Aquaculture Reports 11 (2018) 8–16

Contents lists available at ScienceDirect

Aquaculture Reports
journal homepage: www.elsevier.com/locate/aqrep

Potentials of integrated multi-trophic aquaculture (IMTA) in freshwater T

ponds in Bangladesh
⁎
Abu Syed Md. Kibriaa,b, , Mohammad Mahfujul Haquea
a
Department of Aquaculture, Bangladesh Agricultural University, Mymensingh, Bangladesh
b
Department of Aquaculture, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh

A R T I C LE I N FO A B S T R A C T

Keywords: An experimental study was carried out for a period of six months to assess the potential of integrated multi-
IMTA trophic aquaculture (IMTA) in earthen freshwater ponds. Nine earthen ponds (40 m2 each) were randomly as-
Aquaculture signed to three treatments in triplicate. Carps and stinging catfish; carps, stinging catfish, and snails; and carps,
Freshwater pond stinging catfish, snails, and water spinach as IMTA, were assigned to T1, T2, and T3, respectively. The stocking
Bangladesh
densities were: carps: 20,000 fingerlings ha−1 at a ratio of 3: 1: 2: 2 for catla: silver carp: rohu: mrigal; stinging
catfish: 24,700 fingerlings ha−1 in cage-in-pond for all treatments; and snails: 62 kg ha−1 in T2 and T3. The carps
were fed with supplementary feed, a mixture of rice bran and wheat bran (1: 1) at the rate of 3–5% of fish
biomass; the stinging catfish with commercial feed for the first 45 days, and snail-mixed pelleted feed for the rest
of the experimental period, at the rate of 5–25% of body weight. The highest survival, particularly of silver carp,
mrigal, and stinging catfish was found in T3, i.e., in IMTA ponds. The weight gain of silver carp, rohu, and
stinging catfish was the highest in IMTA ponds. The highest yields of the carps and stinging catfish in cage-in-
ponds were obtained in IMTA ponds. The production of snails and water spinach in IMTA ponds contributed to
the biomitigation process of organic and inorganic waste, keeping the water quality within suitable conditions
for fish culture.

1. Introduction
Globally, traditional fish production from capture fisheries is static,
at 90.8 million metric ton in 2007, and 90.3 million metric ton in 2012
(FAO, 2014). However, total demand for fish is rising, along with the
increasing human population. Sustaining fish supplies from capture
fisheries will, therefore, not be possible if the growing global demand
for aquatic foods is to be met. Aquaculture is considered to be an op-
portunity to bridge the supply and demand gap for aquatic food in most
regions of the world; thus, it is developing, expanding, and intensifying
(Subasinghe et al., 2009), with various positive impacts, including food
and nutrition security, employment generation both upstream and
downstream of the value chain, and poverty reduction (Toufique and
Belton, 2014). However, in contrast with these positive effects, the
negative environmental impacts of aquaculture have received a high
degree of attention over the decades (Subasinghe et al., 2009; Bureau
and Hua, 2010).
The growth of capture fisheries in Bangladesh is very slow, similar
to the global trend of capture fisheries, and therefore, there is an in-
creasing dependency on aquaculture. The contribution of aquaculture
reached 55.93% of total fish production (DoF, 2016) which is char-
acterized by semi-intensive and intensive farming systems, intensive
feed supply, and labor-intensive management (Ali et al., 2013). Feed is
the single most important cost item in aquaculture operations in Ban-
gladesh, incurring over 70% of the total operating investment (Hasan,
2012; Mohsin et al., 2012; Mondal et al., 2012). In fish feed production,
both at commercial and farm levels, approximately 50% of feed in-
gredients are imported from the international market (Mamun-Ur-
Rashid et al., 2013). Intensive feeding of aquaculture species results in a
large amount of sedimentation (Lin and Yang, 2003; Anka et al., 2013),
with high levels of nutrient accumulation (nitrogen, phosphorus, and
organic carbon) in the pond environment, both in soil and water (Nhan
et al., 2006). An early study on semi-intensive aquaculture showed
approximately 80% of nitrogen and phosphorus from feeds and ferti-
lizers accumulated in the pond sediment, and the remainder was re-
moved through the harvested fish (Edwards, 1993; Avnimelech, 1998).
Cumulative nutrient deposition causes stress and diseases in farmed fish
(Anka et al., 2013), resulting in lower production and economic returns
(Edwards et al., 1996). In effect, intensive aquaculture is the transfor-
mation of dietary inputs into fish biomass, which inevitably produces

⁎
Corresponding author at: Department of Aquaculture, Hajee Mohammad Danesh Science and Technology University, Dinajpur, Bangladesh.
E-mail addresses: kibria.aqc@hstu.ac.bd (A.S.M. Kibria), mmhaque.aq@bau.edu.bd (M.M. Haque).

https://doi.org/10.1016/j.aqrep.2018.05.004
Received 4 December 2017; Received in revised form 11 April 2018; Accepted 25 May 2018
Available online 30 May 2018
2352-5134/ © 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/BY/4.0/).
A.S.Md. Kibria, M.M. Haque Aquaculture Reports 11 (2018) 8–16

waste in the enclosure. The waste products released from aquaculture

operations are organic (feed and fecal wastes), and inorganic (nitrogen
and phosphorus containing compounds) in nature, and result in the
environmental degradation of bodies of water (Bureau and Hua, 2010;
Haque et al., 2016). These sorts of problems resulting from aquaculture
operations have been minimized demonstrably in marine environments
applying IMTA principles (Ridler et al., 2007; Costa-Pierce, 2010).
IMTA is the farming of aquaculture species of different trophic le-
vels in the proximity with complementary ecosystem functions, in a
way that allows uneaten feed, waste, and by-products of one species to
be utilized as fertilizers, feed, and energy for the other crops, and to
take advantage of synergistic interactions among the species (Chopin
et al., 2001, 2008; Troell et al., 2003; Neori et al., 2004). IMTA facil-
itates biomitigation, and diversification of fed monoculture practices,
by combining them with extractive aquaculture species, to realize
benefits environmentally, economically, and socially (Chopin et al.,
2012). In salmon-IMTA system, additional income obtained from
mussels and seaweeds reduced economic losses when they occurred,
and provided greater economic resilience to the overall operation
(Ridler et al., 2007). In many cases, IMTA also gained social accept-
ability over conventional fish monoculture in the USA and Canada, Fig. 2. Experimental layout of the study using nine freshwater ponds.
because seafood produced in IMTA systems were considered better for
the environment and animal welfare, and to a lesser degree, safer and 2.2. Experimental design
healthier (Shuve et al., 2009; Barrington et al., 2010). Therefore, the
objective of this study was to assess the potentials of IMTA in fresh- The study consisted of three treatments (T1, T2, and T3), and each
water earthen ponds, for carp and freshwater snail production, using treatment had three replications. Carps and stinging catfish; carps,
snails as feed for stinging catfish reared in cage-in-pond, and cultivating stinging catfish, and snails; and carps, stinging catfish, snails, and water
aquatic plant to keep the water quality suitable for fish growth. Here, spinach were assigned to treatments T1, T2, and T3, respectively
carp culture was combined with organic waste extractive (e.g., mol- (Fig. 2). A cage of 1 m3 (1 × 1 × 1 m) volume was set in each of the
lusk), and inorganic waste extractive (e.g., aquatic plant) aquaculture ponds, in which to rear stinging catfish; the aim was to prevent escape
species (Fig. 1), to create a balanced system which is environmentally of fish from the pond, and to make sampling and harvest convenient,
sustainable, economically stable, and socially acceptable. compared with open ponds. Nine bamboo splits, each 1.1 m long, were
placed in each pond as a temporary shelter for snails, covering an area
of 1 m2 of the pond bottom in a square array of three lines, and em-
2. Materials and methods bedded into the bottom at 45° angles. Stinging catfish was cultured in
cages in order to use snails as a feed ingredient, because snails are not
2.1. Experimental site and pond facilities used as a food item by the general people of Bangladesh, except for a
small percentage of tribes. Four floating trays, each 0.11 m2 in area,
Nine earthen ponds, average size 40 m2 each, depth 1 m, and rec- were placed in the three ponds under T3, for growing water spinach
tangular, located at Bangladesh Agricultural University (BAU) campus, only.
were chosen to conduct this study for a period of 6 months from April
15 to October 08, 2012. All the ponds were of similar size and shape, in
2.3. Pond preparation and setting cages in ponds
terms of geometric configuration, and were well exposed to sunlight
and air. Although the main source of water was rainfall, there was a
Initially, the pond water was drained out completely. Undesirable
facility for water irrigation of individual experimental ponds from a
organisms like small fishes, aquatic weeds, and other rooted vegetation
deep tubewell, through a flexible plastic pipe.
were removed. The excess bottom mud was removed, and broken and
uneven dikes were filled with the same. Agricultural lime (CaCO3) was
applied at 250 kg ha−1, to maintain pH level in the appropriate range

Fig. 1. A conceptual framework of the IMTA experiment in freshwater ponds.

9
A.S.Md. Kibria, M.M. Haque
for fish culture, and compost was applied at 680 kg ha−1 during pond
preparation. Compost was prepared in a pit of a pond dike, using
mustard oil cake, cow dung, urea, and water hyacinth at a rate of 36.50,
36.50, 9.00, and 18.00%, respectively, and was applied as the basal
manure to expedite growth of food organisms for the carps and snails.
After the application of compost, the ponds were filled with water, up
to 1 m depth, from a deep tubewell, through a flexible plastic pipe. Nine
cages were constructed using iron bar frames, and covered with syn-
thetic nylon nets (mesh size 2 cm), with one cage allocated to each
pond. The cages were attached to the pond bottom, so that the stinging
catfish had a natural environment in contact with the bottom mud,
because they are bottom dwelling fish.
2.4. Collection and stocking of fish and snail seed
Fingerlings of the carps (catla, Catla catla; silver carp,
Hypophthalmichthys molitrix; rohu, Labeo rohita, and mrigal, Cirrhinus
mrigala), and stinging catfish, Heteropneustes fossilis, were bought from a
reputable private fish hatchery in Mymensingh district, to ensure good
quality seed, and were brought to the pond site in plastic drums with
continuous aeration. The average initial weights of fingerlings were
21.69 ± 0.76, 27.15 ± 0.58, 23.24 ± 0.79, 24.16 ± 0.57, and
2.86 ± 0.06 g, respectively. Before stocking, the fingerlings were kept
in hapa nets, for acclimatization with the environment of the experi-
mental ponds. The stocking density of the carps in ponds was 20,000
fingerlings ha−1 at a ratio of 3: 1: 2: 2 (catla: silver carp: rohu: mrigal)
and stinging catfish in cages at 24,700 fingerlings ha−1. These stocking
rates were adapted from Wahab et al. (2004) and Haque et al. (2014)
for stinging catfish and carps, respectively. Ponds of T2 and T3 were
stocked with snails (Viviparus bengalensis) at the density of 62 kg ha−1,
collected from the cultured ponds of the Field Laboratory Complex,
BAU, Mymensingh.
2.5. Aquatic plant cultivation on floating trays
Among the cultured species, water spinach (Ipomoea aquatica), an
aquatic plant component of IMTA was cultivated only in the T3 ponds
on plastic trays supported by locally available empty plastic water
bottles, floating on the water surface. A piece of synthetic net was
placed on the bottom of each tray, then a 2 cm layer of bottom mud
from the same pond was added as a substrate for transplanting water
spinach cuttings. The synthetic net was used so that pond mud was not
washed out through the bigger mesh of the plastic tray. Twelve cuttings
(average length 15 cm each) were planted in six clusters in each tray.
2.6. Feeding the carps in ponds, and stinging catfish in cages-in-ponds
The carps were fed with a supplementary feed of rice bran and
wheat bran (1: 1) at 3–5% of body weight (Hossain and Kibria, 2006).
The calculated ration was divided into equal halves: 50% was given at
09:00 AM and the remaining 50% at 04:00 PM. Similarly, stinging
catfish were fed at 5–25% of body weight, dividing into equal halves, at
07:00 AM and 06:00 PM. For stinging catfish, a commercial feed con-
taining 35.78% of protein was supplied for the first 1.5 months, then a
snail mixed pelleted feed (made of snails, rice bran and mustard oil-
cake) for the remaining period. Snails were collected from the bamboo
splits in the experimental ponds manually, with a harvesting device
made of iron rod. The collected snails were mixed with rice bran and
mustard oilcake at a ratio of 3: 4: 3, respectively, to prepare the pelleted
feed, using a locally made pellet machine, to feed the stinging catfish in
cages. The protein content of the snail mixed feed was adjusted to
20.00%, based on Pearson’s Square method, to consider the require-
ments of stinging catfish cultured in a cage system (Lipton, 1983). Later
the prepared feed was analyzed for nutritional composition, and the
protein content was found to be 22.27% (Table 1).
Fish sampling was carried out at 45-day intervals in order to avoid
10
Aquaculture Reports 11 (2018) 8–16
disturbance to snails growing on the pond bottom. A cast net was used
for sampling, and a minimum of 10% of the initially stocked fish were
sampled. The average weight of the cultured species were recorded for
estimating different parameters and to adjust ration size.
2.7. Monitoring water quality parameters
Water quality parameters, such as temperature (°C), pH, dissolved
oxygen (mg L−1), ammonia-nitrogen (mg L−1), nitrite-nitrogen (mg
L−1), and phosphate-phosphorus (mg L−1) were monitored at monthly
intervals. The water samples were collected between 09:00 and 10:00
AM on the sampling days. Water temperature, dissolved oxygen, pH,
ammonia, nitrite, and phosphorus were measured using a Nine-para-
meter Test Kit (Model: FF-1A, Cat. No. 2430-02; Hach Company, USA).
Dissolved oxygen was measured in situ and the other parameters were
analyzed in the laboratory.
2.8. Harvesting and yield estimation
Ponds were dried out completely for the total harvest at the end of
the experiment. All of the fishes were counted by species, and the
weight of individual fish was measured with an electronic balance
(Model: HKD-620AS-LED; A & D Company Limited, China). Percent
weight gain (% weight gain), specific growth rate (SGR, % day−1), food
conversion ratio (FCR), and gross yield of fish, were estimated as per
the following formulae.
% weight gain = (Average final weight – Average initial weight)/
Average initial weight × 100
SGR (% day−1) = (ln final weight – ln initial weight)/Duration of the
experiment (days) × 100
FCR = Feed applied (dry weight)/Live weight gain (wet weight)
Gross yield = Total number of fish at harvest × average final
weight
Total yield of snails was estimated as the sum of the partial harvest
during the culture period, in which snail mixed feed was prepared for
stinging catfish cultured in cages, and the final harvest at the end of the
study. For the latter measurement, snails were sampled from the bottom
of the drained pond with a harvesting device, from 1.8 m2
(0.60 × 3.0 m) of the pond bottom. The process was repeated for three
times for each pond to cover an area at least 10%.
Total yield = Partial harvest + Final harvest
Water spinach was harvested at 30-day intervals (Salam and Roy,
2012), and total yield was calculated at the end of the trial.
2.9. Statistical analyses
One-way analysis of variance (ANOVA) was performed, to test the
significance of difference among the treatment means, in terms of carp
production in the pond, and stinging catfish in cages, and an in-
dependent samples t-test was applied for snail production. The level of
significance was assigned at 0.05 for all the parameters. All statistical
tests were performed with a computer-based statistical software, SPSS -
Statistical Package for Social Sciences, version 16.
3. Results
3.1. Growth parameters of fish
Different species of carp showed different growth patterns in the
three treatments. The average final weight of silver carp and rohu
differed significantly (p < 0.05) among the treatments. Both silver
carp and rohu grew most in T3 (Table 2). The individual final weight of
A.S.Md. Kibria, M.M. Haque Aquaculture Reports 11 (2018) 8–16

Table 1
Proximate compositions (%) of feed ingredients and feeds on a dry matter basis.
Components Dry matter Crude protein Crude lipid Crude fiber Ash NFEa

Commercial feed 88.17 35.78 6.60 16.96 5.23 35.43

Prepared feed 88.02 22.27 20.60 18.02 6.99 32.13
Rice bran 88.50 14.80 16.44 17.49 15.41 35.85
Wheat bran 87.91 15.61 4.89 13.15 5.80 60.55
Mustard oil cake 87.65 35.42 11.72 11.25 9.64 31.96

a
NFE (Nitrogen-free extract) was calculated as: 100 – % (moisture + crude protein + crude lipid + crude fiber + ash).

Table 2 Table 3
Growth parameters (mean ± SE) of cultured species in different treatments. Mean yield (kg ha−1 6-mo−1 ± SE) of cultured species in different treatments.
Parameters Treatments Cultured Treatments
species
T1 T2 T3 T1 T2 T3

Mean initial weight (g) Catla 757.32 ± 24.70 830.66 ± 30.37 759.03 ± 16.50
Catla 22.24 ± 1.56 21.49 ± 1.74 21.33 ± 1.13 Silver carp 278.28 ± 3.11b 289.56 ± 24.64b 387.05 ± 17.26a
Silver carp 26.65 ± 0.81 27.74 ± 1.06 27.07 ± 1.42 Rohu 503.03 ± 29.10 555.26 ± 19.24 586.05 ± 26.47
Rohu 23.11 ± 1.43 23.79 ± 2.04 22.82 ± 0.99 Mrigal 396.97 ± 50.69 347.34 ± 23.86 369.81 ± 38.95
Mrigal 24.04 ± 0.82 23.93 ± 1.07 24.50 ± 1.41 Carps1 1935.61 ± 60.23 2031.82 ± 62.57 2101.93 ± 31.35
Stinging catfish 2.86 ± 0.12 2.97 ± 0.04 2.73 ± 0.12 Stinging 670.61 ± 86.47 682.41 ± 77.35 725.15 ± 80.26
catfish
Mean final weight (g)
Fish2 2606.22 ± 140.23 2714.24 ± 46.80 2827.08 ± 54.21
Catla 158.65 ± 10.93 159.50 ± 4.61 141.39 ± 4.10
Snail – 2756.39 ± 127.80 3123.33 ± 65.83
Silver carp 208.79 ± 7.2a 181.42 ± 6.29b 220.91 ± 4.57a
Fish and 2606.22 ± 140.23c 5470.63 ± 83.72b 5950.41 ± 42.15a
Rohu 169.34 ± 8.15b 171.06 ± 5.03b 192.32 ± 3.71a
snail
Mrigal 137.79 ± 7.59 116.59 ± 5.87 121.49 ± 6.46
Water spinach – – 3567.03 ± 934.85
Stinging catfish 42.99 ± 1.97 46.90 ± 2.57 44.67 ± 2.28
Total 2606.22 ± 140c 5470.63 ± 83.08b 9517.44 ± 969.41a
Mean weight gain (g) biomass3
Catla 136.41 ± 12.11 138.01 ± 6.17 120.06 ± 4.36
Silver carp 182.15 ± 8.01a 153.68 ± 5.4b 193.83 ± 5.98a Mean values followed by different superscript letters in the same row were
Rohu 146.23 ± 8.95b 147.27 ± 4.88b 169.50 ± 3.82a found to be significantly different (p < 0.05), based on Duncan’s multiple range
Mrigal 113.75 ± 8.40 92.65 ± 6.12 97.00 ± 7.71 test (Field, 2005).
Stinging catfish 40.13 ± 2.09 43.93 ± 2.57 41.94 ± 2.18 1
Yield of carps: Total yield of catla, silver carp, rohu, and mrigal.
SGR (% day−1) 2
Yield of fish: Total yield of carps, and stinging catfish.
Catla 1.11 ± 0.07 1.14 ± 0.06 1.07 ± 0.03 3
Yield of total biomass: Total yield of fish, snail, and water spinach.
Silver carp 1.16 ± 0.04ab 1.06 ± 0.01b 1.19 ± 0.04a
Rohu 1.13 ± 0.05 1.12 ± 0.04 1.21 ± 0.03
Mrigal 0.99 ± 0.05 0.89 ± 0.04 0.90 ± 0.06 cage, did not differ significantly (p > 0.05) among the treatments
Stinging catfish 1.55 ± 0.05 1.57 ± 0.03 1.60 ± 0.02 (Table 2).
FCR 3.07 ± 0.24 2.85 ± 0.10 2.63 ± 0.09

Survival (%) 3.2. Yield parameters of fish

Catla 65.74 ± 5.63 70.03 ± 3.55 71.94 ± 0.71
Silver carp 54.63 ± 2.45b 66.03 ± 3.31ab 70.04 ± 4.92a
Rohu 60.65 ± 1.22b 65.32 ± 0.71a 61.43 ± 1.43ab
Species-wise yield of silver carp, total fish and snails, and total
Mrigal 58.80 ± 6.82 59.88 ± 1.55 61.38 ± 5.35 biomass, differed significantly (p < 0.05) among the treatments
Stinging catfish 69.00 ± 5.51 74.67 ± 2.73 72.33 ± 1.45 (Table 3). A significantly higher yield (kg ha−1 6-mo−1) of silver carp
was found in T3 than in the other treatments, whereas yields in T1 and
Mean values followed by different superscript letters in the same row were T2 were almost the same, with no statistical differences. Yields of total
found to be significantly different (p < 0.05), based on Duncan’s multiple range
fish and snails, and total biomass, were significantly the highest
test (Field, 2005). FCR: Food Conversion Ratio.
(p < 0.05) in T3 (i.e., in IMTA ponds), and lowest in T1 (control ponds)
(Table 3).
stinging catfish did not differ among the treatments. Overall, individual
silver carp grew the most compared to the other carps (Table 2).
There were no significant (p > 0.05) differences among the treat- 3.3. Growth and yield of water spinach
ments for the specific growth rate (SGR, % day−1) of the carps, except
for the silver carp. The highest SGR of silver carp was found in T3, As water spinach was cultivated on trays as an inorganic extractive
followed by T2 and T1 (Table 2). As with weight gain, no significant and edible vegetable, its growth and production were monitored during
difference was found among the treatments for the SGR of stinging the study period. The growth of water spinach varied with temperature
catfish. Although insignificant, the highest SGR of stinging catfish in variation in the months from May to October. The highest growth was
cage-in-pond was found in T3, i.e., in IMTA ponds. observed in June, and it gradually declined towards the end of the study
Survival (%) of silver carp and rohu differed significantly in the month of October. The monthly average yield of water spinach
(p < 0.05) among the treatments. Significantly (p < 0.05), the was estimated at 594.50 kg ha−1 during the culture period. Total yield
highest survival (%) of silver carp and rohu was found in T3 and T2, of water spinach in the IMTA ponds was 3567.03 kg ha-1 6-mo−1.
respectively; the lowest was in T1 for both species. This parameter was
significantly higher in T3 than T1 for silver carp; however, there was no 3.4. Growth and yield of snails
significant difference (p > 0.05) between T1 and T3 for rohu, and the
same deviation was found between T1 and T2 for silver carp. The sur- The freshwater snails, stocked as an extractive species of organic
vival (%) of the remaining species, including stinging catfish in the waste in T2 and T3, started to produce yield earlier than the fish, be-
cause they are ovoviviparous and proliferate faster. In terms of kg ha−1

11
A.S.Md. Kibria, M.M. Haque Aquaculture Reports 11 (2018) 8–16

Table 4
Physicochemical parameters (mean ± SE) of pond water during the study
period.
Parameters N Treatments

T1 T2 T3

Temperature (°C) 21 30.31 ± 0.29 30.43 ± 0.25 30.40 ± 0.28

DO (mg L−1) 21 4.86 ± 0.26 4.67 ± 0.19 4.57 ± 0.27
pH (mg L−1) 21 7.45 ± 0.07 7.43 ± 0.06 7.50 ± 0.06
NH3-N (mg L−1) 21 0.015 ± 0.002a 0.017 ± 0.002a 0.008 ± 0.001b
NO2-N (mg L−1) 21 0.00 0.00 0.00
PO4-P (mg L−1) 21 0.27 ± 0.03a 0.23 ± 0.04a 0.16 ± 0.02b

Mean values followed by different superscript letters in the same row were
found to be significantly different (p < 0.05), based on Duncan’s multiple range Fig. 4. Monthly variations in dissolved oxygen in different treatments.
test (Field, 2005). N: number of observations.

6-mo−1, the production of snails in T3 (3123.33 ± 65.83) was com-

paratively higher than that of T2 (2756.39 ± 127.80).

3.5. Water quality parameters

The results of sampling, and the determination of physicochemical

parameters of water (mean values ± SE), are presented in Table 4.
Temperature, dissolved oxygen (DO), and pH had no significant var-
iations (p > 0.05) among the treatments. However, NH3-N and PO4-P
were found to be significantly the lowest (p < 0.05) in T3.
The highest temperature (32 °C) was recorded in May and July, and
the lowest was 28 °C in October (Fig. 3). Dissolved oxygen levels ranged
from 3.00 to 8.00 mg L−1 during the study period. The highest level of Fig. 5. Monthly variations in pH in different treatments.
dissolved oxygen was recorded in an IMTA pond in June (Fig. 4). Very
slight differences were found for pH among the treatments throughout
the study period; they ranged from 7.00 to 8.00, and followed a similar
trend to the dissolved oxygen (Fig. 5). The highest values for NH3-N and
PO4-P were 0.045 and 0.60 mg L−1, respectively, and the lowest values
were 0 for both parameters (Figs. 6, 7).

4. Discussion

Aquaculture research and extension started in Bangladesh with very

low stocking density of 5000 or fewer individuals ha−1 (Rajbangshi and
Shrestha, 1980; Sharma et al., 1985; Sharma and Das, 1988; Sharma,
1989, 1990; Mazid et al., 1997), which has been greatly increased by
several research and development projects. For example, stocking
density in carp polyculture was 20,000 fish ha−1 at the research level
Fig. 6. Monthly variations in NH3-N in different treatments.
(Haque et al., 2014; Wahab et al., 2014), and was 55,000–60,000 fish
ha−1 at the farmers’ level (Nahid et al., 2012; Ali et al., 2013). This
increasing intensification indicates environmental implications of pond
aquaculture on one hand, on the other hand it shows huge productivity
potential to grow diversified aquaculture produces applying IMTA
principles in pond, which is experimented in this study and discussed.

Fig. 7. Monthly variations in PO4-P in different treatments.

4.1. Growth and yield of fish

The total biomass yield, including the carps, stinging catfish, snails,
Fig. 3. Monthly variations in water temperature in different treatments. and water spinach was much higher in T3, i.e., in IMTA ponds,

12
A.S.Md. Kibria, M.M. Haque
compared to other treatments. Stinging catfish is a micronutrient-dense
and high-value fish being commercially cultured in Bangladesh.
However, in semi-intensive and intensive farming operations, feeds
and/or fertilizers account for 40–80% of the total operating costs (De
Silva and Hasan, 2007). Therefore, strategies are needed to reduce the
amount and cost of feed inputs, to provide a good profit margin, par-
ticularly if fish are polycultured with carp, and are relying primarily on
the direct consumption of formulated feeds for their growth, rather than
natural pond productivity (Wahab et al., 2014). In this study, the in-
dividual growth of the carps did not differ significantly (p > 0.05)
among the treatments. In some cases, such as silver carp and rohu, the
growth was significantly higher (p < 0.05) in IMTA ponds (T3) com-
pared to other treatments. This is possibly because the polyculture of
the carps and stinging catfish works well where the production food
organisms is enhanced by co-species; as a result, the total production
per unit of area is also increased (Hepher et al., 1989; Miah et al., 1993;
Azad et al., 2004). Nutrient recycling through polyculture systems is
more practical and efficient than traditional and intensive monoculture
practices. According to Wurts (2000), phytoplankton and zooplankton,
with no market value, occupy sizable respiratory niches (for oxygen
consumption) in the pond environment. Proper selection of suitable
filter-feeding fish and mollusk for polyculture could open up these ni-
ches for the production of species with greater economic value.
Wahab et al. (2014) experimented with the polyculture of carps and
stinging catfish (catla: rohu: stinging catfish = 1: 4: 25), with 1.3 times
higher stocking density of carps (60,000 ha−1) than that used in the
present study. A considerable growth and production of the carps and
stinging catfish in the polyculture system were reported (Chakraborty
and Nur, 2012; Wahab et al., 2014). This is because the carps normally
like natural food organisms (Rahman et al., 2006), whereas stinging
catfish need an external feed supply containing protein (Kamruzzaman
et al., 2013). Although stinging catfish-in-cage was isolated from the
carps in the pond, there was a movement of water containing natural
food organisms horizontally between the pond water and the cage. Via
this movement of water, there was a possibility of competition for
natural food organisms between the carps and stinging catfish. How-
ever, this is unlikely to have happened, as this kind of uncompetitive
relationship was explained by Wahab et al. (2014).
The mean final weights of catla, mrigal, and stinging catfish did not
differ significantly among the treatments but they differed for silver
carp and rohu. The significantly higher final weight of silver carp was
obtained in both T1, and T3, than T2, and it was significantly the highest
in T3 for rohu. In case of mean weight gain, similar results were found
for all fishes. The recorded mean final weights of the carps corroborate
the findings of Uddin et al. (2012), however, they were lower than
those reported by Haque et al. (2003) and Jahan (2008). The lower
mean final weights may be due to the lower protein content in sup-
plementary feed supplied to the carps (Mazid et al., 1997). According to
Ramaswamy et al. (2013), the protein requirement for catla and rohu is
25%, whereas the supplementary diet used in the present study con-
tained only 15.21% protein. This might be the cause of low mean final
weight, and therefore, mean weight gain and yield of the carps. SGR (%
day−1) of fish species did not vary among the treatments, except for the
silver carp. Significantly, the highest SGR of silver carp was found in T3
(IMTA ponds). Although the SGR of the carps was lower than the SGR
reported by Roy et al. (2002); Rahman et al. (2011), and Jena et al.
(2013), the findings of the present study corroborate well with the
findings of Jasmine et al. (2011).
There were no significant differences in the survival (%) of catla,
mrigal and stinging catfish but it was significantly different between
treatments for the silver carp and rohu. The highest survival was found
in T3 and T2, for silver carp and rohu, respectively. These findings agree
with those of Jena et al. (2013). The survival (%) of the carps was lower
than those of Shahin et al. (2011), and Rahman et al. (2011); the reason
may be the predation of the carps by snakes and water monitors. On the
other hand, survival (%) of stinging catfish was higher than that
13
Aquaculture Reports 11 (2018) 8–16
reported by Wahab et al. (2004), who found 39.33–60.67% survival of
stinging catfish in cages.
Total yield of the carps varied from 1935.61 to 2101.93 kg ha−1 6-
−1
mo , with no significant differences (p > 0.05) among the treat-
ments. Carp yield in the present study was higher than the total yield
reported by Uddin et al. (1994, 2012). An estimated gross yield of
1707.75 kg ha−1 6-mo−1 in a carp polyculture operation was reported
by Uddin et al. (1994). Kohinoor et al. (1999) achieved an estimated
yield of 2566 kg ha−1 6-mo−1 from a polyculture of silver barb (Puntius
gonionotus) and exotic carp, which was slightly higher than that of the
present study. However, stinging catfish, snails, and water spinach were
also cultured with the carps in T3. Though it is not significant, the
highest yield of carps was obtained from T3, i.e., IMTA ponds, and the
yields of catfish, snails, and water spinach were 725.15, 3123.33, and
3567.03 kg ha−1 6-mo−1, respectively. The total biomass yield was
significantly highest (p < 0.05) in T3 (9517.44), which was much
higher than that achieved by Kohinoor et al. (1999). The likely reasons
for the highest yields in the IMTA ponds are the prevailing better en-
vironmental conditions, in spite of a much higher stocking density of
cultured species.
4.2. Growth and production of waste extractives (snail and water spinach)
Freshwater snails feed on organic waste, algae, and zooplankton,
and these in turn provide food for many fishes, birds, and human
beings. They are bioindicators, and play vital roles in purifying bodies
of water, because they are saprophytic (Saddozai et al., 2013). In IMTA
systems, the snails live on the bottom of the pond, and they do not
compete with fish for food, as they are sessile in nature, and cannot
swim (Slootweg, 1995). Organic waste is produced from the uneaten
fish feed, and this accumulates on the bottom of the ponds, and is used
by the snails as food (Saddozai et al., 2013). The total yield of snails was
3123 kg ha−1 during the 6 months of the study period, of which only
63 kg was used in feed preparation; the remainder was unutilized. The
prepared feed, formulated using snails, rice bran, and mustard oil cake,
provided the required level of protein for the stinging catfish. Using the
total amount of snails, 8329 kg of additional feed could be prepared,
which in turn, could be used to produce 3332 kg of fish, assuming a feed
conversion ratio (FCR) of 2.5. As with stinging catfish (Unlu et al.,
2011), black carp (Mylopharyngodon piceus), Nile tilapia (Oreochromis
niloticus), and African catfish (Clarias gariepinus) also take freshwater
snails as food (Slootweg, 1995). Therefore, the surplus snails produced
in IMTA ponds could be used to feed the species mentioned above, in
different aquaculture systems. Moreover, snail-mixed feed and whole
snails can also be used for feeding poultry (Diomande et al., 2008) and
duck (Hossain et al., 2014).
Water spinach is a very popular vegetable in Bangladesh as human
food, and all parts except roots of the young water spinach plant are
edible (DEPI, 2002). Water spinach grows in freshwater ponds year-
round in the tropics (DEPI, 2002) which needs sufficient nutrients,
particularly nitrogen. According to Chairuangsri et al. (2014), growth
of water spinach is affected by external NH4+ supply. It grows well in a
medium with NH4+ concentration ranging from 0.5 to 5 mM, but
growth is suppressed at higher concentrations (≥10 mM NH4+). In the
present study, water quality parameters in IMTA ponds were at ap-
propriate levels, and the production of water spinach was satisfactory.
In low nitrate concentration, water spinach satisfies its nitrate re-
quirements by enhancing its root surface with more and longer root
hairs (Foehse and Jungk, 1983; Steingrobe and Schenk, 1991), and
decreases its root diameter as a means of adaptation to nutrient defi-
ciency (Barber, 1984). According to our observation in the IMTA ponds,
the growth of water spinach roots was medium in scale; they did not
touch the pond bottom, rather took nutrients under submerged condi-
tions. This further confirmed that water spinach exhibited a biomiti-
gation process, and kept the concentrations of nitrogenous waste within
suitable ranges.
A.S.Md. Kibria, M.M. Haque
4.3. Water quality parameters in relation to biomitigation
Water quality parameters are very critical for aquaculture, and are
dependent on management aspects such as stocking density, cultured
organisms, and nutritional inputs, etc. (Diana et al., 1997). In this
study, the water quality parameters such as temperature, dissolved
oxygen (DO), and pH did not differ significantly among the treatments
(p > 0.05), except for NH3-N and PO4-P, and all of them were within
the appropriate ranges for fish culture (Boyd and Zimmermann, 2000;
Bhatnagar et al., 2004; Asaduzzaman et al., 2008; Rahman et al., 2010).
Water temperature (28–32 °C) recorded during the study period was
within the appropriate range for fish culture. According to Bhatnagar
et al. (2004), the optimum range of temperatures for tropical fish cul-
ture is 28–32 °C, which is similar to the findings of the present study.
Similar findings were also reported by Hossain and Islam (2006), and
Jena et al. (2013). The concentration of DO in different treatments
ranged from 3 to 8 mg L−1, which was higher than the findings of Jena
et al. (2013). According to Bhatnagar et al. (2004), and Bhatnagar and
Singh (2010), DO concentrations should be maintained at 5 mg L−1 or
above for good production of fish. Below adequate levels of oxygen in
water result in poor feeding of fish, starvation, reduced growth, and
mortality, and the ultimate result is low production (Bhatnagar and
Garg, 2000). The range of pH (7–8) during the study period was very
good for fish culture, because the optimum range of pH for aquaculture
is 7 to 8.5 (Ekubo and Abowei, 2011).
Due to the increased biomass in IMTA ponds, there was a possibility
of an increase in toxic substances, such as nitrite, and ammonia.
However, their presence was very low in particular, nitrite level was
zero. Ammonia-nitrogen levels (0.00–0.045 mg L−1) recorded during
the study period were lower than that reported by Dewan et al. (1991)
and Rahman et al. (2011), who obtained results ranging from 0.05 to
6.20 and 0.01 to 1.35 mg L−1, respectively. Haque et al. (1998) found
ammonia-nitrogen content ranged from 0.11 to 0.13 mg L−1 in their
research ponds. Kohinoor et al. (2001) observed ammonia-nitrogen
ranging from 0.01 to 1.55 mg L−1 in monoculture ponds. The levels of
ammonia-nitrogen content found in the experimental ponds were far
below the tolerance levels as reported by Kohinoor et al. (2001); Islam
(2002), and Islam et al. (2002). Phosphorus is one of the limiting nu-
trients for primary productivity. The concentration of phosphate-
phosphorus (PO4-P) varied from 0.00 to 0.60 mg L−1, which was very
similar to that reported by Rahman et al. (2008). The phosphate-
phosphorus level in the present study was below the highest level of an
acceptable range (0.03–2.00 mg L−1) (Bhatnagar and Devi, 2013), but
higher than the findings of Jena et al. (2013).
The water quality parameters were mostly within the appropriate
range for aquaculture during the study period from April to October.
However, temperature, dissolved oxygen, and ammonia-nitrogen
showed a complex relationship. There was a slight correlation observed
between increasing temperature and decreasing dissolved oxygen con-
tent during the study period. With the decreasing dissolved oxygen
level, there was a delicate relationship found with increasing ammonia-
nitrogen. However, such fluctuations of water quality parameters in the
present study did not exceed the suitable range, thereby had no adverse
impacts on fish growth and survival in different treatments.
5. Conclusion
Anecdotally, aquaculture production has intensified with a few se-
lected species, causing several negative impacts such as deterioration of
water and soil quality of ponds, stress, and poor growth of fish, a low
profit margin, and overall environmental degradation. Against this
background, IMTA has shown a potential for crop diversity, with a
traditional food fish, a cash crop (stinging catfish), mollusk, and water
spinach, from the same pond. The diversity of production increased
pond productivity greatly, keeping the water quality parameters within
balanced levels, according to IMTA principles. This suggests that IMTA
14
Aquaculture Reports 11 (2018) 8–16
could be promoted through action research with potential pond farmers
towards sustaining food security of the poor people.
Acknowledgements
As part of doctoral studies of first author, this study was carried out
with the funding support of Bangladesh Agricultural University
Research System (BAURES), Bangladesh Agricultural University,
Mymensingh, Bangladesh. The opinions expressed herein are those of
the authors and do not necessarily reflect the views of BAURES.
References
Ali, H., Haque, M.M., Belton, B., 2013. Striped catfish (Pangasianodon hypophthalmus,
Sauvage, 1878) aquaculture in Bangladesh: an overview. Aquaclt. Res. 44, 950–965.
Anka, I.Z., Faruk, M.A.R., Hasan, M.M., Azad, M.A.K., 2013. Environmental issues of
emerging pangas (Pangasianodon hypophthalmus) farming in Bangladesh. Prog. Agric.
24 (1–2), 159–170.
Asaduzzaman, M., Wahab, M.A., Verdegem, M.C.J., Azim, M.E., Haque, S., Salam, M.A.,
2008. C/N ratio control and substrate addition for periphyton development jointly
enhance freshwater prawn, Macrobrachium rosenbergii production in ponds.
Aquaculture 280, 117–123.
Avnimelech, Y., 1998. Minimal discharge from intensive fish ponds. World Aquacult. 29
(1), 32–37.
Azad, M.A.K., Raman, M.R., Rahman, Z., Kader, M.A., Haque, M.M., Alam, M.J., 2004.
Polyculture of carp, tilapia and pangas using low cost inputs. Pak. J. Biol. Sci. 7,
1918–1926.
Barber, S.A., 1984. Soil Nutrient Bioavailability: A Mechanistic Approach. Academic
Press, New York.
Barrington, K., Ridler, N., Chopin, T., Robinson, S., Robinson, B., 2010. Social aspects of
the sustainability of integrated multi-trophic aquaculture. Aquacult. Int. 18 (2),
201–211.
Bhatnagar, A., Devi, P., 2013. Water quality guidelines for the management of pond fish
culture. Int. J. Environ. Sci. 3 (6), 1980–2009.
Bhatnagar, A., Garg, S.K., 2000. Causative factors of fish mortality in still water fish ponds
under sub-tropical conditions. Aquaculture 1 (2), 91–96.
Bhatnagar, A., Jana, S.N., Garg, S.K., Patra, B.C., Singh, G., Barman, U.K., 2004. Water
quality management in aquaculture. Course Manual of Summer School on
Development of Sustainable Aquaculture Technology in Fresh and Saline Waters. CCS
Haryana Agricultural University, Hisar, India, pp. 203–210.
Bhatnagar, A., Singh, G., 2010. Culture fisheries in village ponds: a multi-location study in
Haryana. India. Agric. Biol. J. North Am. 1 (5), 961–968.
Boyd, C., Zimmermann, S., 2000. Grow-out systems - water quality and soil management.
In: New, M.B., Valenti, W.C. (Eds.), Freshwater Prawn Culture: the Farming of
Macrobrachium Rosenbergii. Blackwell Science, Oxford, UK, pp. 221–238.
Bureau, D.P., Hua, K., 2010. Towards effective nutritional management of waste outputs
in aquaculture, with particular reference to salmonid aquaculture operations.
Aquacult. Res. 41, 777–792.
Chairuangsri, S., Whangchai, N., Jampeetong, A., 2014. Responses of water spinach
(Ipomoea aquatica Forssk.) on growth, morphology, uptake rate and nutrients allo-
cation under high ammonium concentration. Chiang Mai J. Sci. 41 (2), 324–333.
Chakraborty, B.K., Nur, N.N., 2012. Growth and yield performance of shingi,
Heteropneustes fossilis and koi, Anabas testudineus in Bangladesh under semi-intensive
culture systems. Int. J. Agric. Res. Innov. Technol. 2 (2), 15–24.
Chopin, T., Buschmann, A.H., Halling, C., Troell, M., Kautsky, N., Neori, A., 2001.
Integrating seaweeds into marine aquaculture systems: a key towards sustainability.
J. Phycol. 37, 975–986.
Chopin, T., Cooper, J.A., Reid, G., Cross, S., Moore, C., 2012. Open-water integrated
multi-trophic aquaculture: environmental biomitigation and economic diversification
of fed aquaculture by extractive aquaculture. Rev. Aquacult. 4, 209–220.
Chopin, T., Robinson, S.M.C., Troell, M., Neori, A., Buschmann, A.H., Fang, J., 2008.
Multi-trophic integration for sustainable marine aquaculture. In: Jorgensen, S.E.,
Fath, B.D. (Eds.), The Encyclopedia of Ecology. Elsevier, Oxford, UK, pp. 2463–2475.
Costa-Pierce, B.A., 2010. Sustainable ecological aquaculture systems: the need for a new
social contract for aquaculture development. Mar. Technol. Soc. J. 44 (3), 88–112.
Diomande, M., Koussemon, M., Allou, K.V., Kamenan, A., 2008. Effect of snail (Achatina
fulica) meal on broiler production and meat sensorial quality. Livest. Res. For. Rural
Dev. 20 (12) Retrieved May 8, 2017 from. http://www.lrrd.org/lrrd20/12/
diom20192.htm.
De Silva, S.S., Hasan, M.R., 2007. Feeds and fertilizers: the key to long-term sustainability
of Asian aquaculture. In: Hasan, M.R., Hecht, T., De Silva, S.S., Tacon, A.G.J. (Eds.),
Study and Analysis of Feeds and Fertilizers for SustAinable Aquaculture
Development. FAO, Rome, Italy, pp. 19–47.
DEPI, 2002. Water Spinach (Kangkong). Retrived May 7, 2017, from. Department of
environment and primary industries, 1 Spring Street, Melbourne, Victoria, Australia.
http://agriculture.vic.gov.au/agriculture/horticulture/vegetables/vegetables-a-z/
growing-water-spinach-kangkong.
Dewan, S., Wahab, M.A., Beveridge, M.C.M., Rahman, M.H., Sarker, B.K., 1991. Food
selection, electivity and dietary overlap among planktivorous Chinese and Indian
major carp fry and fingerlings grown in extensively managed rain-fed ponds in
Bangladesh. Aquacult. Res. 22 (3), 277–294.
Diana, J.S., Szyper, J.P., Batterson, T.R., Boyd, C.E., Pied-Rahita, R.H., 1997. Water
A.S.Md. Kibria, M.M. Haque
quality in ponds. In: Egna, H.S., Boyd, C.E. (Eds.), Dynamics of Pond Aquaculture.
CRC Press LLC, Boca Raton, Florida, USA, pp. 53–72.
DoF, 2016. Fisheries Statistical Report of Bangladesh. Fisheries Resources Survey System
(FRSS), Department of Fisheries, Ministry of Fisheries and Livestock, Bangladesh,
pp. 57.
Edwards, P., 1993. Environmental issues in integrated agriculture-aquaculture and was-
tewater-fed fish culture systems. In: Pullin, R.S.V., Rosenthal, H., Maclean, J.L. (Eds.),
Environment and Aquaculture in Developing Countries. Federal Republic of
Germany, Eschborn, pp. 139–170 Proceedings of ICLARM Conference, Manila,
Philippines, September 1990. International Center for Living Aquatic Resources
Management, Manila, Philippines and Deutsche Gesellschaft für Technische
Zusammenarbeit (GTZ) GmbH.
Edwards, P., Demaine, H., Innes-Taylor, N., Turongruang, D., 1996. Sustainable aqua-
culture for small-scale farmers: need for a balanced model. Outlook Agric. 25 (1),
19–26.
Ekubo, A.A., Abowei, J.F.N., 2011. Review of some water quality management principles
in culture fisheries. Res. J. Appl. Sci. Eng. Technol. 3 (2), 1342–1357.
FAO, 2014. The State of World Fisheries and Aquaculture. Food and Agriculture
Organization of the United Nations, Rome, Italy.
Field, A., 2005. Discovering Statistics Using SPSS. SAGE Publication, London, UK.
Foehse, D., Jungk, A., 1983. Influence of phosphate and nitrate supply on root hair for-
mation of rape, spinach and tomato plants. Plant Soil 74, 359–368.
Haque, M.M., Belton, B., Alam, M.M., Ahmed, A.G., Alam, M.R., 2016. Reuse of fish pond
sediments as fertilizer for fodder grass production in Bangladesh: potential for sus-
tainable intensification and improved nutrition. Agric. Ecosyst. Environ. 216,
226–236.
Haque, M.M., Jubayer, A.S.M., Anisuzzaman, M., Kibria, A.S.M., 2014. A study on growth
and production of a freshwater snail, Viviparus bengalensis on different substrates in
carp polyculture ponds. Bangladesh J. Prog. Sci. Technol. 12 (1), 1–4.
Haque, M.M., Narejo, N.T., Salam, M.A., Rahmatullah, S.M., Islam, M.A., 2003.
Determination of optimum stocking density of Macrobrachium rosenbergii in carp
polyculture in earthen ponds. Pak. J. Biol. Sci. 6 (10), 898–901.
Haque, S.M., Wahab, M.A., Wahid, M.I., Haq, M.S., 1998. Impacts of Thai silver barb
(Puntius gonionotus Bleeker) inclusion in the polyculture of carps. Bangladesh J. Fish.
Res. 2, 15–22.
Hasan, M.H.R., 2012. Study on present status and constraints of aquaculture in Pirgachha
and Kawnia upazila of Rangpur district. Master’s Thesis. Bangladesh Agricultural
University, Mymensingh, Bangladesh.
Hepher, B., Milstein, A., Leventer, H., Teltsch, B., 1989. The effect of fish density and
species combination on growth and utilization of natural food in ponds. Aquacult.
Fish. Manage. 20, 59–71.
Hossain, M.A., Islam, M.S., 2006. Optimization of stocking density of freshwater prawn
Macrobrachium rosenbergii (de Man) in carp polyculture in Bangladesh. Aquacult. Res.
37, 994–1000.
Hossain, M.A., Kibria, A.S.M., 2006. Over-wintering growth of Macrobrachium rosenbergii
(de Man) with carp polyculture in Bangladesh fed formulated diets. Aquacult. Res.
37, 1334–1340.
Hossain, M.I., Alam, M.M., Siwar, C., Dey, M.M., Mokhtar, M., Jaafar, A.H., Hossain,
M.Y., 2014. Water productivity for living aquatic resources in floodplains of
Northwestern Bangladesh. J. Coast. Life Med. 2 (4), 324–331.
Islam, M.S., 2002. Evaluation of supplementary feeds for semi-intensive pond culture of
mahseer, Tor putitora (Hamilton). Aquaculture 212, 263–276.
Islam, M.S., Dewan, S., Hussain, M.G., Hossain, M.A., Mazid, M.A., 2002. Feed utilization
and wastage in semi-intensive pond culture of mahseer, Tor putitora (Ham.).
Bangladesh J. Fish. Res. 6, 1–9.
Jahan, D.A., 2008. Substitution of fish meal protein by soybean meal protein in the diet of
two Indian major carps. PhD Thesis. Bangladesh Agricultural University,
Mymensingh, Bangladesh.
Jasmine, S., Molina, M., Hossain, M.Y., Jewel, M.A.S., Ahamed, F., Fulanda, B., 2011.
Potential and economic viability of freshwater prawn, Macrobrachium rosenbergii (de
Man, 1879) polyculture with Indian major carps in northwestern Bangladesh. Our
Nat. 9, 61–72.
Jena, J., Das, P.C., Mitra, G., Patro, B., Mohanta, D., Mishra, B., 2013. Effects of varied
levels of incorporation of Labeo gonius in carp polyculture system in India. Aquacult.
Res. 46 (9), 2073–2078.
Kamruzzaman, M., Rahman, A.F.M.A., Rabbane, M.G., Ahmed, M.S., Mustafa, M.G.,
2013. Growth performances of stinging catfish (Heteropneustes fossilis; Bloch) rearing
and feeding on formulated fish feed in the laboratory condition. IJPSBM 1 (1), 18–28.
Kohinoor, A.H.M., Islam, M.S., Begum, N., Hussain, M.G., 1999. Production of Thai
sharpunti (Puntius gonionotus Bleeker) in polyculture with carps using low-cost feed.
Bangladesh J. Fish. Res. 3, 157–164.
Kohinoor, A.H.M., Wahab, M.A., Islam, M.L., Thilsted, S.H., 2001. Culture potentials of
mola (Amblypharyngodon mola), chela (Chela cachius) and punti (Puntius sophore)
under monoculture system. Bangladesh J. Fish. Res. 5 (2), 123–134.
Lin, C.K., Yang, Y., 2003. Minimizing environmental impacts of freshwater aquaculture
and reuse of pond effluents and mud. Aquaculture 226, 57–68.
Lipton, A.P., 1983. Studies on the culture of Heteropneustes fossilis in cages. In: Natarajan,
P., Santhanam, R., Sukumaran, N., Sundararaj, V., Ramadhas, V. (Eds.), Proceedings
of the National Seminar on Cage and Pen Culture. India Fisheries College 1984,
Tuticorin, pp. 51–54 Tamil Nadu, India, 18–19 March 1983.
Mamun-Ur-Rashid, M., Belton, B., Phillips, M., Rosentrater, K.A., 2013. Improving
aquaculture feed in Bangladesh: from feed ingredients to farmer profit to safe con-
sumption. Working Paper No. 2013-34. WorldFish, Penang, Malaysia.
Mazid, M.A., Zaher, M., Begum, N.N., Ali, M.Z., Nahar, F., 1997. Formulation of cost-
effective feeds from locally available ingredients for carp polyculture system for in-
creased production. Aquaculture 151, 71–78.
15
Aquaculture Reports 11 (2018) 8–16
Miah, M.S., Uddin, M.S., Shah, M.S., 1993. Effects of artificial feed in carps polyculture
system. Bangladesh J. Agric. Sci. 20, 359–364.
Mohsin, A.B.M., Islam, M.N., Hossain, M.A., Galib, S.M., 2012. Constraints and prospects
of carp production in Rajshahi and Natore districts, Bangladesh. Univ. J. Zool.
Rajshahi Univ. 31, 69–72.
Mondal, M.A.H., Ali, M.M., Sarma, P.K., Alam, M.K., 2012. Assessment of aquaculture as
a means of sustainable livelihood development in Fulpur Upazila under Mymensingh
district. J. Bangladesh Agric. Univ. 10 (2), 391–402.
Nahid, S.A.A., Karim, E., Hasan, M.R., Shahabuddin, A.M., Bhuyain, M.A.B., 2012.
Different farming systems and comparative advantages of tilapia over other com-
mercial aquaculture species in Bangladesh. BJPST 10 (1), 93–96.
Neori, A., Chopin, T., Troell, M., Buschmann, A.H., Kraemer, G.P., Halling, C., Shpigel,
M., Yarish, C., 2004. Integrated aquaculture: rationale, evolution and state of the art
emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231,
361–391.
Nhan, D.K., Milstein, A., Verdegem, M.C., Verreth, J.A., 2006. Food inputs, water quality
and nutrient accumulation in integrated pond systems: a multivariate approach.
Aquaculture 261 (1), 160–173.
Rahman, M.A., Azimuddin, K.M., Yeasmine, S., 2011. Polyculture of a critically en-
dangered olive barb, Puntius sarana (Ham.), with indigenous major carps in earthen
ponds. J. World Aquacult. Soc. 42 (6), 778–788.
Rahman, M.M., Verdegem, M., Wahab, M.A., 2008. Effects of tilapia (Oreochromis niloticus
L.) stocking and artificial feeding on water quality and production in rohu-common
carp bi-culture ponds. Aquacult. Res. 39, 1579–1587.
Rahman, M.M., Verdegem, M.C.J., Nagelkerke, L.A.J., Wahab, M.A., Milstein, A., Verreth,
J.A.J., 2006. Growth, production and food preference of rohu Labeo rohita (H.) in
monoculture and in polyculture with common carp Cyprinus carpio (L.) under fed and
non-fed ponds. Aquaculture 257, 359–372.
Rahman, S.M., Wahab, M., Islam, M., Kunda, M., Azim, M., 2010. Effects of selective
harvesting and claw ablation of all-male freshwater prawn (Macrobrachium ro-
senbergii) on water quality, production and economics in polyculture ponds.
Aquacult. Res. 41, 404–417.
Rajbangshi, K.G., Shrestha, M.B., 1980. A case study on the economics of integrated
farming systems: agriculture, aquaculture and animal husbandry in Nepal. In: Pullin,
R.S.V., Shehadeh, Z.H. (Eds.), Proceedings of the ICLARM-SEARCA Conference on
Integrated Agriculture-Aquaculture Farming Systems. Manila, Philippines, 6–9
August 1979. International Center for Living Aquatic Resources Management, Manila
and the Southeast Asian Regional Center for Graduate Study and Research in
Agriculture, College, Los Banos, Luguna, Philippines. pp. 195–208.
Ramaswamy, B.N., Kumar, B.T., Pradeep, D.L., Kamalesh, P., Ramesh, K.S., 2013. Dietary
protein requirement of stunted fingerlings of the Indian major carp, Catla Catla
(Hamilton) during grow-out phase. Indian J. Fish. 60 (4), 87–91.
Ridler, N., Wowchuk, M., Robinson, B., Barrington, K., Chopin, T., Robinson, S., Page, F.,
Reid, G., Szemerda, M., Sewuster, J., Boyne-Travis, S., 2007. Integrated multi-trophic
aquaculture (IMTA): a potential strategic choice for farmers. Aquacult. Econ.
Manage. 11 (1), 99–110.
Roy, N.C., Kohinoor, A.H.M., Wahab, M.A., Thilsted, S.H., 2002. Evaluation of perfor-
mance of Carp–SIS polyculture technology in the rural farmers’ Pond. Asian Fish. Sci.
15, 43–52.
Saddozai, S., Baloch, W.A., Achakzai, W.M., Memon, N., 2013. Population dynamics and
ecology of freshwater gastropods in Manchar Lake Sindh, Pakisthan. J. Anim. Plant
Sci. 23 (4), 1089–1093.
Salam, M.A., Roy, M., 2012. Raft aquaponics for sustainable fish and vegetable produc-
tion from high density fish pond (abstract). In: Wahab, M.A., Alam, M.J., Hoq, M.E.,
Alam, A.K.M.N., Barman, B.K., Rahman, S.M.S., Hossain, M.A.R. (Eds.), Proceedings
of the Fifth Fisheries Conference and Research Fair 2012. Dhaka, Bangladesh, 18-19
January 2012. Bangladesh Fisheries Research Forum, Dhaka, Bangladesh. pp. 81.
Shahin, J., Mondal, M.N., Wahab, M.A., Kunda, M., 2011. Effects of addition of tilapia in
carp-prawn-mola polyculture system. J. Bangladesh Agric. Univ. 9 (1), 147–157.
Sharma, B.K., 1989. Fish culture integrated with various systems of livestock farming-II.
Fish-cum-duck. In: ICAR Training Program on Integrated Fish Farming for Tripura
Fisheries Officers, Comp. of Lect. 2,81–89. Central Institute of Freshwater
Aquaculture, Kausalyaganga, Bhubaneswar, India.
Sharma, B.K., 1990. Development of fish-cum-duck and fish-cum-pig farming in India. In:
Comp. of Lect. 2, 1–19. Central Institute of Freshwater Aquaculture, Kausalyaganga,
Bhubaneswar, India.
Sharma, B.K., Das, M.K., Chalkraborty, D.P., 1985. Package of practices for increasing
production in fish-cum-livestock farming system. Aquaculture Extension Manual,
New Series No. 5. Central Inland Fisheries Research Institute, Barrackpore, West
Bengal, India.
Sharma, B.K., Das, M.K., 1988. Studies on integrated fish-livestock-crop farming system.
Fish. Chimes 7 (11), 15–27.
Shuve, H., Caines, E., Ridler, N., Chopin, T., Reid, G., Sawhney, M., Lamontagne, J.,
Szemerda, M., Marvin, R., Powell, F., Robinson, S., 2009. Survey finds consumers
support integrated multi-trophic aquaculture. Effective marketing concept key.
Global Aquacult. Advocate 12 (2), 22–23.
Slootweg, R., 1995. Snail control by fish: an explanation for its failure. NAGA ICLARM Q.
18 (4), 16–19.
Steingrobe, B., Schenk, M.K., 1991. Influence of nitrate concentration at the root surface
on yield and nitrate uptake of kohlrabi (Brassica oleracea gongyloides L.) and spinach
(Spinacia oleracea L.). Plant Soil 135, 205–211.
Subasinghe, R., Soto, D., Jia, J., 2009. Global aquaculture and its role in sustainable
development. Rev. Aquacult. 1, 2–9.
Toufique, K.A., Belton, B., 2014. Is aquaculture pro-poor? Empirical evidence of impacts
on fish consumption in Bangladesh. World Dev. 64, 609–620.
Troell, M., Halling, C., Neori, A., Chopin, T., Buschmann, A.H., Kautsky, N., Yarish, C.,
A.S.Md. Kibria, M.M. Haque
2003. Integrated mariculture: asking the right questions. Aquaculture 226 (1-4),
69–90.
Uddin, M.N., Shahjahan, M., Haque, M.M., 2012. Manipulation of species composition in
small scale carp polyculture to enhance fish production. BJPST 10 (1), 9–12.
Uddin, M.S., Miah, M.S., Alam, M.S., 1994. Study on production optimization through
polyculture of indigenous and exotic carps. Bangladesh J. Train Dev. 7 (2), 67–72.
Unlu, E., Cicek, T., Deger, D., Coad, B.W., 2011. Range extension of the exotic Indian
stinging catfish, Heteropneustes fossilis (Bloch, 1794) (Heteropneustidae) into the
Turkish part of the Tigris River watershed. J. Appl. Ichthyol. 27, 141–143.
Wahab, M.A., Masud, O.A., Yi, Y., Diana, J.S., Lin, C.K., 2004. Integrated cage-cum-pond
culture systems with high-valued stinging catfish (Heteropneustes fossilis) in cages and
16
Aquaculture Reports 11 (2018) 8–16
low-valued carps in open ponds. In: Aquaculture Collaborative Research Support
Program. Twenty-Second Annual Administrative Report 2003–2004, Corvallis,
Oregon, USA. p. 11. http://pdf.usaid.gov/pdf_docs/Pdacf694.pdf.
Wahab, M.A., Sakib, M.N., Borski, R.J., 2014. Effect of different feeding regimes on
growth and production performance of air-breathing stinging catfish, shing
Heteropneustes fossilis and major carps in pond polyculture (abstract). In: Proceedings
of the Conference Aquaculture America 2014. World Aquaculture Society. Seattle,
Washington, USA, 9–12 February 2014.
Wurts, W.A., 2000. Sustainable aquaculture in the twenty-first century. Rev. Fish. Sci. 8
(2), 141–150.