Article

Gut contents of bighead carp Aristichthys nobilis and the processing and digestion of algal cells in the alimentary canal

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  • Institute of Hydrobiology Chinese Academy of Sciences
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Abstract

Bighead carp is one of the most important freshwater filter-feeding fish of Chinese aquaculture. In recent decades, there have been a number of contradictory conclusions on the digestibility of algae by bighead carp based on the results from gut contents and digestive enzyme analysis or Ž radiolabelled isotope techniques. Phytoplankton in the gut contents of bighead carp cultured in a. large net cage in Lake Donghu were studied during March-May. In biomass, the dominant Ž phytoplankters in the fore-gut contents were the centric diatom Cyclotella average 54.5%, range. Ž. 33.8-74.3% and the dinoflagellate Cryptomonas average 22.8%, range 6.8-55.8%. Phytoplank-ton in water samples were generally present in proportionate amounts in samples from the fore-guts of bighead carp. The size of most phytoplankton present in the intestine of bighead carp Ž was between 8 and 20 mm in length. Bighead carp was also able to collect particles as small as. 5-6 mm much smaller than their filtering net meshes, suggesting the importance of mucus in collecting small particles. Examination of the change in the integrity of Cyclotella on passage through the esophagus of bighead carp indicated that disruption of the algal cell walls is principally by the pharyngeal teeth, explaining the previous contradictory conclusions. q 2001 Elsevier Science B.V. All rights reserved. P. Xie. 0044-8486r01r$-see front matter q 2001 Elsevier Science B.V. All rights reserved. Ž. PII: S 0 0 4 4-8 4 8 6 0 0 0 0 5 4 9-4 () P. Xie r Aquaculture 195 2001 149-161 150

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... Other researchers found that planktivorous carps reduce zooplankton biomass and even increase phytoplankton biomass, presenting results predicted by studies on traditional biomanipulation (Yi et al. 2016a, Shen et al. 2021. The effectiveness of stocking with bighead carps in lakes and reservoirs has been questioned because bighead carps predominantly feed on zooplankton (Cremer and Smitherman 1980;Burke et al. 1986;Dong and Li 1994;Li et al. 2018a) and silver carp mainly feed on phytoplankton (Xie 2003), although bighead carps are effective biological control agents for algal blooms (Cremer and Smitherman 1980;Xie 2001) and played an important role in the trophic dynamics of aquatic ecosystems during top-down and bottom-up processes (Carpenter et al. 1992;Schindler et al. 2001;Jeppesen et al. 2010). The view that bighead carps are ineffective algal control agents is supported by the fact that the mesh size of the gill raker of a bighead carp (with a relatively wide spacing of less than 20 μm) is considerably larger than that of a silver carp (with filtering particles of less than 12 μm (Opuszynski and Shireman 1993;Vörös 2000). ...
... The view that bighead carps are ineffective algal control agents is supported by the fact that the mesh size of the gill raker of a bighead carp (with a relatively wide spacing of less than 20 μm) is considerably larger than that of a silver carp (with filtering particles of less than 12 μm (Opuszynski and Shireman 1993;Vörös 2000). However, evidence of the successful use of bighead carps in manipulation has been presented as well (Xie 1999(Xie , 2001Ke et al. 2007;Chen et al. 2011;Jayasinghe et al. 2015;Nistor et al. 2018). ...
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It is a common practice to improve the water environment of rivers and lakes in China by the enhancement and releasing (EAR) of silver carp (Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis) for biomanipulation. However, the quantity of bighead carp and its effect on water quality and plankton community have been the focus of debate among ecologists. Herein, in order to more accurately simulate the environmental conditions of lakes, we selected earthen ponds with large areas adjacent to Lake Qiandao from May to August in 2016 to study the responses of water quality condition and plankton community to a gradient of bighead carp stocked alone. Experimental groups with different densities of carp stocked were set as follows: 12.1 (LF), 23.5 (MF), and 32.5 g/m³ (HF), and a control group with no fish (NF). Results showed that total phosphorus (TP) in the fish-containing groups considerably decreased, and the lowest chlorophyll-a concentration (chl-a) was detected in the MF group. The biomass accumulation of the crustacean zooplankton was suppressed after carp was introduced, but the diversity, richness, and evenness of the crustacean zooplankton were weakly affected, except in the HF group. Phytoplankton biomass especially that of cyanobacteria was grazed rapidly by fish in the MF and HF groups and biodiversity indices were considerably increased in the fish-containing groups, especially in the late stages of the experiment. At a fish stocking density of 23.5–38.8 g/m³, the highest efficiency in controlling cyanobacteria and promoting water condition was achieved, and the impact on zooplankton diversity was weak. Our results indicated that bighead carp can be included in the EAR of lakes and reservoirs, but the optimal density of bighead carp stocking should be carefully considered.
... Among all phyla, especially Cyanobacteria, it is considered to be directly consumed by filter-feeding fish [60]. As a filter-feeding planktivorous carp, bighead carp easily filter some colony-forming cyanobacteria [27,61,62]. The abundance of Cyanobacteria in the hindgut was significantly higher in NC than in the other two groups (Additional file 1: Fig S1C), possibly due to differences in food sources in the three culture systems. ...
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Background The gut microbiota of fish confers various effects on the host, including health, nutrition, metabolism, feeding behaviour, and immune response. Environment significantly impacts the community structure of fish gut microbiota. However, there is a lack of comprehensive research on the gut microbiota of bighead carp in culture systems. To demonstrate the impact of culture systems on the gut microbiome and metabolome in bighead carp and investigate a potential relationship between fish muscle quality and gut microbiota, we conducted a study using 16S ribosomal ribonucleic acid sequencing, gas chromatography-mass spectrometry, and liquid chromatography-mass spectrometry techniques on bighead carp in three culture systems. Results Our study revealed significant differences in gut microbial communities and metabolic profiles among the three culture systems. We also observed conspicuous changes in muscle structure. The reservoir had higher gut microbiota diversity indices than the pond and lake. We detected significant differences in phyla and genera, such as Fusobacteria, Firmicutes, and Cyanobacteria at the phylum level, Clostridium sensu stricto 1, Macellibacteroides, Blvii28 wastewater sludge group at the genus level. Multivariate statistical models, including principal component analysis and orthogonal projections to latent structures-discriminant analysis, indicated significant differences in the metabolic profiles. Key metabolites were significantly enriched in metabolic pathways involved in "arginine biosynthesis" and "glycine, serine, and threonine metabolism". Variation partitioning analysis revealed that environmental factors, such as pH, ammonium nitrogen, and dissolved oxygen, were the primary drivers of differences in microbial communities. Conclusions Our findings demonstrate that the culture system significantly impacted the gut microbiota of bighead carp, resulting in differences in community structure, abundance, and potential metabolic functions, and altered the host's gut metabolism, especially in pathways related to amino acid metabolism. These differences were influenced substantially by environmental factors. Based on our study, we discussed the potential mechanisms by which gut microbes affect muscle quality. Overall, our study contributes to our understanding of the gut microbiota of bighead carp under different culture systems.
... While these items may require initial forceful grasping or prying actions by the oral jaws, afterwards the pharyngeal jaws do the heavy lifting of prey processing. For example, the pharyngeal jaws may engage in the prolonged and oscillating generation of force necessary to grind and rupture algae cells, thereby facilitating their digestion (Xie 2001;Carr et al. 2006) or generate acute bouts of sufficient force to crush mollusk shells (Hulsey 2006;Hulsey et al. 2008). The asymmetry in the utility of the pharyngeal jaws at the extremes of the velocity-force trade-off likely has broad macroevolutionary consequences. ...
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Trade-offs are thought to bias evolution and are core features of many anatomical systems. Therefore, trade-offs may have far-reaching macroevolutionary consequences, including patterns of morphological, functional, and ecological diversity. Jaws, like many complex anatomical systems, are comprised of elements involved in biomechanical trade-offs. We test the impact of a core mechanical trade-off, transmission of velocity versus force (i.e., mechanical advantage), on rates of jaw evolution in Neotropical cichlids. Across 130 species representing a wide array of feeding ecologies, we find that the velocity-force trade-off impacts evolution of the surrounding jaw system. Specifically, rates of jaw evolution are faster at functional extremes than in more functionally intermediate or unspecialized jaws. Yet, surprisingly, the effect on jaw evolution is uneven across the extremes of the velocity-force continuum. Rates of jaw evolution are 4 to 10-fold faster in velocity-modified jaws, whereas force-modified jaws are 7 to 18-fold faster, compared to unspecialized jaws, depending on the extent of specialization. Further, we find that a more extreme mechanical trade-off resulted in faster rates of jaw evolution. The velocity-force trade-off reflects a gradient from specialization on capture-intensive (e.g., evasive or buried) to processing-intensive prey (e.g., attached or shelled), respectively. The velocity extreme of the trade-off is characterized by large magnitudes of trait change leading to functionally divergent specialists and ecological stasis. By contrast, the force extreme of the trade-off is characterized by enhanced ecological lability made possible by phenotypes more readily co-opted for different feeding ecologies. This asymmetry of macroevolutionary outcomes along each extreme is likely the result of an enhanced utility of the pharyngeal jaw system as force-modified oral jaws are adapted for prey that require intensive processing (e.g., algae, detritus, and molluscs). The velocity-force trade-off, a fundamental feature of many anatomical systems, promotes rapid phenotypic evolution of the surrounding jaw system in a canonical continental adaptive radiation. Considering that the velocity-force trade-off is an inherent feature of all jaw systems that involve a lower element that rotates at a joint, spanning the vast majority of vertebrates, our results may be widely applicable across the tree of life. [adaptive radiation; constraint; decoupling; jaws; macroevolution; specialization]
... Pharyngeal jaws have mostly been recognized for their role in grinding algae (Xie 2001;Carr et al. 2006) and crushing mollusk shells (Wainwright 2005;Hulsey 2006;Hulsey et al. 2008). Although some fish crush mollusks with the oral jaws (e.g., tetraodontiforms and sheepshead ;Palmer 1979;Norton 1988;Fernandez and Motta 1997;Friel and Wainwright 1999) or puncture shells with adaptations on the neurocranium (Norton 1988), most fishes do so with the pharyngeal jaws (Wainwright 2005). ...
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Synopsis Ray-finned fishes have two jaw systems, the oral and pharyngeal jaws, which perform functions associated with prey capture and processing, respectively. The structural independence of the jaw systems is recognized as having broad implications for the functional and ecological diversity of the radiation. Cichlids (and a few other lineages) possess a modified pharyngeal jaw system that enhances prey processing versatility and capacity. This innovation, pharyngognathy, is hypothesized to have freed the oral jaws to diversify in terms of prey capture. We test the relative role of prey capture properties (e.g., evasiveness) and prey processing (e.g., crushing) in driving divergent selection in the oral and pharyngeal jaws using a macroevolutionary model fitting framework. Evolutionary outcomes were asymmetric. All transitions between different properties of prey capture had a corresponding transition in properties of prey processing. In contrast, fewer than half the transitions in the properties of prey processing had a corresponding prey capture transition. This discrepancy was further highlighted by multi-peak models that reflect the opposing function of each jaw system, which fit better than null models for oral jaw traits, but not pharyngeal jaw traits. These results suggest that pharyngeal jaw function can change independently from the function of the oral jaws, but not vice versa. This finding highlights the possibility of ecological limits to the evolutionary decoupling of jaw systems. The independent actions of prey capture and processing may be decoupled, but their respective functional demands (and evolution) are not. Therefore, prey likely impose some degree of coordinated evolution between acquisition and processing functional morphology, even in decoupled jaw systems.
... The filter feeding fish are especially significant to humans because of their role in aquatic ecosystems as direct consumers of phytoplankton, including large amounts of toxic blue-green algae which may contain high concentrations of MCs, their importance as a food fish, and their potential for biological management of cyanobacterial blooms [18]. Although its natural range is in the lowland rivers and shallow lakes of China [19], since bighead carp has been introduced worldwide, primarily for the purpose of cyanobacterial blooms control in hypereutrophic lakes [20]. Previous studies suggested that in the gut MCs content generally showed a reversed pattern: content was highest in the phytoplanktivorous fish, followed by the omnivorous and carnivorous fish. ...
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Cyanobacterial blooms, occurring frequently in eutrophic freshwaters worldwide, are considered as potential hazards to ecosystems and human health, and it is often difficult and expensive to control their outbreaks in large lakes through reduction of nutrient loadings. Biomanipulation, launched as an ecology-based solution in the 1970s, was once believed to be an effective way to counteract cyanobacterial blooms. It is divided into traditional biomanipulation (TB) and nontraditional biomanipulation (NTB) that use filter-feeding Daphnia and filter-feeding fish, respectively. There have been numerous reviews on the former, yet few on the latter. Here, we first revisit the debate on the digestibility of cyanobacteria in silver and bighead carp. Then, we review 42 experiments that clearly mention cyanobacterial changes and reveal substantial reductions in cyanobacterial abundance by filter-feeding carp in 88% of the cases. In particular, in a whole-lake experiment in Lake Donghu, increased stock of silver and bighead carp effectively decreased Microcystis blooms from a coverage of 87% in 2021 to 0% in 2022. Finally, we discuss possible factors related to NTB’s effectiveness that depends not only on standing stock, niche divergence and shape preference of the fish but also on trophic status of the waterbodies. Particularly, silver and bighead carp feed more effectively on colony-forming Microcystis than on filamentous cyanobacteria, but are capable of increasing small-sized algae. NTB can be used to prevent or diminish cyanobacterial blooms that are poorly grazed by Daphnia, providing an effective and sustainable in-lake ecotechnology to combat heavy cyanobacterial blooms in eutrophic waterbodies.
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The hypertrophic subtropic Donghu Lake's dense water bloom (of mainlyMicrocystis, Anabaena andOscillatoria) that occurred annually from the beginning of the 1970s, has disappeared since 1985. The influence of planktivorous fishes (silver and bighead carps) on the water bloom was studied for three years using the enclosure method. The enclosures stocked densely with bighead and/or silver carp were free of water bloom during the experimental period. The water bloom that appeared in the fish-free enclosures was completely eliminated in 10–20 days by introduction of silver and/or bighead carp(grass carp was not effective in controlling water bloom). This study showed clearly that grazing pressure by planktivorous fishes is a key factor in eliminating water bloom from the lake.
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The changes of L. kindti density from 1957 to 1996 were studied in a shallow, eutrophic Chinese lake, Lake Donghu. Despite the fact that the fish yield of planktivorous fish (silver carp and bighead carp) has increased steadily, the population density of L. kindti has also increased since 1957 and peaked in 1982/1983. The increase of both fish and L. kindti densities during this period may have benefitted from a considerable increase in the densities of their zooplankton prey, and fish predation on L. kindti might have been minor. As the fish yield increased further, their predation began to suppress most zooplankton prey including L. kindti. The largely increased fish predation on L. kindti is also evidenced by the remarkable decline of their body length after 1984. The density of L. kindti was significantly higher at the pelagic station (II) than at the littoral station (I), although for L. kindti, the littoral zone was significantly more resource profitable than the pelagic zone. The gradient of fish predation (more fish in the littoral zone) is the most likely explanation, since L. kindti is reported to be a preferred prey for many planktivorous fishes The maximum density of L. kindti was 1.78 ind./l (on Aug. 17, 1984) at Station I and 1.55 ind./l (on Sep. 13, 1985) at Station II, respectively, which are close to those in several other eutrophic lakes.
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On the basis of fishery results and food analyses of the silver carp, Hypophthalmichthys molitrix, and of the bighead carp, Aristichthys nobilis, it was found that the latter species is less useful for intensive rearing in ponds jointly with the common carp. Although the bighead carp, due to its rapid growth rate, gave a higher level of production than the silver carp at the same stocking densities, the drop in common carp production with bighead was so considerable that there are doubts as to the usefulness of joint rearing of the two species in ponds.Comparisons of the amount and composition of food of the silver carp and the bighead carp lead to the conclusion that food competition of the latter species with respect to the common carp is considerably greater. Although neither silver carp nor bighead carp consumed feed given to the common carp (sorghum), and detritus was the main dietary component of the two former species of fish, the proportion of invertebrates in the food of bighead carp was greater and the components more similar to the food of the common carp. The silver carp consumed smaller zooplankton species, mainly Bosmina longirostris and rotifers, which were of no significance as food for the common carp. The bighead carp consumed large Cladocera and Copepoda species, and also Tendipedidae larvae, i.e. organisms constituting the basic component of the food of common carp.
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Bighead carp is one of the most important freshwater filter-feeding fish of Chinese aquaculture. In recent decades, there have been a number of contradictory conclusions on the digestibility of algae by bighead carp based on the results from gut contents and digestive enzyme analysis or radiolabelled isotope techniques. Phytoplankton in the gut contents of bighead carp (cultured in a large net cage in Lake Donghu) were studied during March–May. In biomass, the dominant phytoplankters in the fore-gut contents were the centric diatom Cyclotella (average 54.5%, range 33.8–74.3%) and the dinoflagellate Cryptomonas (average 22.8%, range 6.8–55.8%). Phytoplankton in water samples were generally present in proportionate amounts in samples from the fore-guts of bighead carp. The size of most phytoplankton present in the intestine of bighead carp was between 8 and 20 μm in length. Bighead carp was also able to collect particles (as small as 5–6 μm) much smaller than their filtering net meshes, suggesting the importance of mucus in collecting small particles. Examination of the change in the integrity of Cyclotella on passage through the esophagus of bighead carp indicated that disruption of the algal cell walls is principally by the pharyngeal teeth, explaining the previous contradictory conclusions.
Article
The digestibility of algae by stomachless filter-feeding fish has been debated for decades. Results from gut contents and digestive enzyme analysis suggest poor utilization, while the measurement of food assimilation using radiolabeled isotope techniques indicate reasonable assimilation efficiency. Phytoplankton in the gut contents of the planktivorous filter-feeding silver carp were studied during March–May. The fish were cultured in a large net cage in a shallow, hypertrophic subtropical Chinese lake, Lake Donghu. In terms of biomass, the dominant phytoplankton in the fore-gut contents were Cyclotella (average 77.8%, range 69.7–93.5%) and Cryptomonas (average 9.57%, range 0–20.4%). The Ivlev's electivity index E of silver carp was much higher for Cyclotella (1.54) than for Cryptomonas (0.56). The majority of the phytoplankton found in the intestines of silver carp were 8–20 μm, but they were also able to collect particles as small as 4.5–10 μm, smaller than their filtering net meshes, suggesting that the secretion of mucus may play an important role in collecting such small particles. We conclude that disruption of cell walls is principally by the pharyngeal teeth, explaining previous contradictory conclusions.
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A strong correlation between fish yields and gross photosynthesis by phytoplankton occurs for the lakes and ponds along the Yangtze River, near Wuhan, China. Gross photosynthesis is calculated as the difference in oxygen concentration between light and dark bottles and incorporates respiration by heterotrophic and autotrophic plankton. Among the eighteen waters included in this analysis, net fish yields (total harvest minus weight of stocked juveniles) range from 59 to 14,586 kg (fresh weight) hectare−1·year−1. Two planktivorous fishes, silver carp Hypophthalmichthys molitrix and bighead carp Aristichthys nobilis constitute the majority of the stocked fish. The regression equation describing the relation between net fish yields (FYn) and gross photosynthesis (PGv, mg O2 liter−1·day−1) measured at one subsurface depth is log10 FYn = 0.047PGv + 2.44; N = 18; r2 = 0.76; P < 0.001.
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Food of sterile triploid bighead carp, Hypophthalmichthys nobilis, was examined in ponds receiving water from a hypereutrophic take in Florida. No distinctive seasonal changes in food composition were found. The fish fed selectively on Botryococcus braunii Kuetzing, a large nuisance algal species, which constituted 61% of the volume and 50% of the dry weight of the food. Zooplankton was highly selected, but constituted only 3% of the food volume because of the low zooplankton density in the ponds. The remaining proportion of food consisted mainly of blue-green algae. Final fish biomass was low, ranging from 60 to 97 kg ha−1 in individual ponds. Low biomass was due to slow fish growth and high fish mortality. Despite low biomass, the fish lowered the ratio of blue-green/green algae in the ponds and tended to lower phyto- and zooplankton abundance.
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Activities of digestive enzymes (trypsin and amylase) of microplanktophagous silver carp, Hypophthalmichthys molitrix, and macroplanktophagous bighead carp, Aristichthys nobilis, were investigated in relation to pH in 10 different segments of the gut. In addition, the possible existence of ‘classical’ lysozyme in both species and cellulase in silver carp were scrutinized, but no activities were detected. Tryptic and amylolytic activities decreased sharply from fore-gut to hind-gut indicating an efficient reabsorption mechanism. Trypsin and amylase of both species had a pH optimum at 8.3 and 7.0 respectively. The relatively low pH of 6.4 in the fore-gut of silver carp did not support an efficient operation of these enzymes, which was compensated by a higher enzyme concentration as compared to bighead carp. The latter, however, showed a higher pH of 7.3 in the fore-gut and thereby maintained similar activities as silver carp. The distinction of herbivorous and omnivorous fish in terms of digestion mechanisms is discussed.
Article
Natural food components were analysed for six species of fish grown in nine polyculture ponds. The ponds were stocked with common carp (Cyprinus carpio L.), tilapia hybrids (Sarotherodon (Oreochromis) niloticus L. × S. (O.) aureus Steindachner), grass carp (Ctenopharyngodon idella Val), and either silver carp (Hypophthalmichthys molitrix Val.) or bighead carp (Aristichthys nobilis Rich.) or their inter-specific hybrid. The natural food examined and defined was collected both from the guts of fish sampled and from pond water. The proportional amount of phytoplankton found in the guts of silver carp, bighead carp and their hybrid was 88–95%, 0–2% and 28–55%, respectively. The parallel zooplankton values were 4–7%, 75–95% and 32–63%. In ponds stocked with silver carp, bighead carp and their hybrid, the proportional amount of phytoplankton in the pond water was 12–33%, 54–99% and 17–77% respectively. This demonstrates empirically the inverse relationship between the type of plankton preferentially consumed by a given fish and the predominant plankton type present in ponds stocked with that fish.The mechanism of this preferential feeding is presumably associated with the diameter of the filtering net meshes of the gills of these fishes: 36 μm in silver carp, 84 μm in bighead carp and 56 μm in their hybrid.
Article
Analysis of intestinal contents of silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) showed that silver carp consumed primarily phytoplankton while bighead carp consumed large quantities of zooplankton and detritus in addition to phytoplankton. The size of particles filtered by the bighead carp was larger (17–3,000 μm) than that filtered by silver carp (8–100 μm). Artificial feed was readily consumed by bighead carp but not by silver carp. No growth difference was indicated for silver carp in fertilized ponds and ponds receiving artificial feed. Growth of bighead carp increased substantially with the addition of artificial feed. Silver carp grew more rapidly in cages than bighead carp.
Article
Stocking of ponds with planktivorous carps in polyculture with channel catfish (Ictalurus punctatus and a hybrid) reduced the density of zooplankton when compared to controls. Bighead (Aristichthys nobilis) and silver carp (Hypophthalmichthys molitrix) similarly reduced zooplankton, though the mechanism of suppression may be different. Phytoplankton biomass was significantly higher in ponds containing bighead and silver carp. Ammonia and nitrite concentrations were similar in bighead and silver carp ponds and were significantly lower than in control ponds.
Food habit analysis of silver carp and bighead carp stocked in Lake Donghu
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