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Silver carp (Hypophthalmichthys molitrix) can non-mechanically digest cyanobacteria

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Abstract

The growth of cyanobacteria (blue-green algae) is a typical phenomenon in water bodies worldwide. The use of silver carp (Hypophthalmichthys molitrix) to reduce excessive phytoplankton development is controversial. In the case of cyanobacteria, many of which are toxic, understanding their possible digestion mechanism by fish is particularly desirable. A unique methodical approach, which consists of applying intestinal contents or extracts to a cyanobacteria culture, was used. Unicellular cyanobacteria (Cyanothece) were incubated in vitro with bile, contents of different parts of the intestinal tract, and cytosolic and microsomal extracts of the intestinal tissue of silver carp. The abundance of cyanobacteria decreased in all treatments containing either exclusively bile or its combination with intestinal contents. This research provides the first evidence of non-mechanical digestion of cyanobacteria by silver carp. Cyanobacteria incubated with intestinal contents or extracts reached mostly higher abundances than those incubated with the nutrient medium. The existence of non-mechanical digestion mediated via intestinal contents and extracts or its compensation connected with organic substance uptake is discussed.

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References

  • Bairagi A, Ghosh KS, Sen SK, Ray AK (2002) Enzyme producing bacterial flora isolated from fish digestive tracts. Aquac Int 10:109–121

    Article  CAS  Google Scholar 

  • Ballantyne JS (2014) Membranes and metabolism. In: Evans DH, Claiborne JB, Currie S (eds) The physiology of fishes, 4th edn. CRC Press, Boca Raton, FL, pp 81–147

  • Barsanti L, Gualtieri P (2014) Algae: anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton, FL

    Book  Google Scholar 

  • Beardall J, Raven JA (2016) Carbon acquisition by microalgae. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae, vol 6. Springer, Cham, pp 89–100

    Chapter  Google Scholar 

  • Bitterlich G (1985) Digestive enzyme pattern of two stomachless filter feeders, silver carp, Hypophthalmichthys molitrix Val., and bighead carp, Aristichthys nobilis Rich. J Fish Biol 27:103–112

    Article  CAS  Google Scholar 

  • Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272

    Article  CAS  Google Scholar 

  • Cold Spring Harb. Protoc. (2006) Phosphate-buffered saline (PBS). http://cshprotocols.cshlp.org/content/2006/1/pdb.rec8247.full?text_only&x003D;true. Accessed 12 Mar 2015

  • Datta(Saha) S, Jana BB (1998) Control of bloom in a tropical lake: grazing efficiency of some herbivorous fishes. J Fish Biol 53:12–24

  • De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175

    Article  Google Scholar 

  • Denstadli V, Skrede A, Krogdahl Å, Sahlstrøm S, Storebakken T (2006) Feed intake, growth, feed conversion, digestibility, enzyme activities and intestinal structure in Atlantic salmon (Salmo salar L.) fed graded levels of phytic acid. Aquaculture 256:365–376

    Article  CAS  Google Scholar 

  • Friedland KD, Ahrenholz DW, Haas LW (2005) Viable gut passage of cyanobacteria through the filter-feeding fish Atlantic menhaden, Brevoortia tyrannus. J Plankton Res 27:715–718

    Article  Google Scholar 

  • Gavel A, Maršálek B, Adámek Z (2004) Viability of Microcystis colonies is not damaged by silver carp (Hypophthalmichthys molitrix) digestion. Algol Stud 113:189–194

    Article  Google Scholar 

  • Harpaz S, Uni Z (1999) Activity of intestinal mucosal brush border membrane enzymes in relation to the feeding habits of three aquaculture fish species. Comp Biochem Phys A 124:155–160

    Article  Google Scholar 

  • Herodek S, Tátrai I, Oláh J, Vörös L (1989) Feeding experiments with silver carp (Hypophthalmichthys molitrix Val.) fry. Aquaculture 83:331–344

    Article  Google Scholar 

  • van den Hoek C, Jahns HM, Mann DG (1993) Algen, 3rd edn. G. Thieme, Stuttgart

    Google Scholar 

  • Jančula D, Míkovcová M, Adámek Z, Maršálek B (2008) Changes in the photosynthetic activity of Microcystis colonies after gut passage through Nile tilapia (Oreochromis niloticus) and silver carp (Hypophthalmichthys molitrix). Aquac Res 39:311–314

    Article  Google Scholar 

  • Jónás E, Rágyanszki M, Oláh J, Boross L (1983) Proteolytic digestive enzymes of carnivorous (Silurus glanis L.), herbivorous (Hypophthalmichthys molitrix Val.) and omnivorous (Cyprinus carpio L.) fishes. Aquaculture 30:145–154

    Article  Google Scholar 

  • Kajak Z, Rybak JI, Spodniewska I, Godlewska-Lipowa WA (1975) Influence of the planktonivorous fish Hypophthalmichthys molitrix (Val.) on the plankton and benthos of the eutrophic lake. Pol Arch Hydrobiol 22:301–310

  • Ke Z-X, Xie P, Guo L-G (2009) Impacts of two biomanipulation fishes stocked in a large pen on the plankton abundance and water quality during a period of phytoplankton seasonal succession. Ecol Eng 35:1610–1618

    Article  Google Scholar 

  • Kirilenko NS, Chigrinzkaya YN (1983) Activity of digestive enzymes in the silver carp, Hypophthalmichthys molitrix (Cyprinidae), feeding on blue-green algae. J Ichthyol 23:79–83

  • Kolmakov VI, Gladyshev MI (2003) Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crucian carp. Aquat Ecol 37:237–242

    Article  CAS  Google Scholar 

  • Kolmakov VI, Gladyshev MI, Kravchuk ES, Gribovskaya IV (2002) The possible mechanisms of stimulation of cyanobacterium growth by the passage through the Carassius auratus intestine: an experimental study. Dokl Biol Sci 384:230–232

  • Kolmakov VI, Gladyshev MI, Kravchuk ES, Chuprov SM, Anishchenko OV, Ivanova EA, Trusova MY, (2006) Species-specific stimulation of cyanobacteria by silver carp Hypophthalmichthys molitrix (Val.). Dokl Biol Sci 408:223–225

    Article  CAS  Google Scholar 

  • Komárek J (2003) Coccoid and colonial cyanobacteria. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America. Ecology and Classification. Academic Press, San Diego (CA), pp 59–116

    Chapter  Google Scholar 

  • Krogdahl Å, Sundby A, Bakke AM (2011) Gut secretion and digestion. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment, vol 2. Academic Press, Amsterdam, pp 1301–1310

  • Kuz'mina VV, Gelman AG (1997) Membrane-linked digestion in fish. Rev Fish Sci 5:99–129

    Article  Google Scholar 

  • Kvåle A, Mangor-Jensen A, Moren M, Espe M, Hamre K (2007) Development and characterisation of some intestinal enzymes in Atlantic cod (Gadus morhua L.) and Atlantic halibut (Hippoglossus hippoglossus L.) larvae. Aquaculture 264:457–468

    Article  Google Scholar 

  • Lewin W-C, Kamjunke N, Mehner T (2003) Phosphorus uptake by Microcystis during passage through fish guts. Limnol Oceanogr 48:2392–2396

    Article  Google Scholar 

  • Ma H, Cui F, Liu Z, Fan Z, He W, Yin P (2010) Effect of filter-feeding fish silver carp on phytoplankton species and size distribution in surface water: a field study in water works. J Environ Sci 22:161–167

    Article  CAS  Google Scholar 

  • Miura T, Wang J (1985) Chlorophyll a found in feces of phytoplanktivorous cyprinids and its photosynthetic activity. Verh Int Ver Limnol 22:2636–2642

    Google Scholar 

  • Moriarty CM, Moriarty DJW (1973) Quantitative estimation of the daily ingestion of phytoplankton by Tilapia nilotica and Haplochromis nigripinnis in Lake George, Uganda. J Zool 171:15–23

    Article  Google Scholar 

  • Opuszynski K (1979) Silver carp, Hypophthalmichthys molitrix (Val.), in carp ponds III. Influence on ecosystem. Pol J Ecol 27:117–133

    Google Scholar 

  • Perschbacher PW (2018) An experimental evaluation of the short-term phytoplankton impacts of silver and bighead carps and their hybrids. J Fisheries Livest Prod 6:272. https://doi.org/10.4172/2332-2608.1000272

  • Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332–1334

    Article  CAS  Google Scholar 

  • Provasoli L, McLaughlin JJA, Droop MR (1957) The development of artificial media for marine algae. Arch Microbiol 25:392–428

  • Reddy KJ, Haskell JB, Sherman DM, Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175:1284–1292

    Article  CAS  Google Scholar 

  • Rust MB (2002) Nutritional physiology. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego (CA), pp 368–453

    Google Scholar 

  • Spataru P, Gophen M (1985) Feeding behaviour of silver carp Hypophthalmichthys molitrix Val. and its impact on the food web in Lake Kinneret, Israel. Hydrobiologia 120:53–61

    Article  Google Scholar 

  • Vörös L, Oldal I, Présing M, V.-Balogh K (1997) Size-selective filtration and taxon-specific digestion of plankton algae by silver carp (Hypophthalmichthys molitrix Val.). Hydrobiologia 342-343:223–228

  • Vörös L, Présing M, V.-Balogh K, Oldal I (1998) Nutrient removal efficiency of a pollution control reservoir. Int Rev Hydrobiol 83:665–672 

  • Wang Y, Gu X, Zeng Q, Mao Z, Wang W (2016) Contrasting response of a plankton community to two filter-feeding fish and their feces: An in situ enclosure experiment. Aquaculture 465:330–340

    Article  Google Scholar 

  • Wiegand C, Pflugmacher S, Oberemm A, Steinberg C (2000) Activity development of selected detoxication enzymes during the ontogenesis of the zebrafish (Danio rerio). Int Rev Hydrobiol 85:413–422

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Xie P (2001) Gut contents of bighead carp (Aristichthys nobilis) and the processing and digestion of algal cells in the alimentary canal. Aquaculture 195:149–161

    Article  Google Scholar 

  • Yi C, Guo L, Ni L, Luo C (2016) Silver carp exhibited an enhanced ability of biomanipulation to control cyanobacteria bloom compared to bighead carp in hypereutrophic Lake Taihu mesocosms. Ecol Eng 89:7–13

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Zeng Q, Gu X, Mao Z, Chen X (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

    Article  CAS  Google Scholar 

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Acknowledgements

We wish to thank Jiří Šetlík for his help in the laboratory and for providing valuable comments.

Funding

This work was supported by the Ministry of Agriculture of the Czech Republic, project NAZV QK1710310, and by the Ministry of Education, Youth and Sports of the Czech Republic, projects CENAKVA (LM2018099), Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370), and GAJU (No. 081/2016/Z).

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Authors and Affiliations

  1. Faculty of Agriculture, University of South Bohemia in České Budějovice, České Budějovice, Czech Republic

    Irena Šetlíková & Sandra Maciarzová

  2. Faculty of Fisheries and Protection of Waters, South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses, University of South Bohemia in České Budějovice, Vodňany, Czech Republic

    Martin Bláha & Tomáš Policar

Authors
  1. Irena Šetlíková
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  2. Sandra Maciarzová
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  3. Martin Bláha
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  4. Tomáš Policar
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Correspondence to Irena Šetlíková.

Ethics declarations

The experiments were performed and the experimental fish were handled in accordance with national and international guidelines for the protection of animal welfare (EU-harmonized Animal Welfare Act of the Czech Republic). The unit is licenced (No. 2293/2015-MZE-17214 and No. 55187/2016-MZE-17214 within project NAZV QK1710310) according to the Czech National Directive (the Law against Animal Cruelty, No. 246/1992).

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Šetlíková, I., Maciarzová, S., Bláha, M. et al. Silver carp (Hypophthalmichthys molitrix) can non-mechanically digest cyanobacteria. Fish Physiol Biochem 46, 771–776 (2020). https://doi.org/10.1007/s10695-019-00751-1

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