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ISSN: 2330-8249 (Print) 2330-8257 (Online) Journal homepage: http://www.tandfonline.com/loi/brfs21

Integrated Freshwater Farming: State-of- the-Art and Future Potential

Helcio L. A. Marques, Michael B. New, Marcello Villar Boock, Helenice Pereira Barros, Margarete Mallasen & Wagner C. Valenti

To cite this article: Helcio L. A. Marques, Michael B. New, Marcello Villar Boock, Helenice Pereira Barros, Margarete Mallasen & Wagner C. Valenti (2016) Integrated : State-of-the-Art and Future Potential, Reviews in & Aquaculture, 24:3, 264-293, DOI: 10.1080/23308249.2016.1169245

To link to this article: http://dx.doi.org/10.1080/23308249.2016.1169245

Published online: 20 Apr 2016.

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Download by: [Dr Wagner Valenti] Date: 21 April 2016, At: 11:00 REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 2016, VOL. 24, NO. 3, 264–293 http://dx.doi.org/10.1080/23308249.2016.1169245

Integrated Freshwater Prawn Farming: State-of-the-Art and Future Potential

Helcio L. A. Marquesa, Michael B. Newb, Marcello Villar Boocka, Helenice Pereira Barrosc, Margarete Mallasenc,y, and Wagner C. Valentid aAquaculture Center, Fisheries Institute, Sao Paulo State Secretariat of and Supply, S~ao Paulo, ; bFreshwater Prawn Farming Research Group, CNPq, Brazil, Marlow, Bucks, UK; cCenter for Continental , Fisheries Institute, Sao Paulo State Secretariat of Agriculture and Food Supply, S~ao Paulo, Brazil; dBiosciences Institute and CAUNESP, CNPq., S~ao Paulo State University UNESP, S~ao Paulo, Brazil

ABSTRACT KEYWORDS Integrated aquaculture can be defined as aquaculture systems sharing with other freshwater ; activities, commonly agricultural, agroindustrial, and infrastructural. Freshwater prawns are excellent ; polyculture; options for integration, since they are and can therefore take advantage of a wide range coculture; integration; of feed residuals, either from aquatic or terrestrial species. Furthermore, due to their benthic habit, potential; IMTA they have a well-defined spatial distribution in the environment, thus favoring interaction with various species of fish, other , and even with plants. The integrated farming of freshwater prawns includes different culture systems, such as polyculture and coculture with other aquatic species, rice-prawn culture, hydroponics, and integration with terrestrial animals and plants. Our review includes a worldwide perspective on the main commercial integrated systems involving freshwater prawns, the present status of research on integrated freshwater prawn production and the main opportunities for integrated freshwater prawn farming in a world that is moving toward . The review continues by providing a brief summary of the future prospects for this form of aquaculture. Finally, we conclude that integrating freshwater prawn farming with other aquaculture and farming activities has considerable potential as a means of increasing food production in a sustainable fashion.

Introduction vollenhovenii (see Kutty and Valenti, 2010 for a review). The term freshwater prawn, sometimes referred to as Recently, freshwater prawn farming has become a major freshwater is a general designation for caridean contributor to global aquaculture, both in quantity and , which spend at least the juvenile and adult value (New, 2010). In 2013, 571,152 t of freshwater phases in freshwater. Most species farmed around the prawns were produced globally, which makes freshwater world or used in aquaculture experiments belong to the prawn farming an industry valued at the -gate at genus Macrobrachium. This genus is tropical and native US$ 3 billion/year (FAO, 2015). to , Africa, and America (Holthuis and Ng, 2010). The term “integrated aquaculture” has been fre- Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 Until recently, most commercial culture had been based quently misunderstood. In scientific papers and in the on the giant river prawn Macrobrachium rosenbergii. documents of government agencies or private enter- Nevertheless, >250,000 t of the oriental river prawn prises, there is often a confusion between the terms “inte- Macrobrachium nipponense were produced in in grated aquaculture,”“sustainable aquaculture,”“organic 2013, the culture of the monsoon river prawn Macro- aquaculture,”“responsible aquaculture,” and “socially brachium malcolmsonii has started in and Pakistan, and/or environmentally responsible aquaculture.” These and the monkey river prawn Macrobrachium lar in expressions are quite distinct, although they have some Vanuatu (FAO, 2015). Many other species are under elements in common. For example, a fish monoculture research for aquaculture purposes, including the - may be sustainable, or organic, or environmentally zon river prawn Macrobrachium amazonicum and the responsible, despite not being an integrated aquaculture. painted river prawn Macrobrachium carcinus in the On the other hand, an integrated aquaculture system Americas, and the African river prawn Macrobrachium does not have to be organic and sometimes, it may not

CONTACT Wagner C. Valenti [email protected] Universidade Estadual Paulista, Instituto de Bioci^encias, Caixa Postal 73601, 11380-972, S~ao Vicente, SP, Brazil. Color versions of one or more of the figures in this article can be found online at www.tandfonline.com/brfs. yIn memoriam of Margarete Mallasen. © 2016 Taylor & Francis REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 265

be sustainable or may not even be conducted in an this review, polyculture is defined as the rearing of two environmentally and socially friendly way. or more species (e.g., prawns and ) in bodies According to the Food and Agriculture Organization without physical separation, whereas coculture is the (FAO, 2013), integrated aquaculture is defined as “aqua- rearing of two or more species in the same water body culture systems sharing resources (e.g., water, feeds, but incorporating physical separation (e.g., one species management, etc.) with other activities, commonly agri- in cages). cultural, agroindustrial, and infrastructural (wastewater, power stations, etc.).” Zimmermann et al. (2010) define Benefits of using freshwater prawns in integrated aquaculture as “systems that combine aqua- integrated aquaculture culture with the farming of terrestrial animals and plants.” These authors distinguish it from the term “pol- Freshwater prawns are a good option for integrated sys- yculture,” used to name the art of growing two or more tems, since they are omnivores and detritivorous and compatible aquatic species together in a single . have a benthic habit. Thus, they can take advantage of a These definitions have been largely used in aquaculture. wide range of feed wastes, either from aquatic or terres- In recent years, the expression “integrated multi-trophic trial species, which fall through the by aquaculture” (IMTA) has become popular to describe gravity and sediment at the bottom of the rearing sys- the farming of species from different trophic levels and tems. Furthermore, they have a well-defined spatial dis- with complementary functions. In IMTA, tribution in the environment, and occupy a slender layer uneaten allochthonous feed, wastes, nutrients, and by- in the bottom of the tridimensional space of aquatic sys- products from one species can be caught by other species tems. This avoids competition with various species of and incorporated in (Chopin et al., 2012; Cho- fish, and even allows association with plants. pin, 2013). This concept also includes polyculture. Thus, The addition of freshwater prawns to a culture system in our review, we consider fish-prawn polyculture as a may add value to the crop. Generally, fish, rice, and other form of integrated system, since it shares the available freshwater organisms have low market prices. Con- resources in a complementary way, unlike some polycul- versely, freshwater prawns attain a very high price; for ture systems, which involve two or more fish species that example, the global average in 2013 was US$ 5.23/kg compete for the same resources, rather than share them (FAO, 2015). The inclusion of a higher value species in complementarily. an aquaculture system can yield a significantly increased Sharing natural or allochthonous resources is a way of income for the farmer, even when an increase in produc- increasing their usage efficiency. Thus, integrated aqua- tivity does not occur (Zimmermann et al., 2010). Thus, culture systems are supposed to optimize the use of freshwater prawns provide high income even when resources, contributing to the conservation of finite natu- reared at low densities in fish or rice fields, ral assets. In addition, it is possible to exploit the syner- increasing total crop value. In addition, their use in inte- gistic interactions between the farmed species, leading to grated systems requires minimum alterations in facilities biomitigation processes. Consequently, integrated aqua- and management. New (2002) stated that the introduc- culture generally shows higher sustainability than other tion of prawns in paddy fields does not reduce the pro- Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 systems, as will be shown in this review. duction of rice; for example the profits from Vietnamese Integrated freshwater prawn farming includes various integrated rice-prawn culture can be two or three times farming systems, such as fish-prawn and rice-prawn cul- greater than from rice monoculture. ture, , and integration with terrestrial animals Generally, the performance of freshwater prawns is and plant crops. All these forms of integration can be affected only by their own stocking density and manage- profitable. The decision about implementing an inte- ment. It has been observed that the density of the fish grated system and the choice of integration type depend stocked together and the feeding or fertilizing regimes on the characteristics of the farm, the technical and eco- used for the costocking species has only a minor effect nomic viability of the integration and the existence of on freshwater prawns (Wohlfarth et al., 1985; Araujo technology and market niches for all the species pro- and Portz, 1997). Thus, rearing prawns in low density duced. A previous review of integrated freshwater prawn with fish or in rice paddies generally results in the pro- farming was providing by Zimmermann et al. (2010).In duction of large-sized prawns with high market value. this paper, available information has been updated, and The introduction of freshwater prawns into other cul- nomenclature has been standardized. The current review ture systems may even improve the performance of the focuses mainly on the great advantages of introducing costocking organism. Uddin et al. (2006) observed a pos- freshwater prawns into aquafarms previously operated itive effect of polyculture on the growth of both fish and using plants or other species. For the purposes of prawns. In addition, rice production in has 266 H. L. A. MARQUES ET AL.

been observed to increase in an integrated system available space and food can be optimized. Some fish (prawn-fish-rice) because the prawns and fish improve species, such as Nile tilapia (Oreochromis niloticus), silver fertility and promote an integrated pest management (Hypophthalmichthys molitrix), and (Ahmed et al., 2010; 2014). (Aristichthys nobilis) are filter feeders or actively eat In conclusion, there is great potential for rearing , whereas ( carpio) are freshwater prawns using the bottom of uncountable omnivorous and (Ctenopharyngodon idella) areas of tropical and subtropical fish ponds and rice are primarily herbivorous. Thus, these species in polycul- paddy fields around the world. This provides an oppor- ture with prawns take advantage of all these feeding tunity for fish and rice farmers to increase production niches (Malecha et al., 1981). In addition to increasing and profit with minor extra investment. Furthermore, total production in the pond, the fish in polyculture pre- this increased food production and profit is attained vent the excessive growth of phytoplankton, zooplank- without any additional use, saving the environment. ton, macrovegetation, and filamentous algae (Cohen Therefore, the use of freshwater prawns in integrated et al., 1983). systems has a great potential to increase , In polyculture, prawns can eat tilapia feces and improve local and global economy, and increase the unused fish feed (Santos and Valenti, 2002), while tilapia social, economic and environmental sustainability of filter phytoplankton (Perschbacher and Lorio, 1993) and aquaculture systems. In the following sections of this (Ibrahim et al., 2015), reducing the risk of review, the various systems in which freshwater prawns low dissolved oxygen levels at night. In addition, prawn may be incorporated are described, and the current sta- bioturbation at the pond bottom returns nutrients to the tus of practical integration and research is considered. water column (Kimpara et al., 2011), enhancing phyto- plankton production and consequently the natural feed available for the tilapia. Prawn larvae hatched inside Production systems suitable for freshwater ponds may also be filtered within the plankton and eaten prawn integration by tilapia (Guerrero and Guerrero, 1979). When kept in small tanks, tilapia (mainly fry) eat prawn postlarvae, Fish-prawn polyculture while large prawns may damage tilapia. Such agonistic New (2002) listed some synergistic beneficial effects behavior can be avoided by coculturing (confining one resulting from the inclusion of freshwater prawns in pol- species, e.g., in cages) and is considerably reduced in pol- yculture systems. These include the maintenance of yculture in large ponds because of the differing spatial more stable dissolved oxygen levels, reduction of preda- distribution of the species and/or size and stocking den- tors, increased feeding efficiency, increased pond sity management. Tilapia and prawns exploit different productivity, and a potentially increased total crop value niches in the pond environment, show positive syner- through the inclusion of a high-value species. Zimmer- gism and low antagonistic interactions; thus, they can be mann et al. (2010) highlighted the more rational use of cultivated together with success. the pond because of the different feeding habits of the Generally, prawns are stocked in polyculture systems species and the additional income from freshwater at lower densities than in monoculture, whereas the fish Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 prawns, which have high market value. The same are stocked at densities similar to their monoculture. authors, however, cautioned that proper knowledge of Therefore, prawn productivity is reduced in polyculture, the feeding habits of the species that are cultured with whereas the fish productivity is similar to that from the freshwater prawns is essential. As prawns are tropical monoculture. In this case, the emphasis of the polycul- animals, the fish to be reared with them must be adapted ture is on the production of fish, and thus fish are to warm ; thus, salmonids and other temperate referred to as the “main” species in the system (Cohen species are excluded. et al., 1983). Usually, only the fish are fed with commer- The commonest form of integrated fish-prawn culture cial pellets, while the prawns feed on waste feed, fish is within the same pond, where both prawns and fish feces, and/or on benthic organisms that grow on the grow together freely. The fish used should be pelagic, pond bottom, stimulated by nutrients present in the feces non-carnivorous and non-aggressive. In addition, the and excreta of the fish (Santos and Valenti, 2002). The culture cycle duration of the fish should be similar to prawns must be stocked first, followed 7–10 days later by prawns, to allow the stocking and harvesting of all spe- the stocking of fish. This simple procedure greatly cies simultaneously. The freshwater prawns walk/swim reduces the predation of juvenile prawns by fish (Santos and eat on the bottom, whereas pelagic fish mainly swim and Valenti, 2002). in the water column, feeding on floating artificial diets or A promising form of fish-prawn culture is the cocul- on plankton, suspended detritus, or aquatic plants. Thus, ture of caged fish and free prawns in the same pond REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 267

Figure 1. Coculturing of tilapia in cages placed inside prawn ponds in Brazil (photo by Helcio Marques).

(Rouse and Stickney, 1982; Tidwell et al., 2000, 2010; density (55.3, 54.0, 52.7, and 36.9% for 15, 30, 60, and 90 ¡ Danaher et al., 2007)(Figure 1). The fish receive artificial prawns m 2, respectively). These authors noted that the feed, but the prawns may or may not be fed, depending production from M. rosenbergii cultured in cages was on their stocking density. At low densities (< »80 g comparable to or even higher than those reported from ¡ m 2), prawns are normally not fed. In addition, the cages pond culture, given that the stocking densities used in and pens where the fish are farmed provide shelter and this study were generally higher than in ponds. In addi- substrates for the prawns, as well as additional feed due tion to grow-out, the freshwater prawn nursery phase to the periphyton that grows on those structures. Har- can be successfully carried out in cages inside ponds vesting is greatly facilitated since it is not necessary to using very high postlarval (PL) densities, such as ¡ separate the species manually (Danaher et al., 2007), and 1200 m 2, with high survival and profit (Marques et al., fish can be harvested regardless of the presence of the 2000; 2010; 2012). Cages may decrease the swimming prawns. Thus, the range of species that can be used in space available for pelagic fish, such as tilapia, but they this system is not constrained, and can potentially provide extra feed for the fish because of the periphyton include carnivorous fish and species with a culture cycle that develop on the cage structures and netting. On the shorter than that of freshwater prawns. Species with a other hand, cages may simply occupy vacant space in the long rearing cycle should be avoided because it is difficult pond culture of benthic fish, such as catfish. to harvest the prawns before the fish. The emphasis of Rearing fish at low densities in ponds where freshwa- this system may be placed either on fish or prawns, ter prawns are stocked at the same densities as in mono- Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 depending on the stocking density and management of culture has also been practiced. In this case, fish each species adopted by the farmer. maintain the ecological balance and good Rearing caged prawns and freely swimming fish inside the ponds without disturbing the prawns (Cohen within ponds is feasible, but not common. Prawn growth et al., 1983). Fish are much more efficient than prawns in inside cages may be reduced after maturation (Marques seizing feed pellets, and thus increasing their density will et al., 1998). Nevertheless, promising results were affect prawn feeding, decreasing production (New, obtained by Cuvin-Aralar et al. (2007) rearing M. rose- 2002). The marketable value of fish is normally lower nbergii in cages in a lake in the Philippines. In this study, than prawns; thus this form of polyculture does not juveniles (0.4 g) were cultured in 2.5 m £ 1m£ 1m greatly increase profits, but may be a way of improving cages at replicated stocking densities of 15, 30, 60, and pond water quality, controlling some predators or inva- ¡ 90 prawns m 2 of cage bottom. Mean sizes at harvest sive plants, providing an extra income through the sale after 5 months of culture ranged from 14.3 g for the of fish, or providing extra food for family consumption. highest stocking density to 26.3 g for the lowest. Mean size at harvest and daily growth rate were significantly Rice-prawn culture influenced by stocking density, with those at the lowest stocking density showing significantly better growth. The harvest of fish and prawns from inundated rice fields Survival substantially decreased in the highest stocking is an ancient and traditional practice in many Southeast 268 H. L. A. MARQUES ET AL.

Figure 2. Rice-prawn simultaneous culture. Prawns are stocked in the rice paddies together with the rice plants.

Asian countries (Das, 2002; Galib, 2010). The first fresh- stocked with juvenile M. rosenbergii (2–3 cm) at densities ¡ water prawn cultivation in rice fields appeared in Bangla- from 1.5 to 5 m 2 for 2 to 2.5 months (Figure 2). Simul- desh between the late 1970s and the mid-1980s (Ahmed taneous culture is performed during the monsoon season et al., 2010). During the last two decades, integrated (summer-autumn rice crop) and, after that, only rice is prawn-fish-rice farming has been expanded in Asia, cultured in the dry season. Productivity is low, ranging ¡ mainly because the export potential of M. rosenbergii from 40 to 500 kg ha 1, due to the small size of prawns and its high market value (Ahmed et al., 2010; 2014). at harvest and to low survival rates. Wild-caught juvenile prawns have been replaced by juve- In the simultaneous system, the rice paddies must be niles produced in ; allochthonous feeding adapted for prawn stocking. A trench (called a harvest occurs and water quality control is introduced, making channel) with a depth of 80–100 cm must be dug sur- the rice-prawn culture a commercial activity rather than rounding the rice field or along the dike near to the water an artisanal practice (Phuong et al., 2006). outlet point (Hung 2001)(Figures 2 and 3). This ditch is There are several interactions between prawns and essential for the harvesting of both prawns and rice rice in rice-prawn systems. The paddy fields provide because most prawns shelter in the channel when the flooded space, , and shelter against prawn preda- rice field is drained (Figure 4A and B). After the rice has tors, keeping the water temperature at tolerable levels in been harvested, the level of water may be increased again the hot summer months (Ahmed and Garnett, 2010). In to allow the prawns to eat the leftover by-products of the turn, prawn and fish wastes increase the amount of rice culture (Figure 4C). In addition, the level of the dikes organic material in the rice fields, decreasing the neces- must be increased to enable a raised level of water to sity for fertilization. Prawns also contribute to the partial »30 cm and individual systems of water inlet and outlet control of some weeds, , and pests. If prawns are need to be built (Hung, 2001). Screens are provided to fed, feed waste decomposition results in the release of Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 nitrogen, phosphorus, and other elements important for fertilization purposes in rice culture. Rice paddies do not provide a totally safe environment for prawns and growth reduction or high mortality rates may occur because of temperature oscillations and predation (Boock et al., 2013, 2016). According to Phuong et al. (2006), there are two main forms of rice-prawn farming: rotational culture (alter- nate culture) and simultaneous culture (integrated farm- ing). The choice depends on farmer preference or the site characteristics. In the rotational system, prawns are reared in the monsoon season and rice in the dry season. The flooded rice fields are stocked with prawn PL or ¡ juveniles at densities of »3–12 prawns m 2 and harvest- ing occurs after 6–8 months, resulting in large prawns with 50–110 g body weight. Productivity is about 900 kg Figure 3. Rice-prawn culture in India showing the rice paddy and ¡ ha 1. In the simultaneous culture system, rice fields are the lateral trench (photo by Helcio Marques). REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 269

Figure 4. Rice-prawn culture crop management. Prawns shelter in the refuge (trench) when the rice field is drained (A). Thus, they can be harvested or selected and rice plants can be managed or cropped (B). After the rice has been cropped, the level of water may be increased again to allow the prawns to eat the leftover by-products of the rice culture (C).

prevent the escape of prawns. In Bangladesh, these modi- Rinehart, 2010). In this system, nutrient-rich effluent fied rice fields are referred to as ghers (Ahmed et al., from aquaculture is used for hydroponic vegetable pro- 2010). The gher system has also been described as an duction. In turn, plants and rhizobacteria remove ammo- enclosure made for prawn cultivation by modifying rice nia, nitrates, nitrites, and phosphorus from the water fields through building higher dikes around the field and before it is recirculated back into the prawn tanks. In excavating a canal inside the periphery to retain water addition, prawns control pests and remove wastes from during the dry season (Ahmed and Garnett, 2010). the tanks. Aquaponics may be a great opportunity for The gher system is a combined form of agriculture and urban and suburban family food production because it aquaculture, incorporating the joint operation of three requires little space. The main components of aquaponic enterprises: prawn, fish, and rice production (Rahman units are a hydroponic container, where plants grow, a Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 et al., 2011). In addition, a variety of small-scale vegetables prawn-fish tank, a mechanical filter and a biofilter. and fruits are produced on the dikes.Thisincludescarrot, Pumps are used to circulate water throughout the various tomato, onion, mustard, long yard bean, spinach, pea, units. potato, sweet gourd, cucumber, chilli, and some short- According to Somerville et al. (2014) prawns are cycle fruits such as banana, papaya, and guava (Ahmed very suitable for inclusion in aquaponics systems et al., 2008c; Barmon, 2014). Gher systems can use either simultaneously with mid-water fish. They consume freshwater, when only freshwater prawns are farmed, or uneaten fish feed and suspended and benthic organic brackishwater when marine shrimp are included (Barmon wastes. Thus, they accelerate organic matter decom- et al., 2006). This system had been expanding rapidly in position and contribute to the health of the system. the coastal areas of Bangladesh and has had significant Some systems with tilapia have been tested with impacts on the agricultural characteristics and economy success. of Bangladesh (Rahman et al., 2011). The selection of plant species adapted to aqua- ponics is necessarily related to prawn stocking density and the consequential nutrient concentration of efflu- Aquaponics ents. Lettuce, herbs, and greens (spinach, chives, basil, Aquaponics links recirculation aquaculture with hydro- and watercress) have low to medium nutritional ponic vegetable, flower, or herb production (Diver and requirements and are well adapted to aquaponic 270 H. L. A. MARQUES ET AL.

systems. Nevertheless, the nutrient composition of the Polyculture of prawns with other crustaceans effluent may not fully match the requirements of Martino and Wilson (1986) observed in laboratory these plants; thus, an additional nutritive solution experiments that the freshwater prawn. M. rosenbergii, may be required. and the red swamp crayfish, Procambarus clarkii, showed compatible behavior to be reared together. Intercropping Other crops with these species has been described only in the United States in the 1990s (D’Abramo and Daniels, 1992). No The simplest and earliest form of integration with the further information is being reported on this topic in farming of terrestrial plants other than rice is the use of aquaculture literature nowadays. The polyculture of pond banks (bunds) for planting small trees such as marine shrimp (Litopenaeus vannamei or bananas, coconut, and papaya. Such integrated systems monodon) and freshwater prawns is sometimes per- optimize the space available in paddies and pond layouts formed in paddyfields or in polyculture with fish in Asia and provide an extra income derived from fruit produc- (Azim et al., 2001; Schwantes et al., 2007; Ali et al., 2009; tion. Nevertheless, New (2002) stated that large trees or Belton et al., 2009). For example, Azim et al. (2001) plants with extensive root systems planted on top of the reported the existence of mixed culture of M. rosenbergii bunds may damage them and cause leakage. Prawn pond and tiger prawns () in brackishwater, effluent can be used for the fertilization/ of but the survival of M. rosenbergii was low (23–37%). Fur- crops such as greens, vegetables or fruits (New, 2002). ther examples of the incorporation of marine shrimp in Effluent water is rich in nutrients, such as nitrogen and polyculture systems in Bangladesh are provided later in phosphorus and can thus increase , especially this review. when crops are able to absorb nutrients rapidly, as is the case with vegetables and herbs. Fish-prawn polyculture and coculture A large variety of fish may be reared together with fresh- The integration of prawn culture with livestock produc- water prawns in the same ponds. The choice depends on tion enables the use of animal feces and excreta for pond the region and the availability of fry or fingerlings. New fertilization and provides other benefits. This type of (2002) relates that around the world various freshwater integration may include pig, , goat, sheep, chicken, prawn species are polycultured with single or multiple and duck production. In the case of pigs, their feces may species of fish, including ; common carp (Cypri- be used directly as feed, because of they contain 70% nus carpio); Chinese — (Hypophthalmic- digestible food (Tripathi and Sharma, 2001b; Hung, thys molitrix), bighead carp (Aristichthys nobilis) and 2001). In addition, the pigsty can be built over the ponds grass carp (Ctenopharingodon idella); Indian carps— or on the bunds, optimizing space utilization. Cattle and catla (Catla catla), rohu (Labeo rohita) and mrigal (Cir- chicken manure is readily available and may be added to rhinus mrigala), golden shiners (Notemigonus crysoleu- freshwater prawn ponds for fertilization. Goats and cas), mullets (Mugilidae), tambaqui (Colossoma spp.), Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 sheep may be allowed to graze on the grass of the bunds, and some ornamental fish. Recently, New and Valenti thus contributing to efficient facility maintenance. Prawn (2016) extensively examined the scientific literature on ponds may provide space for ducks to swim; in turn, the polyculture of freshwater prawns with tilapia species ducks will fertilize the ponds, control invasive plants, (mainly Nile tilapia); their conclusions are recorded later and loosen the pond bottom, releasing nutrients from in section “Status of research on integrated freshwater the soil and aerating the water through their swimming prawn farming” of this review. activities (Tripathi and Sharma, 2001a). These examples Carp polyculture has been a traditional practice in indicate that integrating prawn culture with livestock some Asian countries, mainly Bangladesh and India. farming may be environmentally sound and increase This generally involves a combination of the three Indian profits. major carps with three or four species of Chinese carps. The introduction of prawns into carp polyculture is a practice that only started to be investigated in the 1980s Status of integrated freshwater prawn farming (Alam et al., 2001; Rahman et al., 2010a). The polycul- globally ture of carps with freshwater prawns, tilapia and mola The status of a wide range of systems that are currently (Amblypharyngodon mola, an indigenous phytoplankton used in the integration of freshwater prawns within pro- grazing species) has been reported to be more profitable duction systems is considered in this section. than traditional carp polyculture or monoculture REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 271

(Hossain and Islam, 2006; Kunda et al., 2008; Rahman sometimes stocked at densities of 100–500 fingerlings ¡ et al., 2010a; Shahin et al., 2011). This is because of the ha 1 to manage excessive algal blooms (Nair and Salin, higher value of freshwater prawns than the fish and indi- 2006). Nair and Salin (2007) described the use of M. cates that the polyculture of carps and freshwater prawns rosenbergii in polyculture of carps in India. The polycul- ¡ may expand in the future. ture of catla, stocked at 500 fish ha 1 with M. rosenbergii In Bangladesh, M. rosenbergii is commonly known as is practiced in Andhra Pradesh and other States in golda. The polyculture of golda with Indian and Chinese paddy-prawn rotational cropping. Some polyculture sys- carps has increased in the northern region since the tems stock grass carp, catla and rohu in paddy fields at ¡ ¡ 1990s and has popularized freshwater prawn culture 1500 fish ha 1 and prawns at 2 m 2. In , small among existing fish farmers (Hossain and Islam, 2006). and medium size irrigation reservoirs are frequently Al Noor (2010) has reported that some farmers formerly used to produce Indian major carps and M. rosenbergii. practicing freshwater prawn monoculture have started to Some farmers include bottom-feeding freshwater prawns incorporate four species of native and exotic carps. These in place of common carp and mrigal. ¡ typically have about 1,500 m 2 of water surface, Radheyshyam (2009) reported that in Orissa districts, which is generally stocked with 20 rohu, 40 silver carp, 5 M. malcolmsonii is reared in polyculture with carps such bighead carp, and 2 grass carp (about 200 g each). The as catla (surface feeder), rohu (column feeder), and grass carps are stocked one or two months after the prawns. carp (plant eater). Silver carp can be incorporated into Coconut leaves are placed inside the ponds as shelters the species mix when ponds have an abundance of phy- for the growing postlarvae and for prawns to seek refuge toplankton, but carps such as mrigal and during molting. Commercial feed and farm by-products common carp are not used in prawn polyculture. Prawn are supplied for both fish and prawns. Harvesting occurs production varies according to the level of management, ¡ from June to November after 5–6 months stocking. By but can reach more than 700 kg ha 1. In addition to the ¡ this time, most prawns and carps attain 80–100 g and prawns, 3000–4000 kg ha 1 of carps can be also pro- 700–850 g, respectively; total fish and freshwater prawn duced under semi-intensive management practices. production reaches »250 kg/farm (1.66 t/ha). The major Extensive polyculture of carps and M. rosenbergii and constraints are an insufficient supply of PL and the high M. malcolmsonii has been performed in India. Laxmappa cost of artificial feed. Species composition and stocking and Krishna (2015) reported that stocking M. rosenbergii densities are found to be important factors for maximiz- PL in the Malampuzha reservoir in Kerala yielded signifi- ing carp production in polyculture with prawns (Islam cant results, with prawn production ranging from 10 to et al., 2008; Rahman et al., 2010b). 83 kg/ha/year. In addition to the prawns, carps are also Carps are the most commonly fish used in polyculture produced in the same system. There is no uniform with freshwater prawns in Bangladesh, but other species growth in freshwater prawns; the harvest sizes range have aroused the interest of producers, such as Thai from 40 to 110 g each, due to seed quality and the quan- panga (Pangasius hypophthalmus) (Islam et al., 2008) tity stocked in the reservoirs. The same authors reported and Nile tilapia (Uddin et al., 2006, 2007a, b & c, 2008, that extensive polyculture has been practiced in the Koil- 2009; Asaduzzaman et al., 2009a & b). Tilapia have sagar reservoir (Telangana State, South India) since Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 greater market acceptance, are easy to farm, and their 2002, with carps such as catla and rohu stocked at very culture cycle is similar to freshwater prawns (Uddin low densities with prawn juveniles collected from wild et al., 2007c). The movement of tilapia inside the ponds sources (M. malcolmsonii) or produced in hatcheries (M. promotes soil resuspension (Jimenez-Montealegre et al., rosenbergii). In this system, water quality, prawn growth 2002). This process may increase benthic dissolved oxy- and health were not monitored, and supplementary feed- gen availability, leading to better mineralization and ing and organic were not applied. Hence, stimulating the natural food web. Asaduzzaman et al. prawn production was also limited to »10–12 kg/ha/ (2009b) concluded that polyculture with tilapia in the year and fish production was only »75–90 kg/ha/year. presence of periphyton substrates was more profitable In the year 2013–2014, the prawn production of the than prawn monoculture. entire reservoir was of 9.68 t. In India, the polyculture of M. rosenbergii and M. New (2002) provided some technical information on malcolmsonii with Indian carps started to be practiced in polyculture systems in China involving M. rosenbergii. the 1990s in the northern parts of Karnataka, Andhra When the emphasis of polyculture is on the prawns, Pradesh, Orissa, West Bengal, and Punjab, because of the juveniles of M. rosenbergii are stocked with 1–1.2 cm (at ¡ ¡ higher profit achieved when compared to carp or prawn 16.5–22.5 m 2) or 1.5–2.0 cm (at 15–18 m 2), while big- monoculture (Vasudevappa et al., 2002). Even in fresh- head and silver carps (12–15 cm) are stocked at 1500– ¡ water prawn monoculture, Indian carps such as catla are 1800 ha 1. Production of prawns and carps range from 272 H. L. A. MARQUES ET AL.

¡ 1500 to 3000 kg ha 1 per crop and from 750 to 1500 kg single cycle. The normal productivities achieved are gen- ¡ ha 1 per crop, respectively. When the emphasis is on erally »10–12 t of tilapia and 500–600 kg of prawns per ¡ carp production, freshwater prawns are stocked as PL at hectare per cycle. Currently, 4–8 Nile tilapia m 2 and 4– ¡ ¡ 24–30 m 2, or as 1.0–1.2 g juveniles at 4.5–9.0 m 2,or 10 prawns are sometimes used in Parana and S~ao Paulo ¡ as 1.5–2.0 cm juveniles at 3–6m 2, while carps with a States (F. Sussel, personal communication, 2015). Besides ¡ size of 3–4 cm are stocked at 16.5–21 m 2. In this case, tilapia, grass carp and bighead carp are also used in the production per ha per crop ranges from 450 to prawn polyculture in the States of Santa Catarina and 750 kg of prawns averaging 20 g and from 5000 to Espirito Santo. In these cases, prawns are the main spe- ¡ 7500 kg of juvenile carp with 12–15 cm body length. cies, being stocked at normal densities (10–12 m 2) and Feed is supplied to the prawns, varying from 20 to 5% of provided with a pelleted feed, while carps are introduced ¡ prawn biomass, being spread around the pond. Shelters at 0.2 m 2 with the aim of controlling invasive weeds for the prawns, such as aquatic weeds, grasses, and tree and filtering the excess of phytoplankton. Some pro- branches are placed in the ponds. Partial seine harvests ducers have substituted carps by tilapia at the same den- are taken and at the final harvest, fish are firstly removed sity, since the latter have a better market value. with a large-mesh seine before the pond is completely Apparently, tilapia does not compete with prawns for drained. More recently however, Ming (2014) noted that artificial feed at these densities. the polyculture of prawns with fish in China is a minor Prawn polyculture in is uncommon, being activity and often restricted to experimental research. practiced by less than 10% of farmers in mid-2000s Personal contacts in 2014 by New & Valenti (2016) indi- (Schwantes et al., 2007). Some prawn producers have cated that there is now little or no activity of this type stocked tilapia in their systems, but prawns are the main either in China or in . crop, whereas M. rosenbergii are stocked in tilapia ponds Polyculture is still not common in Brazil but has at low densities to provide an additional high value crop potential for expansion, since the low profitability of fish (Belton et al., 2009). This practice was a response to the culture causes hundreds of hectares of ponds to be reportedly declining profits of Thai tilapia farmers. unused all over the country; these could be used for poly- In the Philippines, some farmers polyculture M. rose- culture (Marques and Moraes-Valenti, 2012) and for nbergii with milkfish, Chanos chanos (Rola, 2007). increasing sustainability (Marques et al., 2013). Until Prawns (average stocking size of 3 cm) are normally 2007, polyculture occurred only in the State of Parana, stocked before the milkfish (average stocking size 10 cm) southern Brazil, but nowadays occurs in at least four and the average culture period traditionally adopted is States in the South and Southeast regions. In Parana, four months for both milkfish and prawn production, Barreto et al. (2009) stated that the polyculture of tilapia with two cycles per year. The average stocking rate for and prawns (M. rosenbergii) was becoming much more milkfish varies according to the system adopted; how- ¡ ¡ popular among the tilapia producers. Prawns have a ever, for prawns the stocking rate is »27,000 ha 1yr 1. higher commercial value than fish and thus the eco- Polyculture provides additional income for fish farmers nomic return from polyculture was higher than from because of the high market value of prawns. Neverthe- tilapia monoculture. Furthermore, some farmers say that less, some farms believe that the adoption of polyculture Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 polyculture improves the quality of water in the ponds. needs financial support. This has constrained the poly- Valenti and Tidwell (2006) reported that ponds are culture of fish and freshwater prawns in the Philippines. ¡ stocked at 2–4 PL or juveniles m 2. After a week, tilapia In Egypt, El-Sheriff and Mervat (2009) reported the ¡ juveniles weighing around 10 g are stocked at 1–3m 2. existence of commercial polyculture of prawns with Nile Only tilapias are fed with commercial pellets: the prawns tilapia. New and Kutty (2010) reported that prawn feed on benthic organisms and feed residues. Harvesting were introduced into Egypt from occurs after 5–8 months and tilapia productivity is not and Thailand in 1987–1988. Production was said to have affected by the presence of freshwater prawns. Polycul- peaked at 10.5 t in 1996 and comprised 7 t from mono- ture is profitable: the internal rate of return (IRR) was culture, 3 t from polyculture with Nile tilapia, and 0.5 t estimated to be 15–45% and the payback period (PP) from experimental integrated farming (rice, fish, and 3–6 years in the mid-2000s. prawns). By 1999, the only remaining farm, with a total It has been reported (E. Ballester, personal communi- area of 1000 ha, which had 51% government and 49% cation, 2013) that the producers in Parana State were private ownership and primarily reared , tilapia, stocking prawns and tilapia at higher densities (6–10 bream, sea bass, and marine shrimp, was still using ¡ prawns and 2–3 Nile tilapia m 2) and that the best yields about 5 ha to rear a small quantity of M. rosenbergii in achieved were 16.6 t of tilapia (average size 500 g) and polyculture with tilapia and mullet. By 2007, all the pri- 750 kg of prawns (average size 25 g) per hectare in a vate sector freshwater prawn hatcheries had closed due REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 273

to technical and economic factors and the lack of demand for PL. Prawn culture is almost at a standstill despite promising beginnings and no actual polyculture with tilapia is taking place (S. Sadek, personal communi- cation, 2014). There are also reports about commercial or experi- mental prawn polyculture with tilapia in (Valenti and Tidwell, 2006), USA (Rouse and Stickney, 1982; Tid- well et al., 2000, 2010; Danaher et al., 2007), Puerto Rico (Garcıa-Perez and Alston, 2000; Garcıa-Perez et al., 2000) and Brazil (Valenti and Moraes-Riodades, 2004; Santos and Valenti, 2002; Marques and Moraes-Valenti, 2012). There is a large amount of data on pelagic fish and prawn polyculture that supports the conclusion that nei- ther species affects the other inside the same pond. Figure 5 shows that the growth, survival and yield of tila- pia does not change as prawn density increases. Figure 6 shows that the same occurs with prawns as tilapia den- sity increases. In prawn monoculture, on the other hand, both growth and yield are markedly affected by prawn density (Sampaio and Valenti, 1996; Valenti et al., 2010). Prawn production is related to tilapia production when only tilapia are fed (Figure 7). This reinforces the ratio- nale that prawns eat the wastes generated by tilapia. Commercial fish-prawn polyculture is still relatively uncommon beyond Asia, despite the substantial science- based knowledge available (Zimmermann et al., 2010). New (2002) suggested that the management of this poly- culture species combination system might be complex, mainly with respect to the lack of synchronicity in har- vesting operations; however, this problem has not been specifically reported in the literature. It seems that the major constraints to the expansion of polyculture in Asia Figure 5. Variation of tilapia instantaneous growth rate (IGR), sur- and are the same as those for prawn vival, and yield according to prawn stocking density in tilapia- monoculture, i.e., poor transfer of technology, deficien- prawn integrated culture around the world. Data points were Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 cies in PL supply, lack of capital, and undeveloped obtained from the articles cited in the text. The dashed lines rep- r D marketing. resent the mean values of the dependent variable. Pearson correlation coefficient.

Rice-prawn culture rice-prawn farming, performed at the southwestern Currently, commercial rice-prawn or rice-fish-prawn higher areas. These include Bagerhat, Khulna, Jessore, culture is already commonplace in several Asian Barisal, and Satkhira districts (Ahmed et al., 2008c). countries, such as Bangladesh, where rice-prawn cul- In these regions, the practice of small-scale prawn ture is well developed, playing an important role as farming in paddies is widespread due to the availabil- an economic and social activity. In other countries, it ity of wild freshwater prawn PL, rice fields, a warm has great potential to expand because of the huge climate, fertile soil, and cheap and abundant labor. amount of available paddy field areas. In Bangladesh, Thousands of farmers from that region have con- prawn-rice culture is mainly performed in ghers verted their rice fields to accommodate profitable (Ahmed, 2009;Ahmedetal.,2008b).Barmonetal., prawn culture (Ahmed et al., 2010, 2014). In the (2004, 2006) reported two main types of gher farm- lower areas of Bagerhat, M. rosenbergii is farmed with ing: the brackishwater based per- the penaeid shrimp bagda (Penaeus monodon), the formed in the coastal region and the freshwater based Indian carp’s rohu, catla, mrigal, and silver carp. This 274 H. L. A. MARQUES ET AL.

Figure 7. Relationship between prawn yield (Py) and tilapia yield (Ty). ln D natural logarithm; r2 D coefficient of determination.

pest control and soil fertilization (Ahmed et al., 2010). Freshwater prawn-rice integrated culture may be more sustainable system. Barmon et al. (2006) concluded that in Bangladesh brackishwater shrimp-gher farming causes and has a negative impact on the environment, livestock, and water quality, whereas the rice-prawn freshwater gher farming system is friend- lier to the environment, land and water quality, besides helping to alleviate poverty due to the social inclusion of marginal and landless farmers in the system. Ahmed et al. (2012) suggested that rice-fish-prawn farming might form part of a “blue-green” revolution to increase food production in Bangladesh. Coastal aquaculture, which is dominated by export-oriented freshwater prawn and brackishwater shrimp farming (Ahmed, 2013)is threatened by . Ahmed et al. (2014) pro- posed that integrated prawn-fish-rice farming could be relocated from the coastal region to less vulnerable Figure 6. Variation of prawn instantaneous growth rate (IGR), inland areas, but cautioned that this would require survival, and yield according to tilapia stocking density in tilapia- appropriate adaptation strategies and an enabling insti- Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 prawn integrated culture around the world. Data points were tutional environment. Ahmed et al. (2010) reported that obtained from the articles cited in the text. The dashed lines rep- fi r D the annual yield average of prawn in rice elds was resent the mean values of the dependent variable. Pearson ¡1 ¡1 correlation coefficient. 467 kg ha , ranging from 387 to 564 kg ha (small [up to 0.20 ha] and large [above 0.40 ha] farmers, respec- tively). Kamal (2010) reported prawn productivities ¡ polyculture is performed in fresh to hyposaline water from 375 kg ha 1 in farms larger than 2 ha to 800 kg ¡ (0–3 salinity), integrating marine shrimp, freshwater ha 1 in farms between 0.8 and 2.0 ha. Prawns are fed prawns, and fish with low salinity tolerant paddy either with farm-made feed or commercial pellets, sup- (BR-23, BRRI-27, 40, and 41) and vegetables reared plemented with a variety of other feeds; the preferred onthedike(Alietal.,2009). In this way, prawn-rice type is the snail Pila globosa, harvested from the flood- culture allows the economic use of the thousands of plains in large quantities. A range of fish species is com- hectares of rice fields that remain waterlogged for monly polycultured with the prawns in rice fields, such four to six months of the year because of the mon- as Indian major carps (catla, rohu, and mrigal) and soon in the upper areas or the intrusion of saline exotic carps (silver carp, grass carp, and common carp) water in coastal areas; this improves food security (Ahmed et al., 2008a). The carps are stocked one or two and the socioeconomic conditions of farmers and months later than prawns, generally at »14,000–20,000 ¡ ¡ promotes the production of rice through biological prawn PL ha 1 and 400–570 fingerling carps ha 1 REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 275

(Kamal, 2010). According to Ahmed et al. (2010), the such as resources, weak transforming structures and pro- average stocking density of the carps is 2450 fingerling cesses, vulnerability context, poor institutional support, ¡ ¡ ¡ ha 1 yr 1 and of the prawns is »18,000–26,000 PL ha 1 and lack of extension services (Ahmed et al., 2008a). ¡ ¡ ¡ yr 1. Productivity varies from 387 kg ha 1 yr 1 in farms Moreover, an insufficient supply of wild PL and disease ¡ of up to 0.2 ha to 564 kg ha 1 year in farms above 0.4 ha; problems have been identified as major bottlenecks in ¡ ¡ fish productivities are reported as 703 kg ha 1 yr 1 the development of the activity (Ahmed and Flaherty, ¡ ¡ (small farms) and 1271 kg ha 1 yr 1 (large farms). Cur- 2013; Ahmed et al., 2008c, 2014). To resolve these issues, rently, the production of prawns aims to supply the it is necessary to explore the possibility of developing international market due to their high product value, prawn hatcheries closer to on-growing areas, thus avoid- whereas rice and fish are preferred for household ing dependence on wild seed and the appearance of dis- consumption. eases; this would ensure more sustainable and resilient The yield of rice under gher farming is the same or integrated prawn-fish-rice culture (Ahmed et al., 2008a, higher as the yield from rice monoculture in Bangladesh. 2014; Ahmed and Flaherty, 2013). Despite the con- According to Mohanty et al. (2004), the increase in rice straints identified, Ahmed and Flaherty (2013) con- yield under rice-fish-prawn integration was probably due cluded that the of prawn-fish- to the presence of fish and prawns, since their movement rice farming in southeast Bangladesh had great potential helps to improve dissolved oxygen levels and stirs up soil for improving the food security of farming households, nutrients, making them more available for rice. In addi- and more broadly the economic growth of the country tion, fish and prawns help to enhance soil organic mat- through earnings from the export of prawns. ter/nutrient status by adding fecal matter and may In , rice-prawn farming is one of the most control plankton population and aquatic insects, in addi- important models of prawn production. This system is tion to removing and organic detritus that com- widespread in the Mekong Delta region. Similarly to pete with rice for nutrients and . This system Bangladesh, Vietnamese rice-prawn farming is per- therefore provides a sufficient amount of rice to meet formed simultaneously (where prawn and rice cultures local demands and simultaneously produces a high value are carried out together as mixed farming) or in an alter- species (M. rosenbergii) with good market demand. Bar- nate manner (where prawn culture and rice cultivation mon et al. (2004) found that the gher farming system are carried out on a rotational basis). Productivities vary increased labor demand compared to rice monoculture. according to the initial size of postlarvae or juveniles, Furthermore, the feasibility of using freshwater prawns stocking densities, and food management, ranging from ¡ ¡ in polyculture with fish allowed the farms to obtain addi- 40 to 500 kg ha 1 and from 360 to 900 kg ha 1, for tional fish for home consumption, and also created more simultaneous and alternate systems respectively (Phuong job opportunities for family laborers, benefiting the local et al., 2006). Hai et al. (2015) stated that prawns are cur- ¡ population and neighboring communities. Bangladesh is rently stocked at densities of 1–2m 2 and production is ¡ ¡ considered by Ahmed (2009), as one of the most suitable about 50–100 kg ha 1 crop 1. countries in the world for integrated prawn-fish-rice Duong (2001) described the main steps that were farming, because of its favorable agroclimatic conditions. employed in rice-prawn culture in the Mekong Delta Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 Consequently, integrated prawn farming has been one of region 16 years ago. These included the advice that dikes the most important sectors of the national economy must be sufficiently high and strong to resist floods; (Ahmed, 2009; Ahmed et al., 2008b, 2014). Freshwater inside the paddies, the depth of water varies from 20 to prawns are known as “white gold” or “dollar” (Ali et al., 30 cm. In order to provide shelter during the rearing 2009), becoming in recent years the most desirable spe- period and to harvest the prawns, peripheral trenches cies in aquaculture (Ahmed et al., 2010; 2014). Ahmed (harvest channels) with 3.0–4.0 m wide and 1.0–1.2 m et al., (2014), stated that integrated prawn-fish-rice farm- depth are excavated. Nets or woven strips of bamboo are ing is the most efficient system in terms of utili- fixed at the inlet and outlet water pipes, in order to avoid zation through the complementary use of land and prawn escapes and to minimize the entrance of preda- water. Despite higher production costs per hectare, the tors. Prawn PL and juveniles are collected from the rivers average annual net return was higher in large farms and stocked directly in the paddy fields (resulting in low (US$2,426; farms >0.4 ha), compared to medium production cost). Residues or by-products of farming (US$1,798; 0.21–0.4 ha) and small (US$1,420; 0. 2 ha) and fishing (cassava, sweet potato, broken rice, soaked or farms (Ahmed et al., 2010). Prawn production in gher cooked milled rice, rice bran, , and snails) are sup- systems has been accompanied by a great deal of social plied to the prawns. Farm-made feeds consisting of 50% and economic benefits (Ahmed et al., 2010). Some con- rice bran, 10–20% cooked broken rice, 20–30% trash straints to long-term sustainability have been identified, fish, and 10% oil cake are also used. Fertilization is 276 H. L. A. MARQUES ET AL.

performed with organic and/or inorganic fertilizers and In northeastern India, Das (2002) stated that an indig- weed control is done manually, without using herbicides. enous traditional capture fishery system in rice fields pre- After 4–5 months of rearing, the rice field is drained and vailed at that time. Due to the gradual reduction of the prawns are collected in the harvest channels. natural stocking that they observed, these authors rec- Phuong et al. (2006) stated that during the dry season in ommended that the traditional wild capture system the Mekong Delta, the salinity of water is quite high, so some should be improved or replaced by adopting suitable cul- paddies can only be used to rear marine shrimp; however, in ture techniques that would increase yields, enhancing the inland floodplain and during the rainy season, rice-prawn socioeconomic development in rural areas. In Kuttanad, farming can also be practiced. Trenches usually occupy about State of Kerala, Kurup and Ranjeet (2002) reported that, 20–25% of the paddy area with an average depth of 0.8– as occurs in Bangladesh, the simultaneous culture of rice 1.0 m. Stocking density varies according to the production and prawns was substituted by the rotational farming of system: in the integrated rice-prawn culture system, stocking rice and M. rosenbergii. This occurred mainly because ¡ density ranges from 1.5 to 5 individuals m 2 depending on the double cropping of rice may not always be feasible prawn size; in the alternate rice-prawn culture model, the due to flooding during the monsoon season and to the ¡ stocking is done with M. rosenbergii PL at 3–12 m 2 in the high cost of land and labor. Rotational culture is not type 1 system, where one prawn crop and one rice crop are only helpful in improving farming revenue, but also pro- carried out in a year, or with 15 g prawn juveniles (stocking vides additional employment. This practice is beneficial rate not identified) in the type 2 system, where one prawn because it reduces the cost of pond fertilization, main- crop and two rice crops are carried out per year. Productivity tains soil fertility, avoids the accumulation of waste prod- ¡ ranged from »40 to >500 kg ha 1 in the integrated system, ucts, improves pest control, and enables farmers to ¡ and 900 kg ha 1 in the alternate culture type 1 and 360 kg continue with their traditional forms of livelihood. ¡ ¡ ha 1 in the alternate system type 2 systems, respectively. Lin Prawns are stocked from 1.5 to 6.0 m 2 in rice-prawn ¡ and Lee (1992) reported that the yield of prawns in rice inte- monoculture and from 0.2 to 1.5 m 2 in rice/prawn/fish ¡ ¡ gration ranges from 200 to 400 kg ha 1 in 8 months, with a polyculture (0.1–0.5 fish m 2). The productivity in gross annual income of US$ 600–1200. monoculture of M. rosenbergii ranges from 95 to 1300 kg ¡ ¡ Halwart and Gupta (2004) described the rearing of ha 1 while between 70 and 500 kg ha 1 of prawns and ¡ both M. rosenbergii and M. nipponense in rice fields 200 and 1200 kg ha 1 of fish (mainly catla, rohu, and in China. The physical preparation of the rice fields grass carp) are obtained in polyculture. Some integrated is the same as in other countries but thereafter sub- rice-prawn farms in Kuttanad that do not use chemical merged aquatic plants are planted in the trenches to fertilizers or pesticides have been certified as “organic cover one-half to one-third of the bottom. For M. farms” (Nair and Salin, 2009; Nair el al., 2014). These rosenbergii, the stocking rate of 1.5 cm sized juveniles authors reported that rice productivity decreased about ¡ is 3 m 2, while 4–6cmsizedM. nipponense may be 23% under organic farming; however, the organic prawn ¡ ¡ stocked at 3.0–3.8 kg ha 1 andallowedtobreed,or crop yield of 396 kg ha 1 was 10% higher than the yield ¡ ¡ juveniles are stocked at 23–30 m 2. Feeding consists of the conventional system (360 kg ha 1). Total invest- of soybean milk and fish gruel during the early stages ment for organic rice and prawns was approximately 20 Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 (seven to eight days after stocking) and high-protein and 17% greater than for the non-organic products. pelleted feed or a mixed diet of wheat bran or rice These higher costs were compensated for by the product bran with some animal protein source thereafter. M. values, which were 36 and 26% greater than conventional rosenbergii is harvested before the temperature drops products, respectively. Organic rice farming culture too low; meanwhile the harvest of M. nipponense can brings lower returns than the conventional system. The start on a selective basis by late November or early combination of organic rice farming with organic prawn December. The undersized animals are left to grow farming enhanced net revenue by 20% over conventional for the total harvest by May or June, which takes rice/conventional prawn production (Nair et al., 2014). place before the rice-planting season. Miao and Ge Halwart and Gupta (2004) stated that rice-fish farm- (2002) reported that usually only one crop of prawns ers in East Java () use M. rosenbergii in polycul- (300–450kg)isproducedperyearinChina,using ture with milkfish (Chanos chanos) and silver barb supplementary feeding in addition to the normal rice (Barbodes gonionotus), either in concurrent or rotational production. These authors pointed out that it is a systems. According to Giap et al. (2005), rice-prawn cul- very effective approach to improve the economic ture in Thailand is extensive, based on natural food. return from traditional rice cultivation and also has a These authors reported that the profits were 43–91% very sound environmental effect, due to the signifi- higher in rice-prawn culture than in rice monoculture, cantly reduced use of pesticides and other chemicals. probably because of the higher value of prawns REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 277

compared to the fish species usually cultured in rice common in Asian countries and also in the state of fields. Schwantes et al. 2007 noted that although the Espirito Santo (Brazil). The use of the effluent from fish monoculture of M. rosenbergii was well developed in and prawn ponds to irrigate the cultivation of greens, Thailand, crop rotation and integrated culture were rare fruits, and vegetables occurs, mostly in Asian countries, or non-existent, despite their huge potential. but this practice is increasing in and North Constraints to the expansion of rice-prawn culture in America (Diver and Rinehart, 2010). Lin and Lee (1992) Asian countries have been presented by several authors. reported the existence of vegetable-prawn integrated cul- According to Giap et al. (2005) the increasing use of pes- ture in areas converted from rice fields. This system con- ticides and chemicals in rice production is the main bot- sisted of ditches for prawn rearing and platforms and tleneck. Phuong et al. (2006) considered that there is a embankments for growing cucumbers, string beans, egg- danger that unit price would decrease with increased plants, and bananas, thus providing supplementary production and detrimental effects on the local environ- income as well as food for domestic consumption. ¡ ment would arise. Ahmed and Garnett (2010, 2011) and Prawns were stocked at 4–6m 2 and fed twice daily a Ahmed et al. (2010) reported a number of constraints mash of rice bran, cassava, and trash fish. Each 6 months, for rice-fish-prawn farming in Bangladesh, including a about 100 kg of prawns were cropped. Ahmed et al. shortage of operating capital, increased production costs, (2008a) stated that almost all gher farmers in Bangladesh lack of prawn PL due to the decrease in natural stocks, cultivate dike crops mainly for household consumption, an inadequate supply of snails for feed, prawn diseases, while 32% of farmers sold their crops in local markets. climatic disasters (flood and drought), and social con- During the winter season, different types of dike crops flicts. Nabi (2008) highlighted the fact that rice-prawn such as carrots, tomatoes, onions, mustard, and “yard- technology is still not structured to address the food long” beans were produced, while crops produced in the security goal of smallholders and therefore is adopted summer season included ladies’ fingers, sweet gourds only by those who are better placed to assume the risks and other vegetables. Most of the farmers (88%) pro- of the activity. Kamal (2010) included as constraints the duced more than three dike crops in different seasons, high costs of prawn PL and supplementary feed. Partial while the rest of the farmers produced three or less. solutions for these constraints would be the expansion of Fruits, such as bananas, papayas, and guavas are also cul- prawn hatcheries and the use of low-cost locally pro- tivated. Also in Bangladesh, Ali et al. (2009) studied six duced ingredients for feed other than snails; these commercial ghers (9.08 ha total area) and reported that improvements would help to increase production, reduce the total production of vegetables cultured along the negative environmental impacts, and increase job oppor- dikes of rice fields were: papayas (1,140 kg), eggplants tunities. Recent climate change has also been considered (750 kg), bitter melons (400 kg), ladies’ fingers (521 kg), a risk to growth in this activity (Ahmed et al., 2014). tomatoes (588 kg), peppers (108 kg), bottle gourds Boock et al. (2013) considered that the low level of water (998 kg), and pumpkins (1248 kg); these produced a total in Brazilian paddies may causes large temperature oscil- income of 3808 TK (US$ 48.70) per hectare per cycle. lations and possible prawn mortality, and that the only Aquaponic systems generally use fish species that adapt way to prevent this would be to restrict the period of to intensive recirculated aquaculture systems (RAS), Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 rearing to the warmer months of the year. including tilapia, , and perch. Most commercial aqua- In continents other than Asia commercial rice-prawns ponics systems in North America are based on tilapia, but systems have not been developed but the crawfish Pro- in barramundi (Lates calcarifer) is the species of cambarus clarkii has been reared in small- and medium- choice (Diver and Rinehart, 2010). As freshwater prawns scale in the Southeast of the United States, integrated with are rarely reared in RAS, their inclusion in aquaponic sys- rice or soybean production in alternate systems (McClain tems is still very restricted. There are records of aqua- et al., 2007).Theeconomicimportanceofthissystemin ponics systems that include tilapia in polyculture with M. that country is far from that existing in Asia. Some rosenbergii (Martan, 2008). Some aquaponics producers research on rice-prawn farming outside Asia will be pre- recommend rearing freshwater prawns at low densities sented in section “Status of research on integrated fresh- within hydroponics tanks for pest control, waste disposal water prawn farming” of our review. and as a source of extra income (Friendly Aquaponics, 2013; Somerville et al., 2014). The integration of fish-prawn polyculture with the Other integrated systems rearing of ducks, chicken, and pigs has been reported by There are some commercial initiatives involving the inte- Tripathi and Sharma (2001a, b) in some Asian countries, grated culture of freshwater prawns. The use of pond mainly in India and Vietnam, but occurs only in family- margins for planting bananas, coconut, and papaya is run systems. 278 H. L. A. MARQUES ET AL.

Status of research on integrated freshwater are stocked after the fry phase, generally at < 3 g (New prawn farming and Valenti, 2016). No injuries inflicted by prawns on tilapia have been described. Reduction in prawn survival, This section reviews the current published research when it occurs, is more likely to be caused by the inade- information on integrated freshwater prawn farming. quacy of the feed available to the prawns than by any direct aggressive action of the tilapia (except that of tila- Fish-prawn polyculture pia fry on prawn postlarvae). The use of male sex- Zimmermann et al. (2010) presented an extensive review reversed tilapia is highly recommended in polyculture. If of research on the polyculture of prawns with various they are not available, it is better to coculture the tilapia species of fish. This review included the aspects of man- in cages to avoid reproduction (fertilized eggs will fall agement, water quality, feeding, stocking strategies, and through the cage mesh and cannot be incubated in the profitability. This publication should be considered by mouth of the female). those who seek more details about these topics. Stocking density and the proportion of tilapia and More recently, New and Valenti (2016) reviewed the prawns stocked appear to be important factors (New and literature on the specific polyculture of freshwater Valenti 2016). The optima certainly depend on the site prawns with tilapias, and noted that a considerable characteristics (such as water quality and natural produc- amount of research on tilapia-prawn polyculture had tivity), the general management system utilized (such as been performed during the past four decades. Most the use of artificial substrates and aerators), and the papers on this topic concentrated on the giant river choice of the major species (tilapia versus prawns), which prawn (M. rosenbergii) and Nile tilapia (O. niloticus). will be determined by the characteristics of the intended The problem is that the available information is frag- market. Thus, it is difficult to generalize; the information mented and many important subjects are not covered at available is not sufficient to show a general picture. Most ¡ all. It is almost certain that prawns do not affect the per- research has been performed using 1–2 tilapia m 2 and ¡ formance of tilapia in earthen ponds and stocking them 2–4 prawns m 2. It is the total biomass of both species in such ponds may significantly enhance total revenues. rather than the individual numbers that should be con- According to New and Valenti (2016), polyculture is rec- sidered; this factor has been neglected by investigators. ommended for tilapia-pond culture farmers, who want The best situation would be to consider the amount of to retain tilapia as the major species. On the other hand, waste feed necessary for the prawns and to provide only the presence of tilapia in prawn ponds may reduce prawn the tilapia with floating pelleted feed. In this way, a real yield, but is unlikely to reduce profit. multi-trophic and multi-spatial equilibrated system The main constraint is the feeding of prawns when (IMTA) could be achieved. To obtain a sustainable polycultured with tilapia (i.e., free-swimming within the IMTA, information on natural biota and trophic chains ponds) (New and Valenti, 2016). Tilapia consumes pel- within ponds, energy and nutrient balances, and the leted feed very rapidly and eats much more than they management necessary to drive energy and key nutrients need for growth (superfluous feeding). Thus, prawns do (N, P, and C) to the target species should be determined. not have the opportunity to ingest the supplied pellets. These are important avenues for new research and could Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 In addition, supplying sinking pellets may attract tilapia allow the use of various natural within the ponds, to the pond bottom, which may create negative interac- thus decreasing the supply of allochthonous feed. This tions with the prawns. Thus, it is advisable for those who can also increase the environmental and economic sus- want to intensively feed prawns in order to obtain high tainability of the systems. prawn productivity to use the coculture technique (i.e., During the seventies and the eighties, some trials were stocking tilapia in cages within prawn ponds). It seems conducted in Israel and in the United States, focusing on that caged tilapia can improve water quality by filtering the polyculture of M. rosenbergii with a mixture of fish algae, mainly cyanobacteria, and provide residues, like species in ponds frequently enriched with manure (Buck feces and waste feed, which can be ingested by prawns, and Bauer, 1980; Malecha et al., 1981; Buck et al., 1981, thus reducing the quantity of commercial diet needed. It 1983; Costa-Pierce et al., 1984, 1987; Wohlfarth et al., is important to consider the local costs of cages. When 1985). The most common species of fish were carps (sil- contemplating the establishment of new tilapia-prawn ver carp, big head carp, grass carp, and the common farms, the comparative economics of rearing tilapia in carp) and tilapias. In research work carried out in the polyculture with prawns compared to coculture needs to United States, production of prawns varied greatly. Mal- be carefully assessed. echa et al. (1981) reported averages that ranged from 264 ¡ The stocking size in earthen ponds of both tilapia and to 414 kg ha 1 and Wohlfarth et al. (1985) obtained 66 ¡ prawns in polyculture seems to be irrelevant, since tilapia to 791 kg ha 1 of prawns. This huge variation in REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 279

production may occur due to the feed management sys- with freshwater prawns was strongly affected by its own tems adopted, based on water fertilization with manure stocking density and by the feeding-manuring strategy. that can differentially influence the primary production Karplus et al. (1987) stocked three fractions of size- in the ponds, as a function of diverse ecological interac- graded juveniles of M. rosenbergii in polyculture with tions. In other research, Costa-Pierce et al. (1984) related tilapia and carps (silver, common and grass) and that the polyculture of carps (silver and grass) with M. observed that the fraction of “upper” prawns (32% of the rosenbergii combined with reduced feeding rates may be total) resulted in a smaller proportion (8%) of small a simple solution to the pervasive problems of water males and higher proportion of blue-claws (22%), poten- quality control and benthic reducing conditions. Martino tially providing a net income almost nine times that of and Wilson (1986) noted that the interactions observed the control. Mires (1987) did not find significant differ- in the polyculture of M. rosenbergii, Mossambica tilapia ences in yield when stocking M. rosenbergii juveniles at ¡ and the crawfish Procambarus clarkii were intraspecific 5–7.5 m 2 in polyculture with Nile tilapia fingerlings at ¡ and that the cannibalism observed among the crusta- 0.6–0.7 m 2. Hulata et al. (1990) found that there was no ceans was not influenced by the presence of tilapia. Also significant effect caused by the age or size of juvenile M. Costa-Pierce et al. (1987) observed that the polyculture rosenbergii stocked on the production of prawns in poly- of M. rosenbergii with silver carp, grass carp and grey culture with tilapias ( and red) and carps (com- mullet (Mugil cephalus) resulted in a total production of mon, grass and silver). all species twice as high than in prawn monoculture, In Bangladesh, Haque et al. (2003) determined the even at a low feeding rate and despite the existence of optimum density of M. rosenbergii in polyculture with ¡ competition for resources among the species in catla, rohu and mrigal to be 6000 ha 1. In Pakistan, Mia polyculture. (2004) studied the effect of stocking prawns at three den- ¡ Also in the United States, Rouse et al. (1987) found sities (6000, 8000, and 10,000 ha 1) with a single fish ¡ that optimum prawn survival (93.8%) was attained at density of 5000 ha 1, using several carp species, such as ¡ low stocking densities (4 m 2) in polyculture and that silver carp (35%), catla (15%), rohu (30%), and mrigal tilapia reproduction had a negative impact on prawn (20%) in one experiment and silver carp (30%), catla growth. Scott et al. (1988) studied the polyculture of M. (15%), rohu (34%), mrigal (5%), grass carp (15%), and rosenbergii with the golden shiner Notemigonus crysoleu- (1%) in a second experiment. The best pro- ¡ cas, a cyprinid fish largely used as a bait fish, and found duction achieved was 122 kg ha 1 of prawns and ¡ that prawn yield was significantly higher in polyculture 4200 kg ha 1 of fish, corresponding to the initial prawn ¡ than in monoculture. On the other hand, shiner survival stocking density of 6000 ha 1 and four carp species in was significantly higher in monoculture and shiner yield the first experiment. It is notable that the temperature did not differ between monoculture and polyculture. dropped below 10C during the experiments, which cer- In Israel, the polyculture of prawns with several finfish tainly would have caused high prawn mortality. Simi- species, including carnivores, was commonplace in the larly, Hossain and Islam (2006) tested five stocking 1980s and the success of the stocking strategy was found densities of M. rosenbergii (2500, 5000, 7500, 10,000, and ¡ to depend on the use of compatible stocking sizes of each 12,500 ha 1) in polyculture with catla, rohu and silver

Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 ¡ species (Hulata et al., 1988). These authors recom- carp at fish densities of 2500, 5000, and 2500 ha 1, mended the introduction of carps and tilapias with respectively, during three months of culture in tempera- prawn juveniles weighing 0.25–0.50 g at a density of tures ranging from 27 to 31C. Prawn survival was ¡ 2m 2. This stocking density was also used by Karplus higher than 75% and fish »90%. According to these et al. (1987), who obtained prawn survival up to 87% authors, the overall total production of prawns and fish ¡ and yield among 332–560 kg ha 1 rearing juveniles of was significantly higher at prawn stocking densities of ¡ ¡ ¡ various sizes in 400 m 2 ponds in polyculture with tila- 7500 and 10,000 ha 1 (2916 and 2914 kg ha 1, respec- pias (Oreochromis sp.), common carp (Cyprinus carpio), tively) and the highest profit was obtained at a prawn ¡ silver carp, and grass carp. Cohen and Ra’Anan (1983) density of 10,000 ha 1. Prawn production increased with ¡ concluded that an increase in tilapia density had no density and varied from 86 to 361 kg ha 1. Hossain and influence on prawn yields or on the social structure of Kibria (2006) studied the polyculture of M. rosenbergii M. rosenbergii reared in polyculture with tilapia. Prawn with rohu and catla in ponds during the winter using for- yields and average weights were affected by the density mulated diets, obtaining a production of prawns ranging ¡ of the prawn population alone, and survival rates in all between 253.1 and 323.8 kg ha 1 in the five-month cul- cases were above 85% and unrelated with either prawn ture period. These authors concluded that the overwin- or tilapia stocking rates. On the other hand, these tering rearing of freshwater prawn/fish polyculture is authors found that the growth of tilapia when grown feasible; however, further study was thought to be needed 280 H. L. A. MARQUES ET AL.

to determine the optimum stocking density of M. rose- efficient, concluding that technical efficiency may only nbergii and carp polyculture, for these specific be a short-term concern and the farmers have to be eco- conditions. nomically efficient in the long term as well. Jana et al. (2007) found a significant reduction in Other technologies have been investigated and associ- mean counts of heterotrophic bacteria, ammonifying ated with the production of prawns in polyculture sys- bacteria, protein mineralizing bacteria, and nitrifying tems. Rahman et al. (2010b) determined the best ¡ ¡ bacteria in prawn-carp polyculture when compared to densities of silver carp (1500 ha 1) and catla (1000 ha 1) prawn monoculture or mixed-carp culture; this indi- in polyculture with mola and all-male M. rosenbergii. cated that there was less accumulation of uneaten Also Rahman et al. (2010a) found that selective prawn feed in the polyculture system when prawns were harvesting had a more beneficial effect than the ablation present. Siddique et al. (2010) studied the abundance of the chelae of M. rosenbergii males on prawn and fish of zooplankton and growth of M. rosenbergii in poly- (silver carp, catla, and mola) productivity. Kunda et al. culture with silver carp and catla, concluding that (2009b) found that all-male M. rosenbergii polyculture ¡ stocking prawns at 1.5 m 2 resulted in slightly higher with catla, rohu, and mola was economically more viable total productivity (fish plus prawns) than stocking than all-female and mixed-sex prawn polycultures. ¡ prawns at 1.0 m 2 for identical fish densities. Jahan Kunda et al. (2009a) studied the effects of including catla (2011) tested the effects of two types of feed (100% (Catla catla) and Nile tilapia in a prawn-mola polycul- rice bran and a mixture of 20% rice bran, 30% fish ture performed in rice fields after the harvesting of rice meal, and 50% oil cake) on the production of prawns (rotational rice-fish culture system). Mola (»2 g) plus ¡ and carp. Prawn productivity varied from 798 to prawns (»3 g) were each stocked at 2 m 2. The addi- ¡ 1089 kg ha 1 and the best results were achieved for tional stocking of either tilapia (»10 g) or catla (»43 g) ¡ the mixed diet. Jasmine et al. (2011) shewed that the at 0.25 m 2 increased total crop and profit. These polyculture of M. rosenbergii, catla and silver carp authors also reported that the introduction of catla was more economically feasible than the polyculture resulted in higher cost: benefit ratio and higher com- of carps alone (catla, rohu, mrigal, and silver carp). bined production of fish and prawns than the introduc- Pervin et al. (2012) reported that the inclusion of tion of tilapia or tilapia plus catla in the system. Tilapia ¡ mola at 2 m 2 in polyculture with M. rosenbergii did did not affect prawn size, survival, or productivity, but not affect the production performance and survival of significantly reduced the zooplankton and phytoplank- ¡ prawns stocked at 3 juveniles m 2.Ahsanetal. ton concentration in the water column, creating a better (2013) concluded that the introduction of rohu at a water condition for both fish and prawns. ¡ density of 500 ha 1 increased the net profitandthe The use of biofloc technology in M. rosenbergii-carp combined production of prawns and finfish in poly- polyculture was studied by Prajith (2011). This author culture systems of M. rosenbergii,silvercarp,catla, concluded that 25% rohu and 75% catla should be and mola. included in the system, since these species equally have In Bangladesh, Rahman et al. (2010a) stated that the ability to harvest the biofloc. Catla consumes the prawn juveniles were expensive inputs (about 47% of the plankton enhanced by the floc whereas rohu graze on Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 total cost) in all treatments, followed by prawn feed (16– the bacterial protein. 17%). About 70–77% of the total income was obtained The periphyton-based system is a promising tech- from the proceeds of prawn sales, despite the smaller nique that has shown benefits for tilapia (Oreochromis biomass of prawn production (31–37% of the total). In spp.) and M. rosenbergii in polyculture. In Bangladesh, another trial, Rahman et al. (2010b) studying the poly- Uddin et al. (2007b) found that the introduction of sub- culture of silver carp, catla, and all-male freshwater strates (bamboo poles) improved survival, final weight prawns, concluded that although the prawn biomass gain and net yield of both tilapia and prawns. In this (38%) was smaller than the fish (62%), its value was experiment, 1.8 g fingerlings of Nile tilapia were stocked ¡ ¡ higher, resulting in about 76% of total benefit. Similar at 2 m 2 and 30-day juvenile prawns at 2 m 2 during results were obtained by Hossain and Islam (2006): the 145 days in experimental ponds. Substrate addition highest profit was obtained in the treatment with a resulted in a 46% higher production of tilapia, while ¡ prawn stocking density of 10,000 ha 1, probably due to prawn production increased by 127%. The authors also the higher production of prawns and their high sale val- concluded that prawns did not affect tilapia performance ues. Alam and Murshed-e-Jahan (2008), evaluating the and that there is a very low dietary overlap between the technical and cost efficiency of prawn-carp systems of two species. Uddin et al. (2006) studied the polyculture 105 farmers of Bangladesh, reported that 50% of farmers in a substrate-based system of genetically improved displayed full technical efficiency, but only 9% were cost farmed tilapia (GIFT) and prawns, determining that the REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 281

best stocking ratio was 75% GIFT and 25% prawns, in of 150 g for males and 50 g for females. Mohapatra et al. terms of productivity and economic return. Uddin et al. (2007) found that the polyculture of carps with M. rose- (2007a, c), examining the effect of three total stocking nbergii indicated that higher production levels of 202% ¡ densities—20, 30, and 40 m 2, (each at a 3:1 tilapia: for fish and 156% for prawn could be achieved in green- ¡ prawn ratio)—found that 30 m 2 produced a the best house ponds as compared with outdoor ponds. Soundar- ¡ ¡ net yield (2209 kg ha 1 of tilapia and 163 kg ha 1 of apandian et al. (2008) found that the best stocking prawns) and cost-benefit ratio. densities for the polyculture of M. rosenbergii ¡ ¡ Uddin et al. (2008), studying the combined effects of (25,000 ha 1) and Indian carps (10,000 ha 1) resulted in ¡ periphyton, tilapia, and prawn stocking densities and the production of 381 kg ha 1 of prawns and 500 kg ¡ feed on pond water quality, concluded that the use of ha 1 of fish. substrates for periphyton growth was a low-cost culture The polyculture of M. rosenbergii with channel catfish method that results in a more favorable environment for Ictalurus punctatus has been experimentally studied in the cultured organisms. This resulted from the avoidance the United States. Huner et al. (1983) reported that when ¡ of organic loading and the simultaneous provision of an prawns were stocked at 25,000 ha 1 with catfish fry at ¡ extra source of food. In addition, the synergistic relation- 150,000 ha 1 in nursery ponds where there was also a between tilapia and prawns, through their effects resident crayfish population, both prawn production and ¡ on pond and the good growth rates obtained at survival were low (92–270 kg ha 1 and 15–22%). Miltner relatively high stocking densities of both organisms, indi- et al. (1983) stocked nursed 0.5–1.0 g prawns at a low ¡ cated that their polyculture was technically feasible and density (2500 ha 1) with channel catfish, either finger- ¡ economically viable. Uddin et al. (2009) found a favor- lings (11–12 g) at 3700 or 7400 ha 1, fry (0.05 g) at ¡ able 50–57% net profit margin in trials conducted to 100,000 or 200,000 ha 1. All ponds also contained 3–4g ¡ investigate the effects of substrate addition and supple- silver carp at 740 ha 1 and 250–300 g white amur (grass ¡ mental feeding on plankton composition and production carp) at 100 ha 1. Prawn yields were not significantly in tilapia and prawn polyculture. The net return was different between the various catfish treatments and ¡ higher for substrate-based ponds than for control ponds, ranged from 156 to 170 kg ha 1, compared to 200 kg ¡ indicating that it is profitable to use bamboo in this way. ha 1 in the control (prawns, no catfish). Differences in Asaduzzaman et al. (2009a) determined the optimum prawn survival among the various catfish treatments stocking rates for each species from the point of view of were also not significant (93.3–98.8%). Pavel et al. (1985) economic return. These stocking rates (5 g prawns confirmed the better performance of prawns stocked at ¡ ¡ ¡ stocked at 3 m 2 and 24 g tilapia stocked at 0.5 m 2) low density (4940 ha 1), reporting yields of 124–125 kg ¡ were used by Asaduzzaman et al. (2009b) in a further ha 1 and survival of 76–85% in grow-out ponds during trial. The addition of periphyton substrates (bamboo spring. D’Abramo et al. (1986) stocked juvenile prawns ¡ side shoots) in C/N controlled ponds (C/N D 20:1) sig- (0.1–2.6 g) at 4942 ha 1 in polyculture with fry, finger- nificantly benefited the survival and yield of prawns. lings and adult catfish and fed only the fish, achieving a ¡ In India, Reddy et al. (1988) found that the polycul- prawn yield of 172 kg ha 1 and a survival rate of 93%. ture of M. malcolmsonii with the Indian carps rohu, Heinen et al. (1987) found that a mean survival rate and

Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 ¡ catla, and a hybrid catla £ rohu gave a significantly yield of 75% and 152 kg ha 1, respectively, could be higher prawn survival rate (51.4–68.8%) than when com- attained at similarly low prawn stocking densities ¡ mon and grass carps were the fish species stocked (6.8% (0.5 m 2) in catfish fingerling ponds. Lilyestrom et al. prawn survival). John et al. (1995) found that both M. (1987) found that, in polyculture with catfish, M. rose- rosenbergii and M. malcolmsonii performed better in pol- nbergii fed mainly on insects, macrophytes and the cat- yculture with common and silver carps than in monocul- fish diet. The contribution of formulated feed to prawn ture or in bispecies culture. Productivity of both prawns growth increases as animals grow. Apparently, polycul- and fish shows great variability under polyculture, as ture has no adverse effect on the survival, growth, or pro- might be expected since the trials were conducted under duction of either species. Commercial polyculture of different conditions. Vasudevappa et al. (2002) found a freshwater prawns with fish is almost non-existent in the production of 2418 kg of catla plus rohu and 780 kg of United States, despite the fact that these promising M. rosenbergii per hectare, with survival rates of 98 and results were obtained. Tucker et al. (2004) stated that 80%, respectively. Singh (2003), polyculturing M. rose- commercial polyculture with adult catfish is impractica- nbergii with Indian major carps (catla, rohu, and mrigal) ble due to the difficulty in harvesting both species simul- in saline land holdings of the southwestern districts of taneously, but on the other hand proposed that ¡ Punjab in North India, obtained 2655 kg ha 1 of carps polyculture with fingerlings could be a good alternative, ¡ together with 150 kg ha 1 of prawns with a mean weight since harvesting could be carried out with a seine with a 282 H. L. A. MARQUES ET AL.

2.5 cm2 mesh, that selects the prawns and allows the cat- weight, production and FCR, with combined averages of ¡ fish fingerlings to escape. 38 g, 2465 kg ha 1, and 1.9, respectively. Tilapia in cocul- Studies on the coculture of Nile tilapia in cages sus- ture had a significantly higher survival rate (99.7%) and pended in ponds stocked with M. rosenbergii have been FCR (1.5) than in polyculture (90.3 and 0.8, respectively). carried out in the state of Kentucky. Tidwell et al. (2000) There were no consistent trends in treatment differences found that the use of distillers’ grains with solubles as a among water quality variables or phytoplankton popula- direct feed for the tilapia was economically more inter- tions. These authors stated that the lower prawn produc- esting than the use of commercial feed. Furthermore, the tion in the polyculture treatment is probably due to addition of tilapia in polyculture increased total pond competition for food with the large number of tilapia productivity by approximately 81%. Danaher et al. juveniles, since despite the use of monosex males tilapia, (2007) studied the effects of various densities of caged several cohorts of juvenile tilapia were produced in poly- ¡ Nile tilapia on water quality, phytoplankton populations, culture ponds, resulting in over 2500 kg ha 1 of juve- and prawn and total pond production in ponds stocked niles. These authors concluded that the confinement of ¡ with M. rosenbergii at 69,000 prawns ha 1. This experi- tilapia in cages (coculture) appears preferable to uncon- ment consisted of three treatments (prawn monoculture, fined culture of tilapia (polyculture) with freshwater low-density coculture with two cages of 1 m3 (100 fish prawns. per cage) and high-density coculture with four similar Studies on the rotational polyculture of M. rosenbergii tilapia cages. The total culture period was 106 days for and red swamp crawfish Procambarus clarkii were car- tilapia and 114 days for prawns. The overall mean after- ried out in the United States about 25 years ago. Grana- ¡ noon pH level and phytoplankton biovolume were sig- dos et al. (1991) obtained 157–248 kg ha 1 of 11–17 g ¡ nificantly lower in coculture ponds than in monoculture. prawns and 746–1266 kg ha 1 of crawfish when prawns ¡ Prawn weights were significantly higher in coculture were stocked at 17,500 ha 1. Brood crawfish were than in monoculture, but the survival of both prawns stocked in May when they borrowed into the pond bot- and tilapia did not differ between treatments. Prawn pro- tom. In July, prawn PL were stocked and draining of the duction was significantly greater in high-density pond and prawn harvesting occurred in October. The ¡ (2720 kg ha 1) than in low-density coculture (2368 kg pond was refilled and crawfish were harvested from Jan- ¡ ha 1), which in turn was greater than in monoculture uary to May by trapping. Prawns were of a good size for (2125 kg ha-1). The prawn feed conversion ratios (FCRs) soft shell production during the months when crawfish were significantly lower than in monoculture, while the were not available for soft shell production. Avault specific growth rate (g/d) were significantly higher in (1990) and Caffey et al. (1993) mentioned that the pro- coculture ponds. There were no significant differences in duction of soft-shell M. rosenbergii was viable in autumn the percentage of marketable prawns (>20 g) between and soft-shell crawfish in summer using the same facili- treatments, with an overall average of 93.3%; however, ties. D’Abramo and Daniels (1992) studied the same sys- both coculture treatments had a significantly higher per- tem and obtained a better production of 1444 kg of ¡ centage (83.0%) of premium prawns (>30 g) than mono- crawfish and 855 kg ha 1 of prawns, concluding that the culture ponds (70.4%). system was economically feasible. Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 The effects of confined (coculture) and unconfined Some studies on prawn polyculture were carried out (polyculture) tilapia with freshwater prawns on prawn in Brazil during the last 25 years. Mendes et al. (1998a) growth, tilapia growth, algal populations, and water qual- polycultured M. jelksii with two ornamental fish, Ptero- ity were studied by Tidwell et al. (2010). Juvenile prawns phyllum scalare and Poecilia reticulada over a period of ¡ were stocked at 62,000 ha 1 in nine ponds. Three control two months; the survival rates of the fish were 84 and ponds contained only prawns; monosex (male) Nile tila- 92.5%, respectively, while prawn survival was 49%. ¡ pia were stocked at 4400 ha 1 unconfined in three other Mendes et al. (1998b) reared Xiphophorus helleri (also an ponds; and the same size and number of tilapia were ornamental fish) in nursery tanks of M. rosenbergii for stocked but confined in two, 1 m3 cages at 100 fish two months; mean survival was 60.5 and 63.5%, respec- ¡ cage 1 in three additional ponds. Prawns and tilapia tively. Silva et al. (2008) reported that the polyculture of were fed with commercial pellets. In the polyculture ornamental goldfish ( auratus) and angelfish treatments, average prawn harvest weight (27 g) and (Pterophylum scalare) with M. rosenbergii in 50 L aquaria ¡ prawn production (1625 kg ha 1) were significantly during the nursery phase, using the densities of 20 M. lower and prawn FCR (3.0) was significantly higher than rosenbergii PL, 8 P. scalare, and 1 C. auratus per aquar- in the other two treatments. There were no significant ium was feasible. differences (P > 0.05) between the monocultured and Experiments on the polyculture of freshwater prawns the cocultured treatments in terms of prawn harvest with food fish have also been carried out in Brazil. REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 283

Carvalho et al. (1998) found that the polyculture of M. culture can be performed in fresh or low-salinity water rosenbergii with common carp (Cyprinus carpio)in (<2 salinity) and that the prawns do not affect tilapia Northeastern Brazil was more profitable than either development (Henry-Silva et al., 2015). Rodrigues (2013) prawn or carp monoculture. Production was 606 kg/ha/ evaluated the use of natural and artificial substrates in 4.5 months and 2050 kg/ha/4.5 months, respectively, but the polyculture of M. amazonicum with Nile tilapia. This prawns accounted for 62% of the total income. Araujo author found that the use of substrates significantly and Portz (1997) compared two systems of polyculture increased mean prawn biomass by 34% and also (tilapia-prawn and common carp-prawn) in three differ- increased the number of prawns with individual mass ent stocking densities (0.5–0.5, 0.75–0.75, and 1.5– and length greater than 3.1 g and 7 cm, respectively. ¡ 1.5 m 2) and found that the polyculture with tilapia at Trials on fish-prawn polyculture have also been con- ¡ 1.5–1.5 m 2 provided the best productivity (4240 and ducted in other countries. In an economic study per- ¡ 842 kg ha 1 of tilapia and prawn, respectively), probably formed in Panama, Engle (1987) reported higher due to the minor competition for feed with tilapia than internal rates of return for two polyculture systems— with carps. Prawn densities and the economic feasibility Nile tilapia, grass carp, and M. rosenbergii; and a species of tilapia and prawn polyculture was studied by Santos of pacu (Colossoma mitrei; currently named Piaractus (2001) and Santos and Valenti (2002), who tested three mesopotamicus), grass carp, and M. rosenbergii (17 and ¡ prawn densities (2, 4, and 6 PL m 2) with one fish den- 13%, respectively)—than in prawn monoculture (10%). ¡ ¡ sity (1 fish m 2). The density of 4 m 2 resulted in higher In Saudi Arabia, Siddique et al. (1996) found that total ¡ productivity (909 kg ha 1) and a mean weight of 23.0 g yield from the polyculture of Nile tilapia, common carp and survival of 92% in a cycle of 175 days. The IRR and M. rosenbergii was almost five times as great as that ranged from 15 to 45%, while the PP was of 2.5–6 years, of prawn monoculture. In a limited experiment (one depending on the selling price of tilapia. These authors pond; two cages) in Argentina, Wicki et al. (1998) also concluded that stocking densities of up to 6 prawns showed that the coculture of pacu (Piaractus mesopota- ¡ m 2 did not affect tilapia production and the rearing sys- micus) in cages in a pond stocked with M. rosenbergii tem required neither additional feeding nor significant and grass carp seemed viable, resulting in fish survival of ¡ changes in management. Tilapia monoculture showed 100%, fish production of 800 kg ha 1, and nearly ¡ no profitability, while the polyculture system allowed an »780 kg ha 1 of prawns per cycle (survival 89%). increase in total production with the same amount of In Puerto Rico, Garcıa-Perez et al. (2000) compared ¡ supplied feed. the monoculture of 1.3 g prawns stocked at 7 m 2 and ¡ The polyculture of tilapia fingerlings (33 m 2) during the monoculture of all-male 7.4 g Nile tilapia stocked at ¡ ¡ the nursery phase and Amazon river prawns (14 m 2) 1m 2 with a polyculture system where 1.1 g prawns and ¡ was studied in a commercial farm by Boock et al. (2008), 7.4 g tilapia were stocked at 7 and 1 m 2, respectively. In using a 1500 m2 pond. Every two months, juvenile tilapia an experiment lasting 145 days a commercial feed was (45 g) were harvested and the pond was stocked with applied at rates based on biomass (5% during days 1–90 new fingerlings (8 g). After six months, the total produc- and 3% for days 91–120); maximum daily feeding rates ¡ ¡ tion was 63,000 tilapia juveniles and 282 kg ha 1 of reached 50 kg ha 1 in monoculture (prawns or fish) and

Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 ¡ prawns with mean weight of 2.4 g and a survival of 67 kg ha 1 in polyculture. Total yields and mean weights 80.4%. of tilapia were not significantly different in polyculture The coculture of caged lambari (Astianax altipara- or monoculture, but the yields of prawns were signifi- nae), a small Characidae fish within a pond stocked with cantly different. Total prawn yield in monoculture was ¡ ¡ ¡ M. rosenbergii at 5 PL m 2 was also studied in Brazil by 1367 kg ha 1, but only 951 kg ha 1 in polyculture. Final Sussel et al. (2011). Lambari densities were 300, 450, and prawn mean weights were 55 g in monoculture and 31 g ¡ ¡ 600 m 3. After 60 days, the density of 300 fish m 3 in polyculture. The authors postulated that the fish may resulted in higher mean weight and length, but the best have efficiently consumed the major portion of the feed productivity was achieved at the highest density. As the provided and suggested that further studies should con- objective was the sale of lambari as live bait and the sur- sider increasing feeding rates and improving feed distri- ¡ vival did not differ significantly, the density of 600 m 3 bution. These results also suggest that the wastes showed more profitability. Prawns weighed 3.8 g with a provided by the tilapia were not sufficient to meet the ¡ survival of 91.4%, which would allow selling them as feed requirements of prawns stocked at 7 m 2. ¡ juvenile IIs, with a productivity of 45,700 ha 1. Recently, In Trinidad, Souza et al. (2005) obtained a maximum ¡ intensive research on the polyculture of M. amazonicum mean production of 12,622 kg ha 1 (prawns plus fish) in with Nile tilapia and native fish in a semi-intensive sys- the polyculture of M. rosenbergii with armored catfish ¡ tem has been developed in Brazil. Data suggest that the (Hoplosternum littorale) and 24,176 kg ha 1 in M. 284 H. L. A. MARQUES ET AL.

rosenbergii-tilapia polyculture, after 5.5 months of rear- however, the combination diet showed better net profit ing. In the Philippines, Rola (2007) analyzed three differ- and cost-benefit ratio. In another experiment, Lan et al. ent feeding systems (intensive, semi-intensive and (2006b) compared the two systems of culture (rotational traditional) on the commercial production of M. rose- and integrated) and concluded that the rotational system nbergii and milkfish (Chanos chanos) in polyculture, and gave significantly higher profits than the integrated, but found better economic indicators for the semi-intensive required a greater initial investment. Under both sys- ¡ and intensive systems. In a trial conducted in Egypt, tems, a stocking density of 2 PL m 2 resulted in a signifi- Sadek and Moreau (1996) studied the effect of stocking cantly higher profit and cost-benefit ratio than 4 or 6 PL ¡ ¡ 0.3 g PL or 2 g juvenile prawns at 2 and 5 m 2 in mono- m 2. In subsequent observations from farmer trials, Lan ¡ culture with the stocking of 0.3 g PL at 2 m 2 in polycul- et al. (2008) noted that net profit was significantly higher ture with two stocking densities of <1 g Nile tilapia (1 or for a feeding management using pellets, trash fish, and ¡ ¡ 2m 2) and 15 g common carp (0.25 or 0.5 m 2). The snail meat when compared to feeding with pellets only; highest annual rates of return were obtained from the in these trials the prawn stocking densities used were 4 ¡ ¡ monoculture of 2 g PL at 2 m 2 (57.5%) and the polycul- and 5 m 2. ¡ ture of 0.3 g PL at 2 m 2 with low-density tilapia and The polyculture of M. rosenbergii with fish in rice carp (30.9%). Also in Egypt the effect of monoculture fields has been studied in depth in Bangladesh. Wahab and polyculture of M. rosenbergii with Nile tilapia fry in et al. (2008) tested four densities of M. rosenbergii ¡ nursery tanks on the growth and survival of prawns was (10,000, 15,000, 20,000, and 25,000 ha 1) in polyculture ¡ examined by El-Sheriff and Ali Mervat (2009). These with mola at a stocking density of 2 m 2 in simultaneous authors concluded that the polyculture system was most rice-prawn-fish culture. Production ranged from 222– ¡ ¡ ¡ effective at a density of 100 prawns m 2. 388 kg ha 1 of prawns, 51–68 kg ha 1 of mola and ¡ 2880–3710 kg ha 1 of rice. The prawn density of ¡ 15,000 ha 1 resulted in significantly higher production Rice-prawn culture of both prawn and mola, with a net profit of US$ ¡ In an early study, Sadek and Moreau (1998) stocked M. 1100 ha 1. In a similar experimentally designed study, ¡ rosenbergii at either 10,000 or 20,000 ha 1 in monocul- Rohul Amin and Salauddin (2008) found that the inclu- ¡ ¡ ture and at 10,000 ha 1 with 5000 ha 1 of tilapia in poly- sion of M. rosenbergii and mola in rice fields had pro- culture in rice paddies. Average prawn size at harvest did found impacts on the availability of nutrients in the not differ significantly between the two monoculture water and soil, increasing the yield of rice. The best har- ¡ treatments but was significantly reduced in polyculture. vest of prawns (456 kg ha 1) was achieved at a stocking ¡ ¡ The maximum return (US$ 4507 ha 1) was obtained density of 15,000 ha 1 and the best production of rice ¡ from the high-density prawn monoculture integrated (3710 hg ha 1) was obtained at the prawn density of ¡ with rice culture; unsurprisingly, the lowest was obtained 10,000 ha 1. In another very similar study, Kunda et al. ¡ by the rice-only culture treatment (US$ 904 ha 1). This (2008) found that prawn production (mean survival 49– research has not been followed up and there is little or 57%), which ranged from 294–596 kg/ha, was signifi- ¡ no freshwater prawn culture of any sort in Egypt at pres- cantly higher in the treatment where 20,000 ha 1 of Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 ent (S. Sadek, personal communication, 2015). freshwater prawns were stocked, compared with 10,000, ¡ In Thailand, Giap et al. (2005) compared different fer- 15,000, or 25,000 ha 1. This treatment also resulted in tilization systems (basal and regular) and feeding regimes the highest net profit margin (74%) indicating that ¡ ¡ (with and without commercial feeding) in rice-prawn 20,000 ha 1 prawns and 20,000 ha 1 of mola is the best culture. The treatment with basal fertilization and com- combination for prawn-mola culture in -fed rice mercial feed was more profitable, with higher yields of fields after rice cultivation. Ali et al. (2009) did not find ¡ ¡ rice (0.42 kg m 1) and prawns (347 kg ha 1; 23.8 g in significant differences between the net profit from individual size) per crop. prawn-carp polyculture and polyculture integrated with Lan et al. (2006a) working in the Mekong Delta of rice and vegetables growing on the banks (US$ 835 and ¡ Vietnam, concluded that in the rotational rice-prawn 857 ha 1, respectively). ¡ system, stocking densities of 1, 2, or 3 PL m 2 produced In India, Mishra and Mohanty (2004) studied differ- greater prawn mean weights, but densities of 3 or 4 PL ent weir heights and densities of prawns and fish in rice- ¡ m 2 resulted in higher yields. The best economic viabil- fish-prawn polyculture, concluding that short-duration ¡ ity was obtained at a density of 3 PL m 2. There were no fish and prawn rearing (about 120 days) with a total significant differences between the two feed manage- stocking density (four species of fish with a 10% inclu- ¡ ments employed (commercial pellets and a combination sion of prawns) of 25,000 ha 1 and a weir height of of pellets and snail meat) on production parameters; 12.5 cm resulted in the best net profit. Mohanty et al. REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 285

(2004) evaluated the integration of prawns and fish in species (silver carp, grass carp, catla, rohu, mrigal, and rice fields and concluded that the percentage increase in Thai silver barb Puntius gonionotus) resulted in signifi- ¡ rice yield was 7.9–8.6% above rice monoculture, probably cantly higher fish productivity (5290 kg ha 1 in due to the better aeration of water and additional supply 10 months) than the use of treated manure brought from ¡ of in the form of leftover feed and prawn beyond the farm (3365 kg ha 1 in 10 months) or the ¡ excreta. Mohanty (2010) studied the impact of periodic control without fertilization (885 kg ha 1 10 months). cull harvesting in rice-fish-prawn culture on the popula- Prawn survival and production was significantly lower in tion structure, feed intake pattern and growth perfor- the ponds with fresh chicken manure droppings. Results mance of M. rosenbergii, concluding that it enhances the showed the potential to produce fish and prawns without net return by 28%. feed and to produce chicken above ponds, saving space. In Brazil, Marques et al. (2011), in a partial budget analysis, concluded that the introduction of M. rosenber- Future potential for integrated freshwater gii in rice-monoculture systems resulted in an increase of prawn farming in a sustainable world 10.5% in total crop value. Boock et al. (2013) pointed out that the native species M. amazonicum can be reared in Zimmermann et al. (2010) observed that the polyculture rice fields without being fed and sold as live bait in the of fish is common in tropical aquaculture, but freshwater sport fishing market. These authors observed that the prawn polyculture with fish is less common, despite the stocking of prawns in the rice fields did not degrade considerable amount of research on this subject. As one effluent quality and sometimes improved it, probably of the possible reasons for this situation, New (2002) because prawns consume organic matter, contributing to stated that the management of polyculture systems is the recycling of nutrients. Boock et al. (2016) concluded more complex than that of monoculture, especially that rice-prawn culture at a stocking density of 2 juve- regarding to the harvesting of prawns, since it is difficult ¡ niles m 2 of M. rosenbergii without commercial diets to synchronize both fish and prawn production in order was economically feasible and could compensate for low to achieve the maximum production of marketable ani- ¡ rice prices. Stocking at a higher rate (5 juveniles m 2) mals. On the other hand, some of the constraints that was not cost effective due to an increase in prawn mor- were pointed out by Zimmermann et al. (2010) as limit- tality and the higher cost of purchasing postlarvae. These ing the expansion of integrated prawn cultures in both authors observed that natural food is not a major limit- Asia and Latin America, are the same as those that con- ¡ ing factor for stocking densities of up to 5 prawns m 2; strain the increase of prawn monoculture in those prawns can attain commercial size in this system. In Bra- regions, i.e., lack of technology transfer, shortages of zil, the selling price of rice fluctuates and rice monocul- prawn PL and capital, and deficiencies in marketing. ture often becomes non-profitable. Thus, the integrated In a review of the polyculture and coculture of fresh- rice-prawn system may be an effective alternative for the water prawns with tilapia species, New and Valenti production of rice without the necessity for government (2016) stated that both systems are technically feasible subsidies. today and can improve the use of natural resources (such as space, water, and nutrients), reduce the use of Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 commercial diets, and increase profits. Nevertheless, a Aquaponics and other systems significant research effort is needed to provide science- There are only two reports of studies on integrated sys- based knowledge in order to improve the efficiency of tems other than fish-prawn polyculture or coculture and such aquaculture systems and to take full advantage of rice-prawn culture. In Brazil, the effect of the use of efflu- their potential. ents from a M. amazonicum nursery, operated at a den- Some of the difficulties experienced by producers and ¡ sity of 80 PL m 2, in the production of hydroponic workers in implementing fish-prawn polyculture could watercress and lettuce was evaluated by Castellani et al. be minimized by using newly available technologies. For (2009). The results showed that the effluent was suffi- example, the undesirable proliferation of tilapia in prawn cient to meet the demand for nutrients only in the case ponds could be avoided by using sex-reversed or caged of watercress, when supplemented with a nutritive solu- tilapia. Problems in harvesting prawns and fish or the tion. Further research is necessary to produce a more polyculture of species with different culture cycles could conclusive result. In Bangladesh, Hoq et al. (1999) also be solved by using caged fish, which can be har- obtained good results from integrating poultry, prawns vested independently from the harvest of prawns and fish. These authors reported that the use of fresh (Tidwell et al., 2000; Danaher et al., 2007). chicken manure from poultry sheds situated directly The benefits that result from the implementation of over ponds stocked with M. rosenbergii and several fish rice-prawn farming are already clear-cut. Ahmed and 286 H. L. A. MARQUES ET AL.

Garnett (2010) stated that the sustainability of rice- provide science-based knowledge in order to improve prawn farming in Bangladesh could be expressed in the efficiency of such aquaculture systems and to take terms of production technology (benefits of rice-prawn full advantage of their potential. integration that leads to an increase in rice production as There are good prospects for the expansion of inte- well as other diverse products such as prawns, fish, and grated freshwater prawn culture worldwide. Apart from vegetables), socioeconomic aspects (technology easily the high market value of freshwater prawns and the assimilated by small-scale producers, increasing their increasing interest in prawn production, especially in social status and food consumption—mainly proteina- Asia and South America, some other factors that may ceous food—and creating thousands of direct and indi- lead to this expansion are as follows: rect jobs) and environmental aspects (although it causes 1. There is a worldwide trend by consumers in select- an irredeemable loss of , rice-prawn farming ing products cultured in a sustainable way. Inte- reduces the use of pesticides and fertilizers, increases soil grated systems are recognized as being more fertility and promotes other important environmental efficient in using natural resources, especially benefits). These authors added that rice-prawn farming space, feed, and water, thus being more sustainable. plays an important role in the economy of Bangladesh The dissemination of these qualities may be a good and that, although not entirely sustainable, it can help marketing strategy that leads to obtaining a pre- the country keep pace with the current demand for food. mium price for products from integrated systems. In addition Kamal (2010) considered that gher farming 2. The semi-intensive monoculture of tropical fish in generates an average income that is four times higher ponds often shows minimal economic viability, than any other typical agriculture practice in Bangladesh especially in small-scale or family-run systems. On and increases the demand for labor, reduces food insecu- the other hand, many of these species can be inte- rity, provides education, protein, health care, and grated with prawns, resulting in profitable systems sanitation. when carried out efficiently, even on a small scale. 3. Caged tilapia culture in lakes and reservoirs is gradually replacing pond culture in some tropical Conclusions countries, such as Brazil. Due to this, there are The global landscape of integrated freshwater prawn cul- many abandoned or underutilized natural ponds, ture can be considered as falling into three categories: which could be turned into profitable fish-prawn 1. Having great social and economic importance, as is rearing units. the case of rice-prawn culture in some Asian 4. Integration of prawns into rice monoculture can countries. increase the profitability, mainly in small-scale sys- 2. Being well studied and having established a theo- tems. Furthermore, the production of organic or retical basis for implementation, but still needing free-chemical rice is generally a small-scale enter- to be commercially expanded, as is the case of prise compatible with prawn integration and pre- prawns and fish growing together in a pond mium prices are paid for rice produced in these (polyculture). systems. Downloaded by [Dr Wagner Valenti] at 11:00 21 April 2016 3. Having great promise but needing more studies to 5. The farming of fish confined in cages installed be effectively adopted by the production sector, within ponds stocked with free-swimming prawns which is the farming of caged fish in prawn ponds (coculture) is a promising system. This system (coculture). offers some advantages when compared with the Other integrated systems, such as prawn aquaponics, rearing of fish and prawns together (polyculture). still depend on the development of viable technologies. This includes the possibility of producing various The effective adoption of integrated prawn culture by species of fish at the same time in the same prawn producers will depend much more on strengthening and pond, which would allow production to be adapted organizing the freshwater prawn production chain than to address niche markets. Further research, includ- on technical solutions, in the same way as currently ing studies on the of the ponds, occurs in freshwater prawn monoculture. and economics is still essential. Tilapia and prawns are compatible species for farming through either polyculture or coculture. Both systems are technically feasible today and can improve the use of nat- ural resources (such as space, water, and nutrients), Acknowledgments reduce the use of commercial diets, and increase profits. The authors wish to express their sincere gratitude to Cynthia Nevertheless, a significant research effort is needed to Vilar Boock for providing artwork for our review. REVIEWS IN FISHERIES SCIENCE & AQUACULTURE 287

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