (DOCX 35 kb)

References

  1. Bitterlich, G., 1985. Digestive enzyme pattern of two stomachless filter feeder, silver carp, Hypophthalmichthys molitrix Val., and bighead carp, Aristichthys nobilis Rich. Journal of Fish Biology 27: 103–112.CrossRefGoogle Scholar
  2. Borics, G., I. Grigorszky, J. Padisák & S. Szabó, 2000. Phytoplankton associations in a small hypertrophic fishpond in East Hungary during a change from bottom-up to top-down control. Hydrobiologia 424: 79–90.CrossRefGoogle Scholar
  3. Borics, G., L. Nagy, S. Miron, I. Grigorszky, Z. László-Nagy, B. A. Lukács, L. G. Tóth & G. Várbíró, 2013. Which factors affect phytoplankton biomass in shallow eutrophic lakes? Hydrobiologia 714: 93–104.CrossRefGoogle Scholar
  4. Boros, G., A. Mozsár, Z. Vitál, S. A. Nagy & A. Specziár, 2014. Growth and condition factor of hybrid (Bighead Hypophthalmichthys nobilis Richardson, 1845 x silver carp H. molitrix Valenciennes, 1844) Asian carps in the shallow, oligo-mesotrophic Lake Balaton. Journal of Applied Ichthyology-Zeitschrift für Angewandte Ichthyologie 30: 546–548.Google Scholar
  5. Brown, R. M., D. H. Larson Jr & H. C. Bold, 1964. Airborne algae: their abundance and heterogeneity. Science 143: 583–585.CrossRefPubMedGoogle Scholar
  6. Chrisostomou, A., M. Moustaka-Gouni, S. Sgardelis & T. Lanaras, 2009. Air-dispersed phytoplankton in a Mediterranean river–reservoir system (Aliakmon-Polyphytos, Greece). Journal of Plankton Research 31: 877–884.CrossRefGoogle Scholar
  7. Cox, C. B. & P. D. Moore, 1993. Biogeography: An Ecological and Evolutionary Approach. Blackwell Scientific Publications, Oxford: 326.Google Scholar
  8. 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
  9. Datta, S. & B. B. Jana, 1998. Control of bloom in a tropical lake: grazing efficiency of some herbivorous fishes. Journal of Fish Biology 53: 12–24.CrossRefGoogle Scholar
  10. Dong, S., D. Li, X. Bing, Q. Shi & F. Wang, 1992. Suction volume and filtering efficiency of silver carp (Hypophthalmichthys molitrix Val.) and bighead carp (Hypophthalmichthys nobilis Rich.). Journal of Fish Biology 41: 833–840.CrossRefGoogle Scholar
  11. Ettl, H., 1978. Xanthophyceae. In Ettl, H., J. Gerloff & H. Heynig (eds), Süßwasserflora von Mitteleuropa, Vol. 3/1. Gustav Fischer Verlag, Stuttgart.Google Scholar
  12. Förster, K., 1982. Conjugatophyceae. Zygnematales und Desmidiales (excl. Zygnemataceae). In Huber-Pestalozzi, G. (Ed.), Das Phytoplankton des Süsswassers: Systematik und Biologie, Vol. 16/8. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.Google Scholar
  13. Gavel, A., B. Maršálek & Z. Adámek, 2004. Viability of Microcystis colonies is not damaged by silver carp (Hypophthalmichthys molitrix) digestion. Algological Studies 113: 189–194.CrossRefGoogle Scholar
  14. Genitsaris, S., K. A. Kormas & M. Moustaka-Gouni, 2011. Airborne algae and cyanobacteria: occurrence and related health effects. Frontiers in Bioscience E3: 772–787.CrossRefGoogle Scholar
  15. Hammer, O., D. A. T. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 9.Google Scholar
  16. Hampl, A., J. Jirasek & D. Sirotek, 1983. Growth morphology of the filtering apparatus of silver carp (Hypophthalmichthys molitrix Val.) II. microscopic anatomy. Aquaculture 31: 153–158.CrossRefGoogle Scholar
  17. Herodek, S., I. Tátrai, J. Oláh & L. Vörös, 1989. Feeding experiments with silver carp (Hypophthalmichthys molitrix Val.) fry. Aquaculture 83: 331–344.CrossRefGoogle Scholar
  18. Hofmann, G., M. Wermun & H. Lange-Bertalot, 2011. Diatomeen in Süßwasser-Benthos von Mitteleuropa. A.R.G. Gantner Verlag, Koeltz Scientific Books, Königstein.Google Scholar
  19. Huber-Pestalozzi, G., 1950. Das Phytoplankton des Süsswassers. Systematik und Biologie. Cryptophyceen, Chloromonadinen, Peridineen. In Thiemannn, A. (Ed.), Die Binnengewässer, Vol. 16/3. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.Google Scholar
  20. Huber-Pestalozzi, G., 1955. Das Phytoplankton des Süßwassers. Systematik und Biologie. Euglenophyceen. In Thiemannn, A. (Ed.), Die Binnengewässer, Vol. 16/4. Schweizerbart, Stuttgart.Google Scholar
  21. Huber-Pestalozzi, G., 1961. Das Phytoplankton des Süßwassers. Systematik und Biologie. Chlorophyceae, Volvocales. In Thiemannn, A. (Ed.), Die Binnengewässer, Vol. 16/5. Schweitzerbart’sche Verlagsbuchhandlung, Stuttgart.Google Scholar
  22. Hudon, C., S. Paquet & V. Jarry, 1996. Downstream variations of phytoplankton in the St. Lawrence River (Québec, Canada). Hydrobiologia 337: 1–26.CrossRefGoogle Scholar
  23. 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
  24. Jancula, D., M. Mikovcova, Z. Adamek & B. Marsalek, 2008. Changes in the photosynthetic activity of Microcystis colonies after gut passage through Nile tilapia (Oreochromis niloticus) and silver carp (Hypophthalmichthys molitrix). Aquaculture Research 39: 311–314.CrossRefGoogle Scholar
  25. Jennings, D. P., 1988. Bighead carp (Hypophthalmichthys nobilis): a biological synopsis. The United States Fish and Wildlife Service 88: 1–35.Google Scholar
  26. Kolar, C. S., D. C. Chapman, W. R. Courtenay Jr, C. M. Housel, J. D. Williams & D. P. Jennings, 2007. Bigheaded Carps: A Biological Synopsis and Environmental Risk Assessment, Vol. 33. American Fisheries Society Special Publication, Bethesda, Maryland.Google Scholar
  27. Kolmakov, V. I., M. I. Gladyshev, E. S. Kravchuk, S. M. Chuprov, O. V. Anishchenko, E. A. Ivanova & M. Yu. Trusova, 2006. Species-specific stimulation of cyanobacteria by silver carp Hypophthalmichthys molitrix (Val.). Doklady Biological Sciences 408: 223–225.CrossRefPubMedGoogle Scholar
  28. Komárek, J. & K. Anagnostidis, 1998. Cyanoprokaryota. Chroococcales. In Ettl, H., G. Gärtner, H. Heyni & D. Mollenhauer (eds), Süßwasserflora von Mitteleuropa, Vol. 19/1. Gustav Fisher, Berlin.Google Scholar
  29. Komárek, J. & K. Anagnostidis, 2005. Cyanoprokaryota. Oscillatoriales. In Büdel, B., L. Krienitz, G. Gärtner & M. Schagerl (eds), Süßwasserflora von Mitteleuropa, Vol. 19/2. Gustav Fisher, Jena.Google Scholar
  30. Komárek, J. & B. Fott, 1983. Das Phytoplankton des Süsswassers. Systematik und Biologie. Chlorophyceae (Grünalgen), Ordnung: Chlorococcales. In Huber-Pestalozzi, G. (Ed.), Die Binnengewässer, Vol. 16/7. Schweitzerbart’sche Verlagsbuchhandlung, Stuttgart.Google Scholar
  31. Krammer, K., 2003. Cymbopleura, Delicata, Navicymbula, Gomphocymbellopsis, Afrocymbella. In Lange-Berlot, H. (Ed.), Diatoms of the European Inland Waters and Comparable Habitats. A. R. Gantner Verlag, Ruggell.Google Scholar
  32. Krammer, H. & H. Lange-Bertalot, 1986–1991. Bacillariophyceae. In Ettl, H., G. Gärtner, J. Gerloff, H., Heynig & D. Mollenhauer (eds), Süßwasserflora von Mitteleuropa 2 (1–4). Gustav Fischer, Stuttgart.Google Scholar
  33. Lazzaro, X., 1987. A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts. Hydrobiologia 146: 97–167.CrossRefGoogle Scholar
  34. Lewin, W. C., N. Kamjunke & T. Mehner, 2003. Phosphorus uptake by Microcystis during passage through fish guts. Limnology and Oceanography 48: 2392–2396.CrossRefGoogle Scholar
  35. 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
  36. Miura, A. & J. Wang, 1985. Chlorophyll a found in feces of phytoplanktivorous cyprinids and its photosynthetic activity. Verhandlungen des Internationalen Verein Limnologie 22: 2636–2642.Google Scholar
  37. Moriarty, D. J. W., 1973. The physiology of digestion of blue-green algae in the cichlid fish, Tilapia nilotica. Journal of Zoology (London) 171: 25–39.CrossRefGoogle Scholar
  38. Moriarty, C. M. & D. J. W. Moriarty, 1973. Quantitative estimation of the daily ingestion of phytoplankton by Tilapia nilotica and Haplochromis nigripinnis in Lake George, Uganda. Journal of Zoology (London) 171: 15–23.CrossRefGoogle Scholar
  39. Northcott, M. E. & M. C. M. Beveridge, 1988. The development and structure of pharyngeal apparatus associated with filter feeding in tilapias (Oreochromis niloticus). Journal of Zoology (London) 215: 133–149.CrossRefGoogle Scholar
  40. Okuda, K., 2002. Structure and phylogeny of cell coverings. Journal of Plant Research 115: 283–288.CrossRefPubMedGoogle Scholar
  41. Padisák, J., 2004. Phytoplankton. In O’Sullivan, P. E. & C. S. Reynolds (eds), The lakes handbook. Blackwell Science Ltd., Oxford: 251–307.Google Scholar
  42. Padisák, J., G. Vasas & G. Borics, 2015. Phycogeography of freshwater phytoplankton – traditional knowledge and new molecular tools. Hydrobiologia. doi:10.1007/s10750-015-2259-4.Google Scholar
  43. Popovsky, J. & L. Pfiester, 1990. Dinophyceae (Dinoflagellida). In Ettl, H., J. Gerloff, H. Heynig & D. Mollenhauer (eds), Süßwasserflora von Mitteleuropa, Vol. 6. Gustav Fischer Verlag, Stuttgart.Google Scholar
  44. Porter, K. G., 1973. Selective grazing and differential digestion of algae by zooplankton. Nature 244: 179–180.CrossRefGoogle Scholar
  45. Porter, K., 1976. Enhancement of algal growth and productivity by grazing zooplankton. Science 192: 1332–1333.CrossRefPubMedGoogle Scholar
  46. Reynolds, C. S., 2000. Hydroecology of river plankton: the role of variability in channel flow. Hydrological Processes 14: 3119–3132.CrossRefGoogle Scholar
  47. 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
  48. Smith, D. W., 1989. The feeding selectivity of silver carp, Hypophthalmichthys molitrix Val. Journal of Fish Biology 34: 819–828.CrossRefGoogle Scholar
  49. Spataru, P., 1977. Gut contents of silver carp-Hypophthalmicthys molitrix (Val.) and some trophic relations to other fish species in a polyculture system. Aquaculture 11: 137–146.CrossRefGoogle Scholar
  50. Stanier, R. Y., R. Kunisawa, M. Mandel & G. Cohen-Bazire, 1971. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews 35: 171–205.PubMedCentralPubMedGoogle Scholar
  51. Starmach, K., 1985. Chrysophyceae und Haptophyceae. In Ettl, H., J. Gerloff, H. Heynig & D. Mollenhauer (eds), Süßwasserflora von Mitteleuropa, Vol. 1. Gustav Fischer Verlag, Stuttgart.Google Scholar
  52. Tátrai, I., V. Józsa, Á. I. György, M. Havasi & I. Szabó, 2006. A busa biológiai szerepének és hatásának vizsgálata a Balatonban [Investigation of the biological role and influence of silver carp in Lake Balaton]. In Mahunka, S. & J. Banczerowski (eds), A Balaton kutatásának 2005. évi eredményei. MTA, Budapest: 73–83. In Hungarian with English summary.Google Scholar
  53. Tátrai, I., V. Istvánovics, L. G. Tóth & I. Kóbor, 2008. Management measures and long-term water quality changes in Lake Balaton (Hungary). Fundamental and Applied Limnology, Archiv für Hydrobiologie 172: 1–11.CrossRefGoogle Scholar
  54. 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 Balaton kutatások fontosabb eredményei 1999-2009. MTA, Budapest: 129–141. [In Hungarian with English summary].Google Scholar
  55. Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen phytoplankton-methodik. Mitteilungen Internationale Vereinigung Theoretische und Angewandte Limnologie 9: 1–38.Google Scholar
  56. Van den Hoek, C., D. G. Mann & H. M. Jahns, 1995. Algae: An Introduction to Phycology. Cambridge University Press, Cambridge.Google Scholar
  57. Van Overeem, M. A., 1937. On green organisms occurring in the lower troposphere. Travaux Botaniques Néerlandais 34: 388–442.Google Scholar
  58. Vitál, Z., A. Specziár, A. Mozsár, P. Takács, G. Borics, J. Görgényi, 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. doi:10.1127/fal/2015/0698.Google Scholar
  59. 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.Google Scholar
  60. Xie, P., 1999. Gut contents of silver carp, Hypophthalmichthys molitrix, and the disruption of a centric diatom, Cyclotella, on passage through the esophagus and intestine. Aquaculture 180: 295–305.CrossRefGoogle Scholar
  61. Zeng, Q., X. Gu & Z. Mao, 2014. In situ growth and photosynthetic activity of Cyanobacteria and phytoplankton dynamics after passage through the gut of silver carp (Hypophthalmichthys molitrix), bighead carp (Aristichthys nobilis), and Nile tilapia (Oreochromis niloticus). Hydrobiologia 736: 51–60.CrossRefGoogle Scholar
  62. Zhang, X., P. Xie & X. Huang, 2008. Review of nontraditional biomanipulation. The Scientific World Journal 8: 1184–1196.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Judit Görgényi
    • 1
  • Gergely Boros
    • 2
  • Zoltán Vitál
    • 2
  • Attila Mozsár
    • 2
  • Gábor Várbíró
    • 1
  • Gábor Vasas
    • 3
  • Gábor Borics
    • 1
  1. 1.Department of Tisza ResearchMTA Centre for Ecological ResearchDebrecenHungary
  2. 2.Balaton Limnological InstituteMTA Centre for Ecological ResearchTihanyHungary
  3. 3.Department of BotanyUniversity of DebrecenDebrecenHungary

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