Abstract
The growth and photosynthetic activities of Cyanobacteria passed through the gut of silver carp (Hypophthalmichthys molitrix), bighead carp (Aristichthys nobilis), and tilapia (Oreochromis niloticus) were compared with those of phytoplankton taken directly from Lake Taihu during a 13-day in situ dialysis culture. After the first 3–5 days of reduced activity after excretion by silver carp and bighead carp, the photosynthetic activity of Cyanobacteria recovered and rose significantly higher (P < 0.01) than levels in the control population, whereas there was a notable reduction of photosynthetic activity after passage through tilapia gut. The phytoplankton biomass showed a 2- to 3-fold increase of growth, and extracellular polysaccharide production was also stimulated after passage through silver carp and bighead carp gut. Chlorophyta fluorescence was detected at much higher levels than that of Cyanobacteria and Bacillariophyta after passage through tilapia gut. Scenedesmus obliqnus and Chlamydomonas sp. contributed much to the growth of the Chlorophyta during the in situ cultivation. However, the total phytoplankton biomass showed a distinct reduction in the tilapia treatment during the culture. The study indicated that Nile tilapia feeding and defecation may help remove Cyanobacteria from the water column and favor a community shift to Chlorophyta.
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Bi, B., Z. W. Sun, T. Q. Mao, H. B. Yin & L. J. Wang, 2011. Relationship between digestive tract structure and feeding habits in common carp, grass carp, silver carp and bighead carp. Chinese Journal of Fisheries 24(1): 26–29. (in Chinese).
Cerda, O., U. Karsten, E. Rothäusler, F. Tala & M. Thiel, 2009. Compensatory growth of the kelp Macrocystis integrifolia (Phaeophyceae, Laminariales) against grazing of Peramphithoe femorata (Amphipoda, Ampithoidae) in northern-central Chile. Journal of Experimental Marine Biology and Ecology 377: 61–67.
Chen, J., P. Xie, D. Zhang, Z. X. Ke & H. Yang, 2006. In situ studies on the bioaccumulation of microcystins in the phytoplanktivorous silver carp (Hypophthalmichthys molitrix) stocked in Lake Taihu with dense toxic Microcystis blooms. Aquaculture 261(3): 1026–1038.
Datta, S. & B. B. Jana, 1998. Control of bloom in a tropical lake: grazing efficiency of some herbivorous fishes. Journal of Fish Biology 53(1): 12–24.
Dong, G. F., X. M. Zhu, D. Han, Y. X. Yang, L. R. Song & S. Q. Xie, 2009. Effects of dietary cyanobacteria of two different sources on growth and recovery of hybrid tilapia (Oreochromis niloticus × O. aureus). Toxicon 54: 208–216.
Figueredo, C. C. & A. Giani, 2005. Ecological interactions between Nile tilapia (Oreochromis niloticus, L.) and the phytoplanktonic community of the Furnas Reservoir (Brazil). Freshwater Biology 50(8): 1391–1403.
Flöder, S., S. Jaschinski, G. Wells & C. W. Burns, 2010. Dominance and compensatory growth in phytoplankton communities under salinity stress. Journal of Experimental Marine Biology and Ecology 395(1–2): 223–231.
Friedland, K. D., D. W. Ahrenholz & L. W. Haas, 2005. Viable gut passage of Cyanobacteria through the filter-feeding fish Atlantic menhaden, Brevoortia tyrannus. Journal of Plankton Research 27(7): 715–718.
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.
Hu, H. J., R. Y. Li, Y. X. Wei, H. Z. Zhu, J. Y. Chen & Z. X. Shi, 1980. Freshwater Algae in China. Shanghai Science and Technology Press, Shanghai: 1–525. (in Chinese).
Jančula, D., M. Míkovcová, Z. Adámek & B. Maršálek, 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(3): 311–314.
Juneau, P., B. R. Green & P. J. Harrison, 2005. Simulation of Pulse-Amplitude-Modulated (PAM) fluorescence. Limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica 43: 75–83.
Kamjunke, N. & T. Mehner, 2001. Coupling the microbial food web with fish: Are bacteria attached to Cyanobacteria an important food source for underyearling roach? Freshwater Biology 46(5): 633–639.
Kamjunke, N., R. Mendonca, I. Hardewig & T. Mehner, 2002a. Assimilation of different Cyanobacteria as food and the consequences for internal energy stores of juvenile roach. Journal of Fish Biology 60(3): 731–738.
Kamjunke, N., K. Schmidt, S. Pflugmacher & T. Mehner, 2002b. Consumption of Cyanobacteria by roach (Rutilus rutilus): useful or harmful to the fish? Freshwater Biology 47(2): 243–250.
Kolmakov, V. I. & M. I. Gladyshev, 2003. Growth and potential photosynthesis of Cyanobacteria are stimulated by viable gut passage in crucian carp. Aquatic Ecology 37(3): 237–242.
Kolmakov, V. I., M. I. Gladyshev, E. S. Kravchuk, S. M. Chuprov, O. V. Anishchenkob, E. A. Ivanova & M. Y. Trusova, 2006. Species-specific stimulation of Cyanobacteria by silver carp Hypophthalmichthys molitrix (Val.). Doklady Biological Sciences 408: 223–225.
Lazzaro, X., 1987. A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts. Hydrobiologia 146(2): 97–167.
Lazzaro, X., M. Bouvy, R. A. Ribeiro-Filho, V. S. Oliveira, L. T. Sales, A. R. M. Vasconcelos & M. R. Mata, 2003. Do fish regulate phytoplankton in shallow eutrophic Northeast Brazilian reservoirs? Freshwater Biology 48: 649–668.
Lewin, W. C., N. Kamjunke & T. Mehner, 2003. Phosphorus uptake by Microcystis during passage through fish guts. Limnology and Oceanography 48(6): 2392–2396.
Ma, H., F. Y. Cui, Z. Q. Liu, Z. Q. Fan, W. J. He & P. J. Yin, 2010. Effect of filter-feeding fish silver carp on phytoplankton species and size distribution in surface water: a field study in water works. Journal of Environmental Sciences 22(2): 161–167.
Mátyás, K., I. Oldal, J. Korponai, I. Tátrai & G. Paulovits, 2003. Indirect effect of different fish communities on nutrient chlorophyll relationship in shallow hypertrophic water quality reservoirs. Hydrobiologia 504(1–3): 231–239.
Miura, T. & J. Wang, 1985. Chlorophyll a found in feces of phytoplanktivorous cyprinids and photosynthetic activity. Verhandlungen des Internationalen Verein Limnologie 22: 2636–2642.
Moriarty, C. M. & D. J. W. Moriarty, 1973. The assimilation of carbon from phytoplankton by two herbivorous fishes: Tilapia nilotica and Haplochromis nigripinnis. Journal of Zoology 171: 41–55.
Pápista, É., É. Ács & B. Böddi, 2002. Chlorophyll-a determination with ethanol-a critical test. Hydrobiologia 485(1): 191–198.
Semyalo, R., T. Rohrlack, D. Kayiira, Y. S. Kizito, S. Byarujali, G. Nyakairu & P. Larsson, 2011. On the diet of Nile tilapia in two eutrophic tropical lakes containing toxin producing cyanobacteria. Limnologica 41: 30–36.
Silvertown, J. & D. M. Gordon, 1989. A framework for plant behaviour. Annual Review of Ecology, Evolution, and Systematics 20: 349–366.
Smith, J. L., G. L. Boyer & P. V. Zimba, 2008. A review of Cyanobacterial odorous and bioactive metabolites: impacts and management alternatives in aquaculture. Aquaculture 280(1–4): 5–20.
Sun, S. C. & Y. P. Huang, 1993. Lake Taihu. Chinese Ocean Press, Beijing: 5.
Turker, H., A. G. Eversole & D. E. Brune, 2003. Filtration of green algae and cyanobacteria by Nile tilapia, Oreochromis niloticus, in the Partitioned Aquaculture System. Aquaculture 215: 93–101.
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.
Wang, J., P. Xie, N. Takamura, L. Q. Xie, A. J. Shao & H. J. Tang, 2004. The picophytoplankton in three Chinese lakes of different trophic status and its relationship to fish populations. Journal of Freshwater Ecology 19(2): 285–293.
White, S., A. Anandraj & F. Bux, 2011. PAM fluorometry as a tool to asses microalgal nutrient stress and monitor cellular neutral lipids. Bioresource Technology 102: 1675–1682.
Xu, H., H. W. Paerl, B. Q. Qin, G. W. Zhu & G. Gao, 2010. Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography 55(1): 420–432.
Yang, Z., Y. Liu, J. Ge, W. Wang, Y. Chen & D. Montagnes, 2010. Aggregate formation and polysaccharide content of Chlorella pyrenoidosa Chick (Chlorophyta) in response to simulated nutrient stress. Bioresource Technology 101(21): 8336–8341.
Zhang, X., P. Xie & X. P. Huang, 2008. A review of nontraditional biomanipulation. Science World Journal 8: 1184–1196.
Zhang, X., P. Xie, L. Hao, N. Guo, Y. G. Gong, X. L. Hu, J. Chen & G. D. Liang, 2006. Effects of the phytoplanktivorous silver carp (Hypophthalmichthys molitrixon) on plankton and the hepatotoxic microcystins in an enclosure experiment in a eutrophic lake, Lake Shichahai in Beijing. Aquaculture 257(1–4): 173–186.
Acknowledgment
We are grateful to Wang Yinping for his experimental work for this manuscript. This study has been supported by the National Natural Science Foundation of China (Nos. 30900207 and 31372569), the “twelfth five-year-plan” in National Science and Technology for the Rural Development in China (2012BAD25B07) and State Environmental Protection Commonwealth Trade Scientific Research Funds (No. 2010467014).
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Zeng, Q., Gu, X., Mao, Z. et al. 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 (2014). https://doi.org/10.1007/s10750-014-1886-5
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DOI: https://doi.org/10.1007/s10750-014-1886-5