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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 2003

Abstract

The role of zinc in biological production at three levels of zinc treatments was investigated. The
three treatment levels were 10, 20 and 30 kg ZnSO4/ha with each treatment using three different soil
bases containing 0.45, 0.75 and 1.0 ppm diethylenetriamine pentaacetic acid (DTPA)-extractable
zinc. All treatments showed an increase in both plankton and primary productivity ( p < 0.05) over
control (without zinc) and the maximum increase was at 10, 20 and 30 kg ZnSO4/ha for 1.0, 0.75 and
0.45 ppm DTPA-extractable zinc, respectively. In the same experiment, Labeo rohita fingerlings
were 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 kg
ZnSO4/ha – 0.45 ppm DTPA-extractable zinc, second highest followed by 10 kg – 1.0 ppm, followed
by 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 in
the 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 removal
while the addition of zinc to soil increased these three forms considerably. The contents of occluded
and 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 at
Central Institute of Freshwater Aquaculture, Bhubaneswar, India, during 17 – 20 January, 2000.
* Corresponding author.
E-mail address: sadhikari66@indiatimes.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) 327–336

Water-soluble, organically bound and to a less extent, the exchangeable form of zinc principally
contributed to the pool of available zinc in this soil.
D 2004 Published by Elsevier B.V.

Keywords: Zinc; Diethylenetriamine pentaacetic acid; Labeo rohita

1. Introduction

The essential function of zinc for living organisms is based on its role as an integral part
of a number of metalloenzymes and as a catalyst for regulating the activity of specific zinc-
dependent enzymes such as carbonic anhydrase, alkaline phosphatase and alcohol
dehydrogenase (Moore and Ramamoorthy, 1984). Over 300 proteins have been identified
that 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-factor
for the enzyme carbonic anhydrase which catalyses a critical rate-limiting step for carbon
use in photosynthesis (Goldman and Horne, 1983). Goldman (1965) reported about the
limitation of plankton growth by zinc deficiency. Elder (1974) showed that chelated zinc
was stimulatory to algal growth in Lake Tahoe. Similarly, response to variations in
increasing zinc concentrations were reported for the growth of many marine plankton
species (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 and
could be actively involved in planktonic food webs.
The application of fertilizer in fish ponds has many benefits. The inorganic nutrients
increase the multiplication of plankton and to some extent zooplankton which leads to
better growth and yield of compatible species of fish. While applying fertilizers to any fish
pond, more emphasis is generally paid on their doses which are usually decided based on
their 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 for
extracting nutrients directly from the soil solution. Nutrients in pond soil dissolve in pore
water and nutrients in pore water can diffuse into the overlying pond water where they can
be absorbed by algae (Boyd, 1995). In addition, metal nutrients tend to transfer from pond
soils 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 role
in fish pond fertilization programme (Mandal and Chattopadhyay, 1992).
Widespread occurrence of zinc deficiency in agricultural soil has been reported from
different parts of India. As much as 50% of agricultural soil analysed throughout India under
the All India Co-ordinated Research Project on Micronutrients in soils and plants has been
found to be deficient in zinc (Takkar et al., 1987). To overcome such deficiency, zinc is
usually applied as fertilizer in agriculture (Hazra and Mandal, 1996). However, information
regarding the role of zinc as fertilizer to encourage the growth and abundance of plankton in
the pond culture system which, in turn, helps in better growth of fish is non-existent.

S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336 329

Therefore, the present investigation was made to find out the optimum dose of application of
zinc in freshwater fish ponds and to quantify various fractions of zinc and their contribution
to 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 Â
width = 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 fish
ponds of three different sectors of the Institute’s fish farm, dried, powdered and spread
uniformly on the bottom of the cisterns to a thickness of about 15 cm. The soils had the
following 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 to
establish 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 levels
of zinc (0, 10, 20 and 30 kg ZnSO4Á7H2O/ha with three replications for each treatment
using 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 was
maintained throughout the experiment by periodic addition of pond water.
Indian major carp, L. rohita (Hamilton) fingerlings prefer vegetable debris and
microscopic plants, while adults prefer vegetable debris, microscopic plants, decayed
higher plants, detritus and mud as their food. The feeding habit of this fish is planktophage
and 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 a
rearing pond of the Institute and acclimatized in outdoor conditions for 15 days prior to
their 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 and
average length 78 mm and average weight 5.6 g for 0.45 ppm DTPA-extractable zinc
experiment) were stocked in each outdoor cistern and their growth and yield were studied
for 75 days out of the 90-day study. No artificial feed was provided during the growing
period of the test carp.
The physico-chemical characteristics of water were measured fortnightly following the
standard methods (APHA, 1989). The concentration of chlorophyll a, primary productiv-


ity and plankton biomass in all the treatments for each type of soil were studied at 15-day
intervals. The concentration of chlorophyll a was studied spectrophotometrically after
filtering a 10 ml of water sample through cellulose-nitrate membrane filter of 0.45 Am and
after extraction in acetone (Boyd, 1984). The primary productivity was assessed by the
light and dark bottle dissolved oxygen method (Vollenweider, 1974). Bottles were filled
with water taken from 0.25 and 0.50 m depths from the center of each cistern. Two light
and two dark bottles were resuspended at those depths beginning at 10.00 h. They were
left in cisterns for 4 h. For plankton biomass estimation, a known volume of surface water
was filtered through the plankton net made of bolting silk cloth (No. 25, 64 Am), dried in
an oven, cooled in a desiccator, weighed and the results were expressed as g/10
l (Vollenweider, 1974).
At the end of the experiment, plankton and fish were harvested. The increase in weight
of fish was computed in terms of yield in g/cistern/75 days. The plankton samples were
harvested from the surface waters of experimental cisterns by filtering 50 l of water
through a plankton net made of bolting silk cloth (No. 25, 64 Am). The harvested plankton
and fish samples were first washed with tap water and then rinsed with distilled water. The
plankton and fish samples were dried at 70 and 500 jC, respectively, in a hot air oven. The
soil 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 Smith
and Shoukry (1968). Plankton, fish tissue and soil were digested separately by tri-acid
digestion for zinc estimation (Piper, 1950). For example, total zinc in fish tissue was
estimated by taking 0.5 –1.0 g of tissue and digesting with a mixture of concentrated nitric
acid and perchloric acid in the ratio of 1:3 until the formation of a white residue. The
cooled residue was dissolved completely by adding 10 ml of 1 N hydrochloric acid and
made up to 25 ml with distilled water. The content was filtered by cotton wool and the
filtrate was subjected to zinc analysis. Plankton and soil were digested similarly. Zinc
content in the plankton and fish digestions and soil extracts were determined by atomic
absorption spectrophotometry (Perkin Elmer model number 1331) adopting suitable
measuring 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 significant
difference among treatment means using SPSS software.

3. Results and discussion

The effect of zinc on primary productivity, chlorophyll a concentration and plankton
biomass are presented for the three different soil types in Table 1. The physico-chemical
condition of water in these experiments (ranges) were as follows: pH (7.2 – 8.1), total
alkalinity (90 – 120 ppm as CaCO3), total hardness (75 – 110 ppm as CaCO3), total
ammonia (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 all
three levels of DTPA-extractable zinc showed an increase in primary productivity,
chlorophyll a concentration and plankton biomass over fertilized controls (Table 1). For
0.45 ppm DTPA-extractable zinc, 30 kg ZnSO4/ha treatment showed the maximum yield,


Table 1
Effect of zinc on primary productivity, chlorophyll a concentration and plankton biomass
Parameters DTPA-extractable Fertilizer control Fertilizer + 10 kg Fertilizer + 20 kg Fertilizer + 30 kg
zinc (ppm) (N – P – K) ZnSO4/ha ZnSO4/ha ZnSO4/ha
Gross 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 maximum
yield and for 1.0 ppm DTPA-extractable zinc, 10 kg ZnSO4/ha gave the maximum yield
over fertilized control in terms of primary productivity, chlorophyll a concentration and
plankton biomass, and the other two treatments for all three types of soils showed an
intermediate 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 zinc
from production point of view. Soils having 0.45 ppm DTPA-extractable zinc showed the
maximum fish yield at 30 kg ZnSO4/ha treatment level while the soil having 1.0 ppm
DTPA-extractable zinc gave the maximum fish yield at 10 kg ZnSO4/ha. Soils having 0.75
ppm DTPA-extractable zinc showed the maximum yield at 20 kg ZnSO4/ha treatment
level. All the growth results were statistically significant ( p < 0.05). The lower yield for
1.0 ppm DTPA-extractable zinc at 20 and 30 kg ZnSO4/ha may be due to greater
availability of dissolved zinc in the fish culture system which is responsible for decrease in
growth and maximum size of the fish (Moore and Ramamoorthy, 1984). Zinc concentra-

332
S. Adhikari, S. Ayyappan / Aquaculture 231 (2004) 327–336
Table 2
Response of L. rohita fingerlings and plankton to graded levels of zinc application in different soils
DTPA-extractable Zinc application Survivability Fish yield Zn Zn concentration Zn uptake Zn uptake
zinc (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 4428
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 2832
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 3742
Treatment means followed by the same superscript in a column were not significantly different ( p < 0.05).


tion 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 are
generally below 50 mg/kg dry weight. Zinc uptake by plankton varied from 788 to 4428
Ag/cistern. It may be mentioned here that uptake of zinc by plankton is generally slow and
depends on metabolic/photosynthetic rate, temperature, light, and the concentrations of
zinc in the environment (Harding and Whitton, 1981). Sorption of zinc is also suppressed
by 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 with
intracellular polysaccharides.
Zinc residues in the fish were lower than those found in plankton and their
concentration varied from 19.2 to 26.0 mg/kg dry weight in the whole fish. The average
fish 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 15
species of omnivorous and carnivorous fish collected from industrial and agricultural areas
of the lower Great Lakes were 16– 82 and 3 – 9 mg/kg wet weight, respectively (Brown
and Chow, 1977). Farmer et al. (1979) reported that zinc residues in Atlantic salmon
varied from 27 to 38 mg/kg.
Soil (having 1.0 ppm DTPA-extractable zinc experiment) zinc fractions as influenced
by plankton production and L. rohita fingerlings growth are presented in Table 3. The data
reveals that the relative distribution of different forms of zinc in this soil was in the order
of water-soluble < exchangeable < organically bound < complexed < occluded < residual
zinc. The above results suggest that a major portion of the total zinc in the studied soil
existed in the residual form, while the water-soluble zinc accounted for only trace
quantities. Similar results were reported by Vasuki (1979) and Rosalind (1980) for
agricultural soils.
The effect of plankton production and L. rohita fingerling growth on depletion of
various pools of soil zinc (Table 3) suggest that water-soluble, exchangeable and
complexed forms of zinc were slightly reduced due to plankton and fish removal, but
other forms of zinc in the soil were not influenced. Soil zinc fractions were also influenced
by the application of graded levels of zinc to soil. Water-soluble zinc in the soil did not
increase up to 10 ppm zinc level, but at higher levels of zinc, the increase was
proportionate 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 the

Table 3
Soil zinc fractions as influenced by plankton and fish growth and levels of zinc application to the soil containing
1.00 ppm DTPA-extractable zinc
Soil zinc fraction Initial level (ppm) Zinc level (kg/ha)
0 10 20 30
Water-soluble 0.46 0.38 0.40 0.62 0.78
Exchangeable 1.24 1.02 1.22 2.54 2.98
Complexed 1.93 1.76 1.98 3.16 3.61
Organically bound 1.91 1.90 1.84 3.32 3.73
Occluded 2.24 2.36 2.42 2.46 2.44
Residual 111.4 111.6 112.4 115.6 112.8


Table 4
Simple correlation coefficients (r) between zinc uptake and zinc fractions in soil for 1.0 ppm DTPA-extractable
zinc
Soil Zn fraction Zinc uptake by:
Fish Plankton
Water-soluble 0.639** 0.682**
Exchangeable 0.573* 0.518*
Complexed 0.497 0.517
Organically bound 0.699** 0.672**
Occluded 0.017 0.028
Residual 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 30
ppm zinc level. On the other hand, the contents of occluded and residual zinc in soil did
not change either due to plankton and fish growth or due to addition of zinc to soil. The
occluded form of zinc in Oxisol is held mostly by sesquioxides and residual zinc is mainly
associated with mineral fraction of the soil. The transformation of applied zinc to these
forms of zinc is a slow process. However, upon aging other forms of zinc get slowly
transformed into these forms which are relatively less soluble (Chandrashekhar and
Kedlaya, 1988). Similar results were reported by Vasuki (1979) and Edward Raja (1980).
The correlation coefficients among different fractions of soil zinc (Table 4) suggest that
the 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 by
fish fingerlings and plankton. The contribution of each fraction to the pool of available
zinc 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 are
the principal forms contributing to the pool of available zinc in this soil. The contribution
of 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 has
low cation exchange capacity (CEC), the contribution of exchangeable zinc to the
available pool is limited. Similarly, the contribution of both the occluded and the residual
forms of zinc to the available pool was very little. The findings of the investigation
corroborate those reported by Edward Raja (1980) and Rosalind (1980) for agricultural
rice soils.

4. Conclusions

From the foregoing discussion, it may be concluded that zinc application as fertilizer is
beneficial in pond aquaculture for better plankton and fish growth. The maximum growth
was observed in the 30 kg ZnSO4/ha – 0.45 ppm DTPA-extractable zinc, second highest
followed by 10 kg –1.0 ppm, followed by third highest growth in the 20 kg– 0.75 ppm


treatment. It may also be concluded that water-soluble, organically bound and to some
extent exchangeable forms of zinc contribute to the pool of available zinc in the
experimental soil having 1.0 ppm DTPA-extractable zinc. It is therefore, necessary to
include 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.

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