Can top-down effects of planktivorous fish removal be used to mitigate cyanobacterial blooms in large subtropical highland lakes?

Removal of planktivorous fish is used extensively in northern temperate lakes to reduce phytoplankton abundance via enhanced zooplankton grazing. However, whether this method would work also in large subtropical highland lakes to alleviate cyanobacterial blooms is unknown. We conducted a one-year pilot in situ experiment where we removed a substantial biomass of fish in a fenced-in area, followed by a 3-year whole-lake experiment where the dominant fish species (Japanese smelt) was removed in Lake Erhai in southwest China. The fencing experiments showed that between July and November, when the biomass of the removed stock reached 4 g/m2, the zooplankton biomass inside the fence increased significantly compared to a control fence. In the full-lake experiment, we found that sustained removal of Japanese smelt led to an increase in the biomass of cladocerans (Daphnia spp. but especially of Bosmina spp.) and a significant decrease in the biomass of Cyanobacteria and Chlorophyta. Additionally, a marked increase in the ratio of zooplankton to phytoplankton biomass, as well as an increase in the body size of cladocerans, emphasising the importance of enhanced top-down control for mitigating cyanobacterial blooms following extensive fish removal. Our results reveal that removal of small fish (here Japanese smelt) can lead to a reduction of the phytoplankton and cyanobacteria biomass through a trophic cascade in highland deep subtropical lakes. Thus fish removal may be a feasible additional restoration tool to external nutrient loading reduction in such lakes.

Physicochemical Process, Crustacean, and Microcystis Biomass Changes In Situ Enclosure after Introduction of Silver Carp at Meiliang Bay, Lake Taihu.

In order to control cyanobacteria blooms with silver carp in Lake Taihu, an in situ experiment was carried out by stocking silver carp at a biomass of 35, 70, and 150 g m-3 and no carp control in waterproof enclosures. Physicochemical water parameters and biomass of plankton were measured in enclosures to evaluate the suitable stocking density of silver carp for relieving internal nutrients and constraining cyanobacteria growth in Lake Taihu. It is found that the 35 g m-3 silver carp group and 70 g m-3 silver carp group presented lower total phosphorus, lower chlorophyll-a, and higher water transparency. Increased nitrogen to phosphorus ratio, which indicated the result of algae decline in fish presence enclosures, was attributed to decline of phosphorus. Phosphorus decline also exerted limitation on reestablish of cyanobacteria bloom. Crustacean zooplankton biomass and Microcystis biomass decreased significantly in fish presence enclosures. Silver carp could be more effective to regulate algae bloom in enclosures with dense cyanobacteria. Therefore, nonclassic manipulation is supposed to be appropriate method to get rid of cyanobacteria blooms in Lake Taihu by stocking 35 to 70 g m-3 silver carp in application.

Eutrophication strengthens the response of zooplankton to temperature changes in a high-altitude lake.

To assess whether and how zooplankton communities respond to variations in temperature and how these assemblages change with eutrophication, we performed a large-scale, monthly survey from August 2011 to July 2012 to determine the seasonal and spatial variations in these communities in a high-altitude lake. A detrended correspondence analysis and a path analysis demonstrated that temperature and chlorophyll a were important factors influencing zooplankton. The path diagram showed that Daphnia was negatively affected directly by chlorophyll a and indirectly by temperature, whereas Bosmina was directly and positively affected by temperature. Daphnia spp. decreased in both absolute and relative biomass during warm seasons, whereas Bosmina spp. showed the opposite trend. Moreover, the lowest Daphnia spp. biomass was observed in the southern region, which was the most eutrophic. Our results indicate that increasing temperatures will continue to shift the dominant genus from Daphnia to Bosmina, and this change will be exacerbated by eutrophication. In addition, the zooplankton of Lake Erhai have shifted to smaller species over time as temperature and eutrophication have increased, which implies that zooplankton succession to small cladocerans may be markedly accelerated under further climate change and the increased eutrophication that has been observed in recent decades.

The impact of fish predation and cyanobacteria on zooplankton size structure in 96 subtropical lakes.

Zooplankton are relatively small in size in the subtropical regions. This characteristic has been attributed to intense predation pressure, high nutrient loading and cyanobacterial biomass. To provide further information on the effect of predation and cyanobacteria on zooplankton size structure, we analyzed data from 96 shallow aquaculture lakes along the Yangtze River. Contrary to former studies, both principal components analysis and multiple regression analysis showed that the mean zooplankton size was positively related to fish yield. The studied lakes were grouped into three types, namely, natural fishing lakes with low nutrient loading (Type1), planktivorous fish-dominated lakes (Type 2), and eutrophic lakes with high cyanobacterial biomass (Type 3). A marked difference in zooplankton size structure was found among these groups. The greatest mean zooplankton size was observed in Type 2 lakes, but zooplankton density was the lowest. Zooplankton abundance was highest in Type 3 lakes and increased with increasing cyanobacterial biomass. Zooplankton mean size was negatively correlated with cyanobacterial biomass. No obvious trends were found in Type 1 lakes. These results were reflected by the normalized biomass size spectrum, which showed a unimodal shape with a peak at medium sizes in Type 2 lakes and a peak at small sizes in Type 3 lakes. These results indicated a relative increase in medium-sized and small-sized species in Types 2 and 3 lakes, respectively. Our results suggested that fish predation might have a negative effect on zooplankton abundance but a positive effect on zooplankton size structure. High cyanobacterial biomass most likely caused a decline in the zooplankton size and encouraged the proliferation of small zooplankton. We suggest that both planktivorous fish and cyanobacteria have substantial effects on the shaping of zooplankton community, particularly in the lakes in the eastern plain along the Yangtze River where aquaculture is widespread and nutrient loading is high.

[Canonical correspondence analysis between phytoplankton community and environmental factors in macrophtic lakes of the middle and lower reaches of Yangtze River].

The phytoplankton communities in 4 macrophtic lakes (Longgan Lake, Liangzi Lake, Futou Lake and Baoan Lake) in Middle-Lower Yangtze Plain were investigated in September 2011, and 7 phylum and 231 species of phytoplankton were detected in the waters. The results indicated that phytoplankton was mainly composed of Cyanophyta, Bacillariophyta and Chlorophyta. The four lakes were mesotrophic. And the main phytoplankton was Phormidium foveolarum, Synedra ulna, Phormidium tenu and Tribonema minus. The relationships between the distribution of phytoplankton and environmental factors in each sampling site were studies by canonical correspondence analysis. The results demonstrated that pH and Total phosphorus are the key factors for the distribution of phytoplankton communities in 4 typical macrophtic lakes in Middle-Lower Yangtze Plain.

Risk assessment of microcystins in silver carp (Hypophthalmichthys molitrix) from eight eutrophic lakes in China.

Bioaccumulation and risk assessment of microcystins (MCs) in muscle of silver carp (Hypophthalmichthys molitrix) from eight eutrophic lakes along the Yangtze River of China were examined by using liquid chromatography electrospray ionisation mass spectrometry. MCs contents in seston collected from these eutrophic lakes ranged from 0.02 to 21.7 µg/L. MCs concentrations in silver carp muscle samples varied from 0.014 to 0.036 µg/g DW with an average of 0.028 µg/g DW. The total length of silver carp showed a significant negative correlation with MCs concentrations in their muscle (r=-0.85, p<0.05), suggesting that MCs accumulation in silver carp muscle seems to be size dependent. EDI values of MCs in fish muscle from these eight eutrophic lakes varied from 0.0027 to 0.0071 µg/kg day, which was much lower than the TDI value of 0.04 µg/kg day previously established by WHO, indicating that it is safe to consume silver carp muscle from eutrophic lakes in China.

[Effects of large bio-manipulation fish pen on community structure of crustacean zooplankton in Meiliang Bay of Taihu Lake].

In 2005, a large bio-manipulation pen with the stock of silver carp and bighead carp was built to control the cyanobacterial bloom in Meiliang Bay of Taihu Lake. This paper investigated the seasonal variation of the community structure of crustacean zooplankton and the water quality within and outside the pen. There were no significant differences in the environmental parameters and phytoplankton biomass within and outside the pen. The species composition and seasonal dynamics of crustacean zooplankton within and outside the pen were similar, but the biomass of crustacean zooplankton was greatly suppressed by silver carp and bighead carp. The total crustacean zooplankton biomass and cladocerans biomass were significantly lower in the pen (P < 0.05). In general, silver carp and bighead carp exerted more pressure on cladoceran species than on copepod species. A distinct seasonal succession of crustacean zooplankton was observed in the Bay. Many crustacean species were only dominated in given seasons. Large-sized crustacean (mainly Daphnia sp. and Cyclops vicnus) dominated in winter and spring, while small-sized species (mainly Bosmina sp., Ceriodaphnia cornuta, and Limnoithona sinensis) dominated in summer and autumn. Canonical correspondence analysis showed that water transparency, temperature, and phytoplankton biomass were the most important factors affecting the seasonal succession of the crustacean.

Nephrotoxic effects from chronic toxic cyanobacterial blooms in fishes with different trophic levels in a large Chinese lake.

Physiological and biochemical responses in kidneys of fishes with different trophic levels to toxic cyanobacterial blooms were studied. We sampled four fishes: the phytoplanktivorous Hypophthalmichthys molitrix and Aristichthys nobilis, the omnivorous Carassius auratus, and the carnivorous Culter ilishaeformis. Alterations of the antioxidant (GSH) and the major antioxidant enzymes (CAT, SOD, GPx, GST) were monitored monthly. Catalase and glutathione S-transferase were significantly higher during blooms than before and after blooms. All fishes showed ultrastructural alterations during blooms, which mainly are inosculation of foot processes in epithelial cell of glomeruli and mitochondria swelling in the proximal tubules. The results suggested that kidney impairment from chronic exposure of toxic cyanobacterial blooms might be the first step, and then followed by hepatic failure. Compared with livers in terms of physiological status, the weaker antioxidant ability of kidney made it more susceptible to chronic MCs exposure, besides its effective accumulation of MC metabolites.

Factors affecting temporal and spatial variations of microcystins in Gonghu Bay of Lake Taihu, with potential risk of microcystin contamination to human health.

A field survey of the seasonal variation of microcystin (MC) concentration was performed in Gonghu Bay (a total of 15 sampling sites) of Lake Taihu from January to December 2008. Microcystis spp. biomass and intra-/extracellular MCs were significantly correlated with water temperature, suggesting the importance of temperature in cyanobacterial blooming in the lake. Higher MC concentration was found in summer and autumn, and peaks of Microcystis biomass and intra-/extracellular MC concentrations were all present in October. Spatially, risk of MCs was higher in littoral zones than in the pelagic area. There were significant correlations between N or P concentrations, and Microcystis biomass or MC content, suggesting that N and P levels affected MC production through influencing Microcystis biomass. Intra-/extracellular MCs and Microcystis biomass had negative exponential relationships with TN:TP, and the maximum values all occurred when TN:TP was <25. Multivariate analyses by PCCA indicated that intra- and extracellular MC concentrations had better correlations with biological factors (such as Microcystis biomass and chl-a) than with physicochemical factors. The maximum MC concentration reached up to 17 micrograms/L MC-LReq, considerably higher than the drinking water safety standard (1 micrograms/L) recommended by the WHO. So it is necessary to take measures to reduce the exposure risk of cyanobacterial toxins to human beings.

Antioxidant response in liver of the phytoplanktivorous bighead carp (Aristichthys nobilis) intraperitoneally-injected with extracted microcystins.

The worldwide occurrence of cyanobacterial blooms makes it necessary to perform environmental risk assessment procedures to monitor the effects of microcystins (MCs) on fish. Oxidative stress biomarkers are valuable tools in this regard. In the present study, phytoplanktivorous bighead carp (Aristichthys nobilis) were injected intraperitoneally (i.p.) with extracted MCs (mainly MC-RR and -LR) at two doses, 400 and 1,000 microg kg(-1) bw, and antioxidant responses of the liver as biomarkers of oxygen-mediated toxicity were studied at 1, 3, 12, 24 and 48 h after injection. Contents of reactive oxygen species (ROS) and activities of antioxidant enzymes [catalase (CAT), superoxide dismutase (SOD), glutathione peroxide (GPX), and glutathione reductase (GR)] as well as glutathione S-transferase (GST) in the liver in both dose groups showed a biphasic change with an increase at initial 3 h followed by a decrease after injection, owing to the roles of the antioxidant system in eliminating excessive ROS and regenerating glutathione (GSH). The increased GST was probably due to the high transcription of cytosolic GST alpha and rho, suggesting the importance of MCs detoxification by GSH pathway. The stable GSH levels in liver may be explained by the high basic GSH concentration in liver, and/or an increased GSH synthesis, suggesting a high ability to detoxify MCs and to release associated high oxidative pressure in phytoplantivorous fish.

Plasma biochemical responses of the planktivorous filter-feeding silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) to prolonged toxic cyanobacterial blooms in natural waters.

The planktivorous filter-feeding silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) are the attractive candidates for bio-control of plankton communities to eliminate odorous populations of cyanobacteria. However, few studies focused on the health of such fishes in natural water body with vigorous toxic blooms. Blood parameters are useful and sensitive for diagnosis of diseases and monitoring of the physiological status of fish exposed to toxicants. To evaluate the impact of toxic cyanobacterial blooms on the planktivorous fish, 12 serum chemistry variables were investigated in silver carp and bighead carp for 9 months, in a large net cage in Meiliang Bay, a hypereutrophic region of Lake Taihu. The results confirmed adverse effects of cyanobacterial blooms on two phytoplanktivorous fish, which mainly characterized with potential toxicogenomic effects and metabolism disorders in liver, and kidney dysfunction. In addition, cholestasis was intensively implied by distinct elevation of all four related biomarkers (ALP, GGT, DBIL, TBIL) in bighead carp. The combination of LDH, AST activities and DBIL, URIC contents for silver carp, and the combination of ALT, ALP activities and TBIL, DBIL, URIC concentrations for bighead carps were found to most strongly indicate toxic effects from cyanobacterial blooms in such fishes by a multivariate discriminant analysis.

Phenotypic plasticity in gut length in the planktivorous filter-feeding silver carp (Hypophthalmichthys molitrix).

Phenotypic plasticity widely exists in the external morphology of animals as well as the internal traits of organs. In the present study, we studied the gut length plasticity of planktivorous filter-feeding silver carp under different food resources in large-net cage experiments in Meiliang Bay of Lake Taihu in 2004 and 2005. There was a significant difference in stocking density between these 2 years. Under a low stocking density and abundant food resources, silver carp increased their energy intake by feeding on more zooplankton. Meanwhile, silver carp adjusted their gut length to match the digestive requirements of food when exposed to different food resources. In the main growth seasons (from April to October), silver carp significantly increased their relative gut length when feeding on more phytoplankton in 2005 (p < 0.01, 9.23 +/- 1.80 in 2004 and 10.77 +/- 2.05 in 2005, respectively). There was a nearly significant negative correlation between zooplankton proportion in the diet and the relative gut length when silver carp were stocked in a high density (p = 0.112). It appears that silver carp might have evolved plasticity to change their gut length rapidly to facilitate efficient utilization of food resources. Such resource polymorphisms in the gut may be a good indication of temporal adaptation to resource conditions. Our work provided field evidence for understanding the functional basis of resource polymorphisms and the evolution of phenotypic plasticity in planktivorous filter-feeding fish.

Field and laboratory studies on pathological and biochemical characterization of microcystin-induced liver and kidney damage in the phytoplanktivorous bighead carp.

Field and experimental studies were conducted to investigate pathological characterizations and biochemical responses in the liver and kidney of the phytoplanktivorous bighead carp after intraperitoneal (i.p.) administration of microcystins (MCs) and exposure to natural cyanobacterial blooms in Meiliang Bay, Lake Taihu. Bighead carp in field and laboratory studies showed a progressive recovery of structure and function in terms of histological, cellular, and biochemical features. In laboratory study, when fish were i.p. injected with extracted MCs at the doses of 200 and 500 microg MC-LReq/kg body weight, respectively, liver pathology in bighead carp was observed in a time dose-dependent manner within 24 h postinjection and characterized by disruption of liver structure, condensed cytoplasm, and the appearance of massive hepatocytes with karyopyknosis, karyorrhexis, and karyolysis. In comparison with previous studies on other fish, bighead carp in field study endured higher MC doses and longer-term exposure, but displayed less damage in the liver and kidney. Ultrastructural examination in the liver revealed the presence of lysosome proliferation, suggesting that bighead carp might eliminate or lessen cell damage caused by MCs through lysosome activation. Biochemically, sensitive responses in the antioxidant enzymes and higher basal glutathione concentrations might be responsible for their powerful resistance to MCs, suggesting that bighead carp can be used as biomanipulation fish to counteract cyanotoxin contamination.

In situ studies on physiological and biochemical responses of four fishes with different trophic levels to toxic cyanobacterial blooms in a large Chinese lake.

Physiological and biochemical responses of four fishes with different trophic levels to toxic cyanobacterial blooms were studied in a large net cage in Meiliang Bay, a hypereutrophic region of Lake Taihu. We sampled four fishes: the phytoplanktivorous Hypophthalmichthys molitrix and Aristichthys nobilis, the omnivorous Carassius auratus, and the carnivorous Culter ilishaeformis. Alterations of the antioxidant (GSH) and the major antioxidant enzymes (CAT, SOD, GPx, GST) in livers were monitored monthly, and the ultrastructures of livers were compared between the bloom and post-bloom periods. During the cyanobacterial blooms, the phytoplanktivorous fishes displayed only slight ultrastructural changes in liver, while the carnivorous fish presented the most serious injury as swollen endomembrane system and morphologically altered nuclei in hepatocytes. Biochemically, the phytoplanktivorous fishes possessed higher basal GSH concentrations and better correlations between the major antioxidant enzymes in liver, which might be responsible for their powerful resistance to MCs. This article provided physiological and toxicological evidences for the possible succession of fish communities following occurrence of toxic cyanobacterial blooms and also for the applicability of using phytoplanktivorous fish to counteract toxic cyanobacterial blooms in natural waters.

Sequential ultrastructural and biochemical changes induced in vivo by the hepatotoxic microcystins in liver of the phytoplanktivorous silver carp Hypophthalmichthys molitrix.

Up to now, in vivo studies on the toxic effects of microcystins (MCs) on the ultrastructures of fish liver have been very limited. The phytoplanktivorous silver carp was injected i.p. with extracted hepatotoxic microcystins (mainly MC-RR and -LR) at a dose of 1000 microg MC-LReq. kg(-1) body weight, showing a time-dependent ultrastructural change in liver as well as significant increases in enzyme activity of plasma alanine aminotransferase (ALT), aspartate aminotransferase (AST) and lactate dehydrogenase (LDH). We observed for the first time the occurrence of a large amount of activated secondary lysosomes, which might be an adaptive mechanism to eliminate or lessen cell damage caused by MCs through lysosome activation. Quantitative and qualitative determinations of MCs in the liver were conducted by HPLC and LC-MS2, respectively. MCs concentration in the liver reached the maximum (114.20 microg g(-1) dry weight) after 3 h post-injection, and then rapidly dropped to 7.57 microg g(-1) dry weight at 48 h, indicating a depuration of 99% accumulated MC-LReq. On the other hand, a decrease trend in glutathione (GSH) concentration was observed in the liver of silver carp while the activity of glutathione S-transferase (GST) increased significantly after injection. The high tolerance of silver carp to MCs might be due to the high basic GSH level in their liver, and/or an increased GSH synthesis.

[Effects of eutrophication on distribution and population density of Corbicula fluminea and Bellamya sp. in Chaohu Lake].

The investigation on the distribution an d population density of C. fluminea and Bellamya sp. in Chaohu Lake during September 2001 and September 2002 showed that in the west region of the lake where was seriously eutrophic, the density and biomass of C. fluminea were 5.1 ind. x m(-2) and 17.87 g x m(-2) in 2001, and 8.8 ind. x m(-2) and 47.29 g x m(-2) in 2002, while those of Bellamya sp. were 13.3 ind. x m(-2) and 45.45 g x m(-2) in 2001, and 3.8 ind. x m(-2) and 12.56 g x m(-2) in 2002, respectively. In the east region of the lake where was eutrophic, the density and biomass of C. fluminea were 23.8 ind. x m(-2) and 67.86 g x m(-2) in 2001, and 29.2 ind. x m(-2) and 96.18 g x m(-2) in 2002, while those of Bellamya sp. were 10.1 ind. x m(-2) and 32.00 g x m(-2) in 2001, and 9.4 ind. x m(-2) and 31.21 g x m(-2) in 2002, respectively. The density and biomass of C. fluminea and Bellamya sp. were declined with increasing eutrophication. In hypertrophic region, C. fluminea and Bellamya sp. were absent. The density and biomass of the two species were obviously higher in littoral than in pelagic region. The distribution type of C. fluminea was core-model, while that of Bellamya sp. was random. The correlation between the density and biomass of C. fluminea and Bellamya sp. and water depth was not significant (P > 0.05). The biomass of Bellamya sp. was negatively correlated with water TN (P < 0.01), NO3-N (P < 0.05), TP(P < 0.01) and PO4-P (P < 0.05), while that of C. fluminea only had a significantly negative correlation with PO4-P(P < 0.05). Compared with 1981, there was fewer C. fluminea in the lake nowadays. The effects of other environmental factors on the population distribution and growth of C. fluminea and Bellamya sp. were also discussed.

Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China.

This article reports the organ distribution and bioaccumulation of hepatotoxic microcystins (MCs) in freshwater fishes at different trophic levels from the large, shallow, eutrophic Lake Chaohu in September 2003, when there were heavy surface blooms of toxic cyanobacteria. Among all fish, intestines and blood had the highest average content of MC-RR + MC-LR (22.0 and 14.5 microg g(-1) DW, respectively), followed by liver, bile, and kidney (7.77, 6.32, and 5.81 microg g(-1) DW, respectively), whereas muscle had the least (1.81 microg g(-1) DW). MC content in muscle was highest in carnivorous fish (Culter ilishaeformis, 2.22 microg g(-1) DW) and omnivorous fish (Carassius auratus, 1.96 microg g(-1) DW) and was lowest in phytoplanktivorous fish (Hypophthalmichthys molitrix, 1.65 microg g(-1) DW) and herbivorous fish (Parabramis pekinensis 0.660 microg g(-1) DW). However, the amount of MC in the gut of H. molitrix (137 microg g(-1) DW) was more than 20 times that in the other fish (<6.50 microg g(-1) DW). The MCs showed a tendency to accumulate up the food chain, and piscivorous fish at the top of the food chain were at high risk of exposure to MCs in Lake Chaohu. Our study is the first to report MC concentrations in the bile and blood of wild fish. One hundred grams of fish muscle would contain 2.64-49.7 microg of MC-LR equivalent, or about 1.3-25 times the recommended tolerable daily intake of MC-LR by humans, indicating that fish are already severely contaminated by MCs and that the local authorities should warn the public of the risk of poisoning by eating the contaminated fish.

Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in a freshwater snail (Bellamya aeruginosa) from a large shallow, eutrophic lake of the subtropical China.

Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in a freshwater snail (Bellamya aeruginosa) were studied monthly in a large shallow, eutrophic lake of the subtropical China during June-November, 2003. Microcystins (MCs) were quantitatively determined by High-Performance Liquid Chromatography (HPLC) with a qualitative analysis by a Finnigan LC-MS system. On the average of the study period, hepatopancreas was the highest in MC contents (mean 4.14 and range 1.06-7.42 microg g(-1)DW), followed by digestive tracts (mean 1.69 and range 0.8-4.54 microg g(-1)DW) and gonad (mean 0.715 and range 0-2.62 microg g(-1)DW), whereas foot was the least (mean 0.01 and range 0-0.06 microg g(-1)DW). There was a positive correlation in MC contents between digestive tracts and hepatopancreas. A constantly higher MC content in hepatopancreas than in digestive tracts indicates a substantial bioaccumulation of MCs in the hepatopancreas of the snail. The average ratio of MC-LR/MC-RR showed a steady increase from digestive tracts (0.44) to hepatopancreas (0.63) and to gonad (0.96), suggesting that MC-LR was more resistant to degradation in the snail. Since most MCs were present in the hepatopancreas, digestive tracts and gonad with only a very small amount in the edible foot, the risk to human health may not be significant if these toxic parts are removed prior to snail consumption. However, the possible transference of toxins along food chains should not be a negligible concern.