Aquaculture 231 (2004) 327 – 336 www.elsevier.com/locate/aqua-online Behavioural role of zinc on primary productivity, plankton and growth of a freshwater teleost, $ Labeo rohita (Hamilton) S. Adhikari *, S. Ayyappan Central Institute of Freshwater Aquaculture, P.O. Kausalyaganga, Bhubaneswar-751002, India Received 27 September 2002; received in revised form 23 October 2003; accepted 27 October 2003Abstract The role of zinc in biological production at three levels of zinc treatments was investigated. Thethree treatment levels were 10, 20 and 30 kg ZnSO4/ha with each treatment using three different soilbases containing 0.45, 0.75 and 1.0 ppm diethylenetriamine pentaacetic acid (DTPA)-extractablezinc. All treatments showed an increase in both plankton and primary productivity ( p < 0.05) overcontrol (without zinc) and the maximum increase was at 10, 20 and 30 kg ZnSO4/ha for 1.0, 0.75 and0.45 ppm DTPA-extractable zinc, respectively. In the same experiment, Labeo rohita fingerlingswere stocked after 15 days of zinc treatment. All the treatments showed an increase in growth of fish( p < 0.05) as compared with the control. Overall, maximum growth was obtained in the 30 kgZnSO4/ha – 0.45 ppm DTPA-extractable zinc, second highest followed by 10 kg – 1.0 ppm, followedby third highest growth in the 20 kg – 0.75 ppm treatment. Zinc from the soil was fractionated into different forms and the distribution of various forms inthe soil was found in the order of water-soluble < organically bound < complexed < occluded < re-sidual. The major portion of total zinc in the soil existed in the residual form. The amount of water-soluble, exchangeable and complexed forms of zinc diminished due to plankton and fish removalwhile the addition of zinc to soil increased these three forms considerably. The contents of occludedand residual zinc in soil did not change due to plankton and fish growth or due to addition of zinc. $ A preliminary report of this work was presented in the Fifth Indian Fisheries Forum which was held atCentral Institute of Freshwater Aquaculture, Bhubaneswar, India, during 17 – 20 January, 2000. * Corresponding author. E-mail address: email@example.com (S. Adhikari).0044-8486/$ - see front matter D 2004 Published by Elsevier B.V.doi:10.1016/j.aquaculture.2003.10.038
328 S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336Water-soluble, organically bound and to a less extent, the exchangeable form of zinc principallycontributed to the pool of available zinc in this soil.D 2004 Published by Elsevier B.V.Keywords: Zinc; Diethylenetriamine pentaacetic acid; Labeo rohita1. Introduction The essential function of zinc for living organisms is based on its role as an integral partof a number of metalloenzymes and as a catalyst for regulating the activity of specific zinc-dependent enzymes such as carbonic anhydrase, alkaline phosphatase and alcoholdehydrogenase (Moore and Ramamoorthy, 1984). Over 300 proteins have been identifiedthat need zinc for their functions and the number is increasing (Vallee and Falchuk, 1993).The biological activities of these proteins include steps in the metabolism of nucleic acids,proteins, carbohydrates and fatty acids (Hogstrand and Wood, 1996). Zinc is a co-factorfor the enzyme carbonic anhydrase which catalyses a critical rate-limiting step for carbonuse in photosynthesis (Goldman and Horne, 1983). Goldman (1965) reported about thelimitation of plankton growth by zinc deficiency. Elder (1974) showed that chelated zincwas stimulatory to algal growth in Lake Tahoe. Similarly, response to variations inincreasing zinc concentrations were reported for the growth of many marine planktonspecies (Brand et al., 1983; Coale, 1991; Sunda and Huntsman, 1995). Wang and Guo(2000) also reported that colloidal metals like zinc are available to marine plankton andcould be actively involved in planktonic food webs. The application of fertilizer in fish ponds has many benefits. The inorganic nutrientsincrease the multiplication of plankton and to some extent zooplankton which leads tobetter growth and yield of compatible species of fish. While applying fertilizers to any fishpond, more emphasis is generally paid on their doses which are usually decided based ontheir inherent availability in bottom soil and water phase (Hickling, 1971; Chaudhuri et al.,1974, 1975; Boyd, 1984). However, plankton, the dominant flora of aquaculture ponds,absorbs nutrients from water. Plankton and other algae do not have root systems forextracting nutrients directly from the soil solution. Nutrients in pond soil dissolve in porewater and nutrients in pore water can diffuse into the overlying pond water where they canbe absorbed by algae (Boyd, 1995). In addition, metal nutrients tend to transfer from pondsoils to water at low pH and EH (redox potential) of soils (Morris, 1975; Jackson et al.,1993). Thus, it is evident that nature and properties of bottom soils play an important rolein fish pond fertilization programme (Mandal and Chattopadhyay, 1992). Widespread occurrence of zinc deficiency in agricultural soil has been reported fromdifferent parts of India. As much as 50% of agricultural soil analysed throughout India underthe All India Co-ordinated Research Project on Micronutrients in soils and plants has beenfound to be deficient in zinc (Takkar et al., 1987). To overcome such deficiency, zinc isusually applied as fertilizer in agriculture (Hazra and Mandal, 1996). However, informationregarding the role of zinc as fertilizer to encourage the growth and abundance of plankton inthe pond culture system which, in turn, helps in better growth of fish is non-existent.
S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336 329Therefore, the present investigation was made to find out the optimum dose of application ofzinc in freshwater fish ponds and to quantify various fractions of zinc and their contributionto the pool of available zinc in pond soils using Labeo rohita (Hamilton) as a test crop.2. Materials and methods The experiment was conducted in 36 outdoor cement cisterns (height Â length Âwidth = 1.0 Â 0.5 Â 0.3 m). Three types of soils having different DTPA-extractable(available) zinc content were chosen. The soils were collected from three different fishponds of three different sectors of the Institute’s fish farm, dried, powdered and spreaduniformly on the bottom of the cisterns to a thickness of about 15 cm. The soils had thefollowing characteristics:(A) Sandy loam texture, pH = 5.8, cation exchange capacity = 8.4 cmol (P+) kgÀ 1, organic carbon = 0.72%, total zinc = 111.4 ppm and diethylenetriamine pentaacetic acid (DTPA)-extractable (available) zinc = 1.0 ppm.(B) Sandy clay loam texture = pH 6.1, cation exchange capacity = 11.4 cmol (P+) kgÀ 1, organic carbon = 0.63%, total zinc = 124.6 ppm and DTPA-extractable zinc = 0.75 ppm.(C) Sandy loam texture = pH 6.4, cation exchange capacity = 10.6 cmol (P+) kgÀ 1, organic carbon = 0.80%, total zinc = 127.0 ppm and DTPA-extractable zinc = 0.45 ppm. The cisterns were then filled with water from the parent pond. One week was allowed toestablish the soil and water conditions before fertilization with the standard dose of N – P –K (200:100:40 kg haÀ 1) developed at the Institute. The treatment consisted of four levelsof zinc (0, 10, 20 and 30 kg ZnSO4Á7H2O/ha with three replications for each treatmentusing three different soil bases containing 0.45, 0.75 and 1.0 ppm DTPA-extractable zinc.The cisterns receiving no zinc served as controls. A constant water level of 85 cm wasmaintained throughout the experiment by periodic addition of pond water. Indian major carp, L. rohita (Hamilton) fingerlings prefer vegetable debris andmicroscopic plants, while adults prefer vegetable debris, microscopic plants, decayedhigher plants, detritus and mud as their food. The feeding habit of this fish is planktophageand they are predominantly column feeder (Jhingran, 1991). Therefore, L. rohita finger-lings were chosen for the present study as test carp. The fingerlings were collected from arearing pond of the Institute and acclimatized in outdoor conditions for 15 days prior totheir use in the experiment. After 15 days of zinc application, 10 acclimatised fingerlings(average length 83 mm and average weight 5.9 g for 1.0 ppm DTPA-extractable zinc;average length 71 mm and average weight 5.03 g for 0.75 ppm DTPA-extractable zinc andaverage length 78 mm and average weight 5.6 g for 0.45 ppm DTPA-extractable zincexperiment) were stocked in each outdoor cistern and their growth and yield were studiedfor 75 days out of the 90-day study. No artificial feed was provided during the growingperiod of the test carp. The physico-chemical characteristics of water were measured fortnightly following thestandard methods (APHA, 1989). The concentration of chlorophyll a, primary productiv-
330 S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336ity and plankton biomass in all the treatments for each type of soil were studied at 15-dayintervals. The concentration of chlorophyll a was studied spectrophotometrically afterfiltering a 10 ml of water sample through cellulose-nitrate membrane filter of 0.45 Am andafter extraction in acetone (Boyd, 1984). The primary productivity was assessed by thelight and dark bottle dissolved oxygen method (Vollenweider, 1974). Bottles were filledwith water taken from 0.25 and 0.50 m depths from the center of each cistern. Two lightand two dark bottles were resuspended at those depths beginning at 10.00 h. They wereleft in cisterns for 4 h. For plankton biomass estimation, a known volume of surface waterwas filtered through the plankton net made of bolting silk cloth (No. 25, 64 Am), dried inan oven, cooled in a desiccator, weighed and the results were expressed as g/10l (Vollenweider, 1974). At the end of the experiment, plankton and fish were harvested. The increase in weightof fish was computed in terms of yield in g/cistern/75 days. The plankton samples wereharvested from the surface waters of experimental cisterns by filtering 50 l of waterthrough a plankton net made of bolting silk cloth (No. 25, 64 Am). The harvested planktonand fish samples were first washed with tap water and then rinsed with distilled water. Theplankton and fish samples were dried at 70 and 500 jC, respectively, in a hot air oven. Thesoil samples collected after the harvest of fish were used for a zinc fractionation study.Fractionation of soil zinc was carried out according to the modified procedure of Smithand Shoukry (1968). Plankton, fish tissue and soil were digested separately by tri-aciddigestion for zinc estimation (Piper, 1950). For example, total zinc in fish tissue wasestimated by taking 0.5 –1.0 g of tissue and digesting with a mixture of concentrated nitricacid and perchloric acid in the ratio of 1:3 until the formation of a white residue. Thecooled residue was dissolved completely by adding 10 ml of 1 N hydrochloric acid andmade up to 25 ml with distilled water. The content was filtered by cotton wool and thefiltrate was subjected to zinc analysis. Plankton and soil were digested similarly. Zinccontent in the plankton and fish digestions and soil extracts were determined by atomicabsorption spectrophotometry (Perkin Elmer model number 1331) adopting suitablemeasuring conditions for zinc. All the results were subjected to statistical evaluation. One-way analysis of variance(ANOVA) with Duncan multiple range test (DMRT) was applied to find out the significantdifference among treatment means using SPSS software.3. Results and discussion The effect of zinc on primary productivity, chlorophyll a concentration and planktonbiomass are presented for the three different soil types in Table 1. The physico-chemicalcondition of water in these experiments (ranges) were as follows: pH (7.2 – 8.1), totalalkalinity (90 – 120 ppm as CaCO3), total hardness (75 – 110 ppm as CaCO3), totalammonia (0.01 – 0.03 ppm), soluble orthophosphate (0.03 –0.10 ppm) and dissolved zinc(42 – 263 Ag/1). All three zinc addition treatments in cisterns with sediments containing allthree levels of DTPA-extractable zinc showed an increase in primary productivity,chlorophyll a concentration and plankton biomass over fertilized controls (Table 1). For0.45 ppm DTPA-extractable zinc, 30 kg ZnSO4/ha treatment showed the maximum yield,
S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336 331Table 1Effect of zinc on primary productivity, chlorophyll a concentration and plankton biomassParameters DTPA-extractable Fertilizer control Fertilizer + 10 kg Fertilizer + 20 kg Fertilizer + 30 kg zinc (ppm) (N – P – K) ZnSO4/ha ZnSO4/ha ZnSO4/haGross primary 0.45 0.064 – 0.111 0.078 – 0.117 0.141 – 0.191 0.152 – 0.243 production (0.099)a (0.106)a (0.159)b (0.199)c (g C/m2/day)Chlorophyll a 63 – 92 71 – 111 69 – 37 101 – 153 concentration (75)k (90)k (110)l (128)m (Ag/l)Plankton 0.21p 0.32q 0.41q 0.50r biomass (g/10 l)Gross primary 0.75 0.081 – 0.111 0.094 – 0.124 0.159 – 0.225 0.135 – 0.165 production (0.099)a (0.114)a (0.187)b (0.148)c (g C/m2/day)Chlorophyll a 48 – 70 54 – 85 89 – 128 75 – 115 concentration (68)k (78)k (111.3)l (98.6)l (Ag/l)Plankton 0.16p 0.30q 0.46r 0.38q biomass (g/10 l)Gross primary 1.00 0.071 – 0.108 0.142 – 0.237 0.117 – 0.181 0.082 – 0.114 production (0.093)a (0.193)b (0.131)c (0.107)a (g C/m2/day)Chlorophyll a 60 – 90 92 – 140 73 – 124 65 – 96 concentration (71)k (121)l (109)l (81)k (Ag/l)Plankton 0.20p 0.52q 0.43q 0.33p biomass (g/10 l)Treatment means followed by the same superscript in a row were not significantly different ( p < 0.05).Figures in the parenthesis denote mean value.for 0.75 ppm DTPA-extractable zinc, 20 kg ZnSO4/ha treatment showed the maximumyield and for 1.0 ppm DTPA-extractable zinc, 10 kg ZnSO4/ha gave the maximum yieldover fertilized control in terms of primary productivity, chlorophyll a concentration andplankton biomass, and the other two treatments for all three types of soils showed anintermediate results. In all the experiments, fish yields increased for all the treatments (Table 2). However,the experiment with three different soils responded differently to the graded levels of zincfrom production point of view. Soils having 0.45 ppm DTPA-extractable zinc showed themaximum fish yield at 30 kg ZnSO4/ha treatment level while the soil having 1.0 ppmDTPA-extractable zinc gave the maximum fish yield at 10 kg ZnSO4/ha. Soils having 0.75ppm DTPA-extractable zinc showed the maximum yield at 20 kg ZnSO4/ha treatmentlevel. All the growth results were statistically significant ( p < 0.05). The lower yield for1.0 ppm DTPA-extractable zinc at 20 and 30 kg ZnSO4/ha may be due to greateravailability of dissolved zinc in the fish culture system which is responsible for decrease ingrowth and maximum size of the fish (Moore and Ramamoorthy, 1984). Zinc concentra-
332 S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336Table 2Response of L. rohita fingerlings and plankton to graded levels of zinc application in different soilsDTPA-extractable Zinc application Survivability Fish yield Zn Zn concentration Zn uptake Zn uptakezinc (ppm) (%) (g/cistern/75 concentration of plankton (Ag/fish) by plankton days) of fish (mg/kg (mg/kg dry weight) (Ag/cistern) dry weight)0.45 Fertilized control 90 69.0a 19.2k 28.0p 540 875 10 kg ZnSO4/ha 74.6a,b 20.8k,l 33.4p,q 2240 2801 20 kg ZnSO4/ha 80.5b 21.0k,l 38.6q 1800 3843 30 kg ZnSO4/ha 95.8c 22.8l 46.0r 1680 44280.75 Fertilized control 90 54.7a 21.7k 30.2p 450 788 10 kg ZnSO4/ha 76.0b 22.8k 38.4p,q 990 1692 20 kg ZnSO4/ha 88.3c 24.6k 44.7q 1620 3281 30 kg ZnSO4/ha 80.6b 23.8k 42.5q 1480 28321.00 Fertilized control 80 80.0a 23.5k 25.0p 501 887 10 kg ZnSO4/ha 91.7b 24.5k 30.2p 992 2190 20 kg ZnSO4/ha 87.3a 26.0k 42.4q 2080 4180 30 kg ZnSO4/ha 81.1a 26.0k 38.8r 2092 3742Treatment means followed by the same superscript in a column were not significantly different ( p < 0.05).
S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336 333tion in plankton ranged from 25.0 to 46.0 mg/kg dry weight. Trollope and Evans (1976)reported that residues of zinc in aquatic plants from uncontaminated parts of the world aregenerally below 50 mg/kg dry weight. Zinc uptake by plankton varied from 788 to 4428Ag/cistern. It may be mentioned here that uptake of zinc by plankton is generally slow anddepends on metabolic/photosynthetic rate, temperature, light, and the concentrations ofzinc in the environment (Harding and Whitton, 1981). Sorption of zinc is also suppressedby H+, chelators, Mg2 + and Na+ (Moore and Ramamoorthy, 1984). Skipnes et al. (1975)suggested that only a small fraction of uptake in living algae was due to ion exchange withintracellular polysaccharides. Zinc residues in the fish were lower than those found in plankton and theirconcentration varied from 19.2 to 26.0 mg/kg dry weight in the whole fish. The averagefish contains about 10– 40 mg zinc/kg wet weight, depending on species (Johnson, 1987;Spry et al., 1988; Shearer, 1984; Shearer et al., 1992). Zinc in muscle tissue from 15species of omnivorous and carnivorous fish collected from industrial and agricultural areasof the lower Great Lakes were 16– 82 and 3 – 9 mg/kg wet weight, respectively (Brownand Chow, 1977). Farmer et al. (1979) reported that zinc residues in Atlantic salmonvaried from 27 to 38 mg/kg. Soil (having 1.0 ppm DTPA-extractable zinc experiment) zinc fractions as influencedby plankton production and L. rohita fingerlings growth are presented in Table 3. The datareveals that the relative distribution of different forms of zinc in this soil was in the orderof water-soluble < exchangeable < organically bound < complexed < occluded < residualzinc. The above results suggest that a major portion of the total zinc in the studied soilexisted in the residual form, while the water-soluble zinc accounted for only tracequantities. Similar results were reported by Vasuki (1979) and Rosalind (1980) foragricultural soils. The effect of plankton production and L. rohita fingerling growth on depletion ofvarious pools of soil zinc (Table 3) suggest that water-soluble, exchangeable andcomplexed forms of zinc were slightly reduced due to plankton and fish removal, butother forms of zinc in the soil were not influenced. Soil zinc fractions were also influencedby the application of graded levels of zinc to soil. Water-soluble zinc in the soil did notincrease up to 10 ppm zinc level, but at higher levels of zinc, the increase wasproportionate and it was nearly double at 30 ppm zinc level. The contents of exchangeable,complexed and organically bound forms of zinc in soil increased progressively with theTable 3Soil zinc fractions as influenced by plankton and fish growth and levels of zinc application to the soil containing1.00 ppm DTPA-extractable zincSoil zinc fraction Initial level (ppm) Zinc level (kg/ha) 0 10 20 30Water-soluble 0.46 0.38 0.40 0.62 0.78Exchangeable 1.24 1.02 1.22 2.54 2.98Complexed 1.93 1.76 1.98 3.16 3.61Organically bound 1.91 1.90 1.84 3.32 3.73Occluded 2.24 2.36 2.42 2.46 2.44Residual 111.4 111.6 112.4 115.6 112.8
334 S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336Table 4Simple correlation coefficients (r) between zinc uptake and zinc fractions in soil for 1.0 ppm DTPA-extractablezincSoil Zn fraction Zinc uptake by: Fish PlanktonWater-soluble 0.639** 0.682**Exchangeable 0.573* 0.518*Complexed 0.497 0.517Organically bound 0.699** 0.672**Occluded 0.017 0.028Residual 0.089 0.102 * Significant at p < 0.05. ** Significant at p < 0.01.addition of increasing levels of zinc to soil and these forms were more than double at 30ppm zinc level. On the other hand, the contents of occluded and residual zinc in soil didnot change either due to plankton and fish growth or due to addition of zinc to soil. Theoccluded form of zinc in Oxisol is held mostly by sesquioxides and residual zinc is mainlyassociated with mineral fraction of the soil. The transformation of applied zinc to theseforms of zinc is a slow process. However, upon aging other forms of zinc get slowlytransformed into these forms which are relatively less soluble (Chandrashekhar andKedlaya, 1988). Similar results were reported by Vasuki (1979) and Edward Raja (1980). The correlation coefficients among different fractions of soil zinc (Table 4) suggest thatthe water-soluble and organically bound forms of zinc in soil were highly correlated( p < 0.01) with the uptake of zinc by both plankton and L. rohita fingerlings. Exchange-able form of zinc were also significantly correlated ( p < 0.05) with the uptake of zinc byfish fingerlings and plankton. The contribution of each fraction to the pool of availablezinc in this soil (having 1.00 ppm DTPA-extractable zinc) was in the following order:water-soluble < organically bound < exchangeable < complexed < occluded < residual.From the above results, it is evident that water-soluble and organically bound zinc arethe principal forms contributing to the pool of available zinc in this soil. The contributionof exchangeable zinc to the available pool was relatively less particularly for plankton.Since the soil of the present study is coarse textured, low in organic matter content and haslow cation exchange capacity (CEC), the contribution of exchangeable zinc to theavailable pool is limited. Similarly, the contribution of both the occluded and the residualforms of zinc to the available pool was very little. The findings of the investigationcorroborate those reported by Edward Raja (1980) and Rosalind (1980) for agriculturalrice soils.4. Conclusions From the foregoing discussion, it may be concluded that zinc application as fertilizer isbeneficial in pond aquaculture for better plankton and fish growth. The maximum growthwas observed in the 30 kg ZnSO4/ha – 0.45 ppm DTPA-extractable zinc, second highestfollowed by 10 kg –1.0 ppm, followed by third highest growth in the 20 kg– 0.75 ppm
S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336 335treatment. It may also be concluded that water-soluble, organically bound and to someextent exchangeable forms of zinc contribute to the pool of available zinc in theexperimental soil having 1.0 ppm DTPA-extractable zinc. It is therefore, necessary toinclude these forms of zinc in characterising the available zinc status of this soil. However,further research is necessary for zinc application as fertilizer under field conditions.Acknowledgements We are very much thankful to the reviewers for their helpful remarks.ReferencesAPHA, 1989. Standard Methods for the Examination of Water and Wastewater, 17th ed. American Public Health Association, Washington, DC.Boyd, C.E., 1984. Water Quality in Warmwater Fish Ponds. Auburn University, USA, p. 354.Boyd, C.E., 1995. Bottom Soils, Sediments and Pond Aquaculture. Chapman & Hall, New York, p. 348.Brand, L.E., Sunda, W.G., Guillard, R.R.L., 1983. Limitation of marine phytoplankton reproductive rates by zinc, manganese and iron. Limnology and Oceanography 28, 1182 – 1198.Brown, J.R., Chow, L.Y., 1977. Heavy metal concentrations in Ontario fish. Bulletin of Environmental Con- tamination and Toxicology 17, 190 – 195.Chandrashekhar, P., Kedlaya, N., 1988. Soil zinc fractions and their availability in Oxisol. Journal of the Indian Society of Soil Science 36, 487 – 491.Chaudhuri, H., Chakraborti, R.D., Rao, N.G.S., Janakiram, K., Chatterjee, D.K., Jena, S., 1974. Record fish production with intensive culture of Indian and exotic carps. Current Science 43, 303 – 304.Chaudhuri, H., Chakraborty, R.D., Sen, P.R., Rao, N.G.S., Jena, S., 1975. A new high in fish production in India with record yields by composite fish culture in freshwater ponds. Aquaculture 6, 343 – 355.Coale, K.H., 1991. Effects of iron, manganese, copper and zinc enrichments on productivity and biomass in the sub-arctic Pacific. Limnology and Oceanography 36, 1851 – 1864.Raja, E., 1980. PhD Thesis, University of Agricultural Sciences, Bangalore, India.Elder, J.F., 1974. Trace metals from ward creek and their influence upon phytoplankton growth in Lake Tahoe. PhD Thesis, University of California, Davis, pp. 144.Farmer, G.J., Ashifield, D., Samant, H.S., 1979. Effects of zinc on juvenile Atlantic salmon Salmon salar: acute toxicity, food intake, growth and bioaccumulation. Environmental Pollution 19, 103 – 117.Goldman, C.R., 1965. Micronutrient limiting factors and their detection in natural phytoplankton populations. In: Goldman, C.R. (Ed.), Primary Productivity in Aquatic Environments. Mem. 1st Ital. Idrobiol., vol. 18, pp. 121 – 135. Suppl.Goldman, C.R., Horne, A.J., 1983. Limnology. McGraw-Hill, New York, p. 464.Harding, J.P.C., Whitton, B.A., 1981. Accumulation of zinc, cadmium, and lead by field populations of Lamanea. Water Research 15, 301 – 319.Hazra, G.C., Mandal, B., 1996. Desorption of adsorbed zinc in soils in relation to soil properties. Journal of the Indian Society of Soil Science 44, 233 – 237.Hickling, C.F., 1971. Fish Culture. Faber and Faber, London, p. 225.Hogstrand, C., Wood, C.M., 1996. The physiology and toxicology of zinc in fish. In: Taylor, E.W. (Ed.), Toxicology of Aquatic Pollution: Physiological, Molecular and Cellular Approaches. Society for Experimen- tal Biology Seminar Series, vol. 57. Cambridge University Press, Great Britain, pp. 61 – 84.Jackson, L.J., Kalff, J., Rasmussen, J.B., 1993. Sediment pH and redox potential affect the bioavailability of Al, Cu, Fe, Mn and Zn to rooted aquatic macrophytes. Canadian Journal of Fisheries and Aquatic Sciences 50, 143 – 148.Jhingran, V.G., 1991. Fish and Fisheries of India. Hindustan Publishing, New Delhi, India, p. 727.
336 S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336Johnson, M.G., 1987. Trace element loadings to sediments of fourteen Ontario lakes and correlations with concentrations in fish. Canadian Journal of Fisheries and Aquatic Sciences 44, 3 – 13.Mandal, L.N., Chattopadhyay, G.N., 1992. Nutrient management in aquaculture. In: Tandon, H.L.S. (Ed.), Non- Traditional Sectors for Fertilizer Use. FDCO, New Delhi, pp. 1 – 17.Moore, J.W., Ramamoorthy, S., 1984. Heavy Metals in Natural Waters: Applied Monitoring and Impact Assess- ment Springer, New York. 268 pp.Morris, J.R., 1975. The Distribution of Heavy Metals and pH in the Surficial Sediments of Nelson Lake and Ecological Implications. Ont. Ministry of Natural Resources, Ottawa, p. 28.Piper, C.S., 1950. Soil and Plant Analysis. Interscience Publishers, New York.Rosalind, M., 1980. MSc (Ag) Thesis, University of Agricultural Sciences, Bangalore, India.Shearer, K.D., 1984. Changes in elemental composition of hatchery-reared rainbow trout, Salmo gairdneri, associated with growth and reproduction. Canadian Journal of Fisheries and Aquatic Sciences 41, 1592 – 1600.Shearer, K.D., Maage, A., Opstredt, J., Mundheim, H., 1992. Effects of high ash diets on growth, feed efficiency, and zinc status of juvenile Atlantic salmon (Salmo salar). Aquaculture 106, 345 – 355.Skipnes, O., Roald, T., Haug, A., 1975. Uptake of zinc and strontium by brown algae. Physiologia Plantarum 34, 314 – 320.Smith, R.L., Shoukry, K.S.M., 1968. Isotopes and Radiation in Soil Organic Matter Studies. IAEA, Viena, p. 397.Spry, D.J., Hodson, P.V., Wood, C.M., 1988. Relative contributions of dietary and water brone zinc in the rainbow trout, Salmo gairdneri. Canadian Journal of Fisheries and Aquatic Sciences 45, 32 – 41.Sunda, W.G., Huntsman, S.A., 1995. Cobalt and zinc interreplacement in marine phytoplankton: biological and geochemical implications. Limnology and Oceanography 40, 1404 – 1417.Takkar, P.N., Chhibba, I.M., Mehta, S.K., 1987. Twenty years of co-ordinated Research on Micronutrients in soils and plants (1967 – 1987). Indian Council of Agricultural Research, Indian Institute of Soil Science, Bhopal.Trollope, D.R., Evans, B., 1976. Concentrations of copper, iron, lead nickel and zinc in freshwater algal blooms. Environmental Pollution 11, 109 – 116.Vallee, B.L., Falchuk, K.H., 1993. The biochemical basis of zinc physiology. Physiological Reviews 73, 79 – 118.Vasuki, N., 1979. PhD Thesis, University of Agricultural Sciences, Bangalore, India.Vollenweider, R.A., 1974. A manual on methods of measuring primary production in aquatic environment, 2nd ed. IBP Handbook, vol. 12. Blackwell Scientific Publication, Oxford, p. 225.Wang, W.X., Guo, L., 2000. Bioavailability of colloid-bound Cd, Cr and Zn to marine plankton. Marine Ecology Progress Series, vol. 202. Inter-Research Science Publisher, Oldendorf/Luhe, pp. 41 – 49.