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

Aquaculture Reports 11 (2018) 8–16

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

T

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Abu Syed Md. Kibriaa,b, , Mohammad Mahfujul Haquea a b

Department of Aquaculture, Bangladesh Agricultural University, Mymensingh, Bangladesh 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: IMTA Aquaculture Freshwater pond Bangladesh

An experimental study was carried out for a period of six months to assess the potential of integrated multitrophic aquaculture (IMTA) in earthen freshwater ponds. Nine earthen ponds (40 m2 each) were randomly assigned to three treatments in triplicate. Carps and stinging catfish; carps, stinging catfish, and snails; and carps, stinging catfish, snails, and water spinach as IMTA, were assigned to T1, T2, and T3, respectively. The stocking 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-inponds 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 opportunity 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 increasing dependency on aquaculture. The contribution of aquaculture

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reached 55.93% of total fish production (DoF, 2016) which is characterized 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 Bangladesh, 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 ingredients are imported from the international market (Mamun-UrRashid 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 fertilizers accumulated in the pond sediment, and the remainder was removed 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 transformation 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: [email protected] (A.S.M. Kibria), [email protected] (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 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/).

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A.S.Md. Kibria, M.M. Haque

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 levels 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 facilitates 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 acceptability over conventional fish monoculture in the USA and Canada, because seafood produced in IMTA systems were considered better for the environment and animal welfare, and to a lesser degree, safer and healthier (Shuve et al., 2009; Barrington et al., 2010). Therefore, the objective of this study was to assess the potentials of IMTA in freshwater earthen ponds, for carp and freshwater snail production, using snails as feed for stinging catfish reared in cage-in-pond, and cultivating aquatic plant to keep the water quality suitable for fish growth. Here, carp culture was combined with organic waste extractive (e.g., mollusk), and inorganic waste extractive (e.g., aquatic plant) aquaculture species (Fig. 1), to create a balanced system which is environmentally sustainable, economically stable, and socially acceptable.

Fig. 2. Experimental layout of the study using nine freshwater ponds.

2.2. Experimental design The study consisted of three treatments (T1, T2, and T3), and each treatment had three replications. Carps and stinging catfish; carps, stinging catfish, and snails; and carps, stinging catfish, snails, and water spinach were assigned to treatments T1, T2, and T3, respectively (Fig. 2). A cage of 1 m3 (1 × 1 × 1 m) volume was set in each of the ponds, in which to rear stinging catfish; the aim was to prevent escape of fish from the pond, and to make sampling and harvest convenient, 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 embedded 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 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, were placed in the three ponds under T3, for growing water spinach only.

2. Materials and methods 2.1. Experimental site and pond facilities Nine earthen ponds, average size 40 m2 each, depth 1 m, and rectangular, located at Bangladesh Agricultural University (BAU) campus, 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 terms of geometric configuration, and were well exposed to sunlight and air. Although the main source of water was rainfall, there was a facility for water irrigation of individual experimental ponds from a deep tubewell, through a flexible plastic pipe.

2.3. Pond preparation and setting cages in ponds Initially, the pond water was drained out completely. Undesirable organisms like small fishes, aquatic weeds, and other rooted vegetation 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

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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 synthetic 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.

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-parameter 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.

2.4. 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 experimental 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.

2.8. 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)

2.5. Aquatic plant cultivation on floating trays

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%.

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.

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.

2.6. 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 containing 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 oilcake) 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 requirements 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

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 independent 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 10

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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 Prepared feed Rice bran Wheat bran Mustard oil cake

88.17 88.02 88.50 87.91 87.65

35.78 22.27 14.80 15.61 35.42

6.60 20.60 16.44 4.89 11.72

16.96 18.02 17.49 13.15 11.25

5.23 6.99 15.41 5.80 9.64

35.43 32.13 35.85 60.55 31.96

a

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

Table 2 Growth parameters (mean ± SE) of cultured species in different treatments. Parameters

Table 3 Mean yield (kg ha−1 6-mo−1 ± SE) of cultured species in different treatments.

Treatments

Cultured species T2

T3

Mean initial weight (g) Catla 22.24 ± 1.56 Silver carp 26.65 ± 0.81 Rohu 23.11 ± 1.43 Mrigal 24.04 ± 0.82 Stinging catfish 2.86 ± 0.12

21.49 ± 1.74 27.74 ± 1.06 23.79 ± 2.04 23.93 ± 1.07 2.97 ± 0.04

21.33 ± 1.13 27.07 ± 1.42 22.82 ± 0.99 24.50 ± 1.41 2.73 ± 0.12

Mean final weight (g) Catla 158.65 ± 10.93 Silver carp 208.79 ± 7.2a Rohu 169.34 ± 8.15b Mrigal 137.79 ± 7.59 Stinging catfish 42.99 ± 1.97

159.50 ± 4.61 181.42 ± 6.29b 171.06 ± 5.03b 116.59 ± 5.87 46.90 ± 2.57

141.39 ± 4.10 220.91 ± 4.57a 192.32 ± 3.71a 121.49 ± 6.46 44.67 ± 2.28

Mean weight gain (g) Catla 136.41 ± 12.11 Silver carp 182.15 ± 8.01a Rohu 146.23 ± 8.95b Mrigal 113.75 ± 8.40 Stinging catfish 40.13 ± 2.09

138.01 ± 6.17 153.68 ± 5.4b 147.27 ± 4.88b 92.65 ± 6.12 43.93 ± 2.57

120.06 ± 4.36 193.83 ± 5.98a 169.50 ± 3.82a 97.00 ± 7.71 41.94 ± 2.18

SGR (% day−1) Catla Silver carp Rohu Mrigal Stinging catfish FCR

1.11 1.16 1.13 0.99 1.55 3.07

1.14 1.06 1.12 0.89 1.57 2.85

1.07 1.19 1.21 0.90 1.60 2.63

Survival (%) Catla Silver carp Rohu Mrigal Stinging catfish

65.74 54.63 60.65 58.80 69.00

T1

± ± ± ± ± ±

0.07 0.04ab 0.05 0.05 0.05 0.24

± ± ± ± ±

5.63 2.45b 1.22b 6.82 5.51

± ± ± ± ± ±

70.03 66.03 65.32 59.88 74.67

0.06 0.01b 0.04 0.04 0.03 0.10

± ± ± ± ±

3.55 3.31ab 0.71a 1.55 2.73

± ± ± ± ± ±

71.94 70.04 61.43 61.38 72.33

Catla Silver carp Rohu Mrigal Carps1 Stinging catfish Fish2 Snail Fish and snail Water spinach Total biomass3

T1

T2

T3

757.32 ± 24.70 278.28 ± 3.11b 503.03 ± 29.10 396.97 ± 50.69 1935.61 ± 60.23 670.61 ± 86.47

830.66 ± 30.37 289.56 ± 24.64b 555.26 ± 19.24 347.34 ± 23.86 2031.82 ± 62.57 682.41 ± 77.35

759.03 ± 16.50 387.05 ± 17.26a 586.05 ± 26.47 369.81 ± 38.95 2101.93 ± 31.35 725.15 ± 80.26

2606.22 ± 140.23 – 2606.22 ± 140.23c

2714.24 ± 46.80 2756.39 ± 127.80 5470.63 ± 83.72b

2827.08 ± 54.21 3123.33 ± 65.83 5950.41 ± 42.15a

– 2606.22 ± 140c

– 5470.63 ± 83.08b

3567.03 ± 934.85 9517.44 ± 969.41a

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 test (Field, 2005). 1 Yield of carps: Total yield of catla, silver carp, rohu, and mrigal. 2 Yield of fish: Total yield of carps, and stinging catfish. 3 Yield of total biomass: Total yield of fish, snail, and water spinach.

0.03 0.04a 0.03 0.06 0.02 0.09

± ± ± ± ±

Treatments

cage, did not differ significantly (p > 0.05) among the treatments (Table 2). 3.2. Yield parameters of fish

0.71 4.92a 1.43ab 5.35 1.45

Species-wise yield of silver carp, total fish and snails, and total biomass, differed significantly (p < 0.05) among the treatments (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 T2 were almost the same, with no statistical differences. Yields of total fish and snails, and total biomass, were significantly the highest (p < 0.05) in T3 (i.e., in IMTA ponds), and lowest in T1 (control ponds) (Table 3).

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 test (Field, 2005). FCR: Food Conversion Ratio.

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 treatments 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, followed by T2 and T1 (Table 2). As with weight gain, no significant difference was found among the treatments for the SGR of stinging catfish. Although insignificant, the highest SGR of stinging catfish in cage-in-pond was found in T3, i.e., in IMTA ponds. Survival (%) of silver carp and rohu differed significantly (p < 0.05) among the treatments. Significantly (p < 0.05), the highest survival (%) of silver carp and rohu was found in T3 and T2, 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 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 survival (%) of the remaining species, including stinging catfish in the

3.3. Growth and yield of water spinach As water spinach was cultivated on trays as an inorganic extractive and edible vegetable, its growth and production were monitored during the study period. The growth of water spinach varied with temperature variation in the months from May to October. The highest growth was observed in June, and it gradually declined towards the end of the study in the month of October. The monthly average yield of water spinach was estimated at 594.50 kg ha−1 during the culture period. Total yield of water spinach in the IMTA ponds was 3567.03 kg ha-1 6-mo−1. 3.4. Growth and yield of snails The freshwater snails, stocked as an extractive species of organic waste in T2 and T3, started to produce yield earlier than the fish, because they are ovoviviparous and proliferate faster. In terms of kg ha−1 11

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

Temperature (°C) DO (mg L−1) pH (mg L−1) NH3-N (mg L−1) NO2-N (mg L−1) PO4-P (mg L−1)

N

21 21 21 21 21 21

Treatments T1

T2

T3

30.31 ± 0.29 4.86 ± 0.26 7.45 ± 0.07 0.015 ± 0.002a 0.00 0.27 ± 0.03a

30.43 ± 0.25 4.67 ± 0.19 7.43 ± 0.06 0.017 ± 0.002a 0.00 0.23 ± 0.04a

30.40 ± 0.28 4.57 ± 0.27 7.50 ± 0.06 0.008 ± 0.001b 0.00 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 test (Field, 2005). N: number of observations.

Fig. 4. Monthly variations in dissolved oxygen in different treatments.

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

Fig. 5. Monthly variations in pH in different treatments.

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 (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. 6. Monthly variations in NH3-N in different treatments.

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, and water spinach was much higher in T3, i.e., in IMTA ponds,

Fig. 3. Monthly variations in water temperature in different treatments. 12

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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 treatments. 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 environmental conditions, in spite of a much higher stocking density of cultured species.

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, particularly 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 individual 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) compared 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 niches 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. However, 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 supplementary 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 contained 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

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 yearround 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 appropriate levels, and the production of water spinach was satisfactory. In low nitrate concentration, water spinach satisfies its nitrate requirements 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 deficiency (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 conditions. This further confirmed that water spinach exhibited a biomitigation process, and kept the concentrations of nitrogenous waste within suitable ranges. 13

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could be promoted through action research with potential pond farmers towards sustaining food security of the poor people.

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 culture 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 nutrients for primary productivity. The concentration of phosphatephosphorus (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 phosphatephosphorus 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 content during the study period. With the decreasing dissolved oxygen level, there was a delicate relationship found with increasing ammonianitrogen. 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.

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. 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