Improving production and diet assimilation in fish-prawn integrated aquaculture, using iliophagus species

Journal Pre-proof Improving production and diet assimilation in fish-prawn integrated aquaculture, using iliophagus species

Ariel C. Franchini, Gelcirene A. Costa, Stefany A. Pereira, Wagner C. Valenti, Patricia Moraes-Valenti PII:

S0044-8486(19)32680-8

DOI:

https://doi.org/10.1016/j.aquaculture.2020.735048

Reference:

AQUA 735048

To appear in:

aquaculture

Received date:

10 October 2019

Revised date:

29 January 2020

Accepted date:

30 January 2020

Please cite this article as: A.C. Franchini, G.A. Costa, S.A. Pereira, et al., Improving production and diet assimilation in fish-prawn integrated aquaculture, using iliophagus species, aquaculture (2020), https://doi.org/10.1016/j.aquaculture.2020.735048

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Improving Production and Diet Assimilation in Fish-prawn Integrated Aquaculture, Using Iliophagus Species Ariel C. Franchini1 , Gelcirene A. Costa1,2 , Stefany A. Pereira1 ; Wagner C. Valenti1 , Patricia Moraes-Valenti1 . 1

UNESP - São Paulo State University, Aquaculture Center; Via Paulo Donato Castelane s/n,

Jaboticabal, SP, Brazil. Zip code 14 884-900 and CNPq. UFRPE – Rural Federal University of Pernambuco, Department of Fisheries and

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Corresponding author: Patricia Moraes-Valenti

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Aquaculture; Rua Dom Manuel de Medeiros s/n, Dois Irmãos, Recife, PE 52171-900, Brazil.

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Abstract

In the integrated culture of pelagic fishes and benthic prawns, a large quantity of nutrients and energy remain in the pond bottom after harvest. This study assessed whether the inclusion of an iliophagus species, such as curimbata (Prochilodus lineatus), can take advantage of those

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resources and improves yield and diet use efficiency in tambaqui (Colossoma macropomum) and Amazon river prawn (Macrobrachium amazonicum) integrated aquaculture. A completely

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randomized experiment was designed with two treatments, and five replicates each of

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integrated systems: tambaqui and Amazon river prawn (TP) and tambaqui, Amazon river prawn, and curimbata (TPC). Ten 0.01-ha earthen ponds were used as experimental unities.

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Juveniles of tambaqui (3.93 ± 1.63 g) and Amazon river prawn (0.02 ± 0.02 g) were stocked

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in all ponds at a density of 3 and 11 individuals per m-2 , respectively. Five ponds, selected at random, were also stocked with curimbata (3.11 ± 2.61 g) at a density of 5 individuals per m. Tambaqui was fed twice a day with an extruded commercial diet (32 % crude protein) to

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apparent satiation. The prawn and curimbata were not fed.. The experiment lasted 53 days. The presence of curimbata did not affect tambaqui performance, whereas reduced the production of prawn in ~25%. The inclusion of curimbata increased total species yield by ~35% (from 734 to 991 kg.ha-1 ) and decreased FCR by ~31% (from 0.61 to 0.42). These results indicate that a mud-feeder like curimbata can take advantage of the large quantity of nutrients and energy deposited in the bottom of freshwater pond aquaculture.

Keywords: Integrated Aquaculture, IMTA, tambaqui, Amazon river prawn, curimbata.

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1. Introduction Aquaculture is the food production segment that most expand in the world. This growth increases the use of space, water, natural resources, and the release of pollutants in the environment (Valenti et al., 2018). Therefore, farm systems should evolve toward more sustainable systems that optimize the use of resources and reduce environmental impacts. Integrated multi-trophic aquaculture (IMTA) is a good example that combines the farming of

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species with complementary ecologic requirements, improving the assimilation of wastes in the biomass of the target species (Chopin et al., 2012; Marques et al., 2016). In freshwater,

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integrated aquaculture systems using pelagic fishes and benthic prawns have been performed

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with success globally (Marques et al., 2016; New and Valenti, 2017). Nevertheless, recently, David et al. (2017a; 2017b) and Flickinger et al. (2019a; 2019b) demonstrated that a large

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quantity of nutrients and energy remain in the pond bottom after harvest. These authors

efficiencies.

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suggested that a mud-feeder species should be introduced in the systems to improve their

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Recent studies showed the technical feasibility of farming tambaqui (Colossoma

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macropomum) integrated to Amazon river prawn (Macrobrachium amazonicum) (Dantas et al., 2020). Tambaqui is a native fish largely produced in South America (Valadão et al. 2016). This species is farmed in semi-intensive monoculture pond systems and has a vast market in many South American countries, such as Brazil, Colombia, Bolivia, Venezuela, and Peru. Global production attained about 140,000 t in 2017 (FAO, 2020). Amazon river prawn is produced by fisheries and traded as bait-fish and for human consumption in some countries, mainly in Brazil. Curimbata (Prochilodus spp) is a group of iliophagus South-American native species exploited by fisheries and aquaculture in different regions (Wright and Flecker, 2004; Taylor

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et al., 2006; Sampaio et al. 2011; Freire et al. 2012; Saint-Paul 2017). In the past decades, Prochilodus lineatus was introduced in the aquaculture of China and Vietnam and has been used in integrated culture (Kalous et al. 2012). This species has a large market in Brazil, which is supplied mainly by fisheries. Curimbata may be suitable to be combined with tambaqui and prawn to eat the excess of accumulated organic matter on the pond bottom. The three species have complementary

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feeding habits and occupy different spaces inside the ponds. The tambaqui is pelagic and eat zooplankton, some insects, fruits, seeds, and plant material originated from the banks of rivers

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(Oliveira et al., 2006). The Amazon river prawn is benthonic and feeds mainly on benthic

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fauna and detritus (Moraes‐ Valenti &Valenti, 2010). Curimbata swims close to the bottom and eats mostly detritus and periphyton (Kalous et al. 2012).

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This study tested the hypothesis that the inclusion of an iliophagus species can increase

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the total yield and improve the use of supplied diet in the integrated fish-prawn aquaculture. An experiment was conducted, including fingerlings of the curimbata, P. lineatus, in the

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integrated culture of tambaqui fingerlings, and Amazon river prawn post-larvae in earthen

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ponds. This arrangement was conceived as a model of study.

2. Material and Methods

The study was conducted in the Crustacean Sector of Aquaculture Center (CAUNESP) at Sao Paulo State University, Jaboticabal, Sao Paulo, Brazil (21°15’ 22’’ S, 48°18’ 48’’ W). A completely randomized experiment was designed with two treatments and five replicates of each: the integrated culture of tambaqui and prawn (TP), and the integrated culture of tambaqui, prawn, and curimbata (TPC). This experiment was not planned to obtain animals in commercial size but only as a model to test the proposed hypothesis. Nevertheless, the animal

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stocking size and the experiment duration correspond to the nursery phase of the three species used in the model. Ten 0.01-ha earthen ponds 1 m depth were filled with hypereutrophic water from two reservoirs that received effluents from other aquaculture systems. The pond water was continuously renewed. Ponds were stocked with 60-days juveniles of tambaqui (C. macropomum) and 15-days post-larvae of Amazon river prawn (M. amazonicum). Five ponds

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randomly sorted were also stocked with juveniles of curimbata (P. lineatus). All juveniles and post-larvae were acquired from CAUNESP. The initial mean mass of tambaqui, prawn, and

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curimbata were 3.93 ± 1.63 g, 0.02 ± 0.02 g, and 3.11 ± 2.61 g, respectively. The stocked

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densities were 3 tambaqui.m-2 , 11 prawns.m-2 and 5 curimbatas.m-2 . Inappropriate management of tambaqui during transportation produced mass mortality in the firsts days

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after stocking. Dead fish fluctuated, and they were picked up and counted to estimate the

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mortality. It was estimated that the density was reduced to ~1.4 tambaqui.m-2 after 3-4 days.

stocking.

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Then, the mortality was as usual. No mortality of prawn and curimbata was observed after

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The target species was tambaqui, which was fed twice a day until apparent satiety with an extruded commercial diet for onívorous fish (Fri-Aqua juvenile, Fribe-Ribe - 32% crude protein, pellets of 2-3mm,). Curimbata and Amazon river prawn fed only on uneaten diet and wastes of the diets provided to tambaqui. The water variables were monitored. Temperature, dissolved oxygen (DO), conductivity, and pH were measured daily; total ammonia-nitrogen (TAN), N-nitrate, N-nitrite, total phosphorus, and chlorophyll-a were monitored biweekly. Temperature, dissolved oxygen (DO), and conductivity were monitored using a probe YSI Model 2030 (YSI Pro 2030), and pH with a pH meter (EcoSense pH 100 A). Nitrogen

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compounds, total phosphorus, and chlorophyll-a were determined according to the methodology of APHA (2005) (Table 1). The experiment lasted 53 days. After that, ponds were drained, and all animals were harvested. Then, they were counted, weighed, and measured, using a precision scale (Gehaka BK 2000 – precision: 0.01g) and a measuring board (1 mm precision). The mean survival, gain in body mass, and length were obtained for each species. Survival of tambaqui was

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computed considering the total number of fish stocked, i.e., no correction was made to compensate for the initial mass mortality. Yield by species and total yield by the pooled

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species were calculated for each pond and converted in kg.ha-1 by dividing the pond yield by

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the pond area and multiplying by 10,000. The feed conversion rate (FCR) was computed to the tambaqui and to the pooled species by dividing the total diet supplied during the

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experiment by the final biomass gain during the experiment, i.e., harvested biomass minus

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stocked biomass.

Data were subjected to tests of normality (Shapiro-Wilk) and homoscedastic

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(Barlett) follow by the Student´s t-test. Data on survival were subjected to arcsine square-root

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transformation before analyses. Water quality data were subjected to a principal component analysis (PCA) to verify the differences between treatments and variation during the culture. The significance level was set at P ≤ 0.05. Statistical analyses were performed using the software R-Statistic (version 3.4.3) and Microsoft Excel 2010.

3. Results and Discussion The inclusion of curimbata in the integrated culture showed a low effect on the tambaqui and prawn development as well as in water quality (Tables 2 and 3). The presence of this species increased total species yield by ~35% and decreased FCR by ~31%. These

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results indicate that the curimbata can use the large quantity of nutrients and energy deposited on the bottom of freshwater ponds (David et al., 2017a, Flickinger et al., 2019a). The low tambaqui survival was due to the inappropriate transportation and stocking. Thus, mass mortality occurred in the firsts days after stocking when density was reduced to ~ 1.4 tambaqui.m-2 in all ponds. However, the mortality was similar in the experimental unities and stopped in a few days. Thus, the tambaqui initial mortality did not prejudice the aim of

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the study since it has demonstrated the effect of the addition of the iliophagus fish in total yield and the FCR. The results showed that curimbata did not affect the tambaqui

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development, increased total biomass production, and the efficiency of commercial feed use.

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Tambaqui growth and yield were comparable with those that were obtained in previous studies on monoculture and polyculture. Merola and Pagá-Font (1988) stocked

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∼11.7 g tambaqui fingerlings in earthen ponds at 1.7 fish. m−2 ; after 45 days, fish weight was ∼41 g and yield 680 kg/ha. Ferrari et al. (1991) stocked ~5 g fingerlings at a density of 5 fish.

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m−2 , which reached ∼106 g after 127 days. Teichert-Coddington (1996) stoked 0.8 g

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tambaqui at a density of 3 fish.m-2 and obtained ~50 g fish after 85 days. Tortolero et al.

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(2015) performed an experiment, in which ~5 g tambaqui were stoked at 0.3 fish.m-2 together 0.7 jaraqui. m-2 (Semaprochilodus insignis) in 46 m2 masonry tanks. Tambaqui grew to 43-50 g in 60 days, and yielded ~326 kg.ha-1 after 90 days. In the present study, tambaqui fingerlings, stocked with ~4 g, attained 40-50 g and yielded ~500 kg.ha-1 in 53-days. The Amazon river prawn showed high survival, which was, on average, 82.4 to 92.9% in treatments TPC and TP, respectively. Moraes-Valenti and Valenti (2007) obtained a mean survival of 72.2% in 5-month monoculture of the Amazon river prawn stocked at 10.m-2 , which is similar to the density of the present study. Rodrigues et al. (2019) stocked 22 postlarvae of the Amazon river prawn together tilapia and obtained survival of ~80% in 4

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months. Dantas et al. (2020) reported prawn survival of 75.1% with a final mass of ~3 g in a tambaqui and Amazon river prawn 6-month integrated system. The present study obtained a final mass of 2.14 g to the treatment TP and 1.74 to TPC during ~2-month integrated culture. Although the prawn survival and body weight gain did not show significant differences between treatments, prawn yield decreased by 25% when curimbata was included. This result suggests that curimbata affects prawn performance. However, the curimbata biomass

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produced compensates prawn productivity reduction. Juveniles of curimbata sized 5-10 g may be sold for grow-out farms or to hydropower companies to be released in natural rivers to

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mitigate the impact caused by the dams. The price of these juveniles (~US$ 200 per thousand)

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surpasses the amount of 1.5-2.0 g prawns in Brazil (~US$ 40 per thousand). Farming curimbata in integrated systems without feed reduces the costs, increasing the profit of

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farmers.

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The low feed conversion ratio (FCR) of tambaqui is due to the natural biota exploitation. This species filter zooplankton during all life stages (Araújo-Lima and Goulding

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1998). The aquatic biota is very important to the tambaqui gain of mass, even with the supply

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of a balanced diet (Gomes and Silva, 2009). Dantas et al. (2020) observed FCR of 1.09 ± 0.05 for tambaqui monoculture and 1.02 ± 0.04 for the tambaqui farmed with Amazon river prawn. Other authors reported FCR varying from 0.92 to 1.27 to tambaqui juveniles farmed in cages systems, 1.35 in natural ponds, and 1.80 in channels built inside small rivers in Amazonia (Arbeláez-Rojas et al. 2002; Chagas and Val 2003; Brandão et al. 2004). The present study shows low FCR for the pooled species, which was expected once the farming utilized species with complimentary food niches in both treatments. The bioturbation of the prawn and curimbata suspend the nutrients accumulated in the pond bottom, increasing phytoplankton

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development and, consequently, the zooplankton communities. Thus, this process enhances natural food available by the tambaqui. The addition of a third species in the system did not affect water-quality parameters. Despite the increase of biomass in the ponds with curimbata, the water remains adequate to farming, during the entire experiment (Table 3), according to the general recommendation of Boyd (2015) to freshwater pond aquaculture systems. The PCA analysis showed a random

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distribution of the parameters to both treatments (Figure 1), indicating that treatments did not affect water quality. However, the data collected on days 1, 15, and 30 of culture were

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prevalent in quadrants II and III, and data obtained in day 45 in the quadrant I. This pattern

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indicates that water parameters varied in time during the culture. A higher concentration of total nitrogen and phosphorus occurs at the final farming samples. The PCA component I

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showed a positive correlation with dissolved oxygen and total nitrogen and phosphorus and a

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negative correlation with temperature, conductivity, and inorganic nitrogen. These correlations suggest that the component I represents the photosynthesis process. The PCA

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component II showed a positive correlation with inorganic nitrogen and negative correlation

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with temperature, dissolved oxygen, pH, and chlorophyll-a. These correlations suggest a relation between the component II and the decomposition process. In this manner, the PCA analysis indicates the predominance of decomposition at the beginning of culture and of primary productivity after 45 days. The increase in primary production may be due to the rise in the upwelling of nutrients to the water column caused by the bioturbation of the benthonic species that grow during the culture.

4. Conclusion and recommendation

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The present study corroborates the hypothesis that an iliophagus species can improve the production of biomass and efficiency in using the supplied diet. The curimbata associated with the Amazon river prawn was able to assimilate a large quantity of nutrients deposited in the pond bottom without any negative impact on tambaqui, the pelagic species. Therefore, farm efficiency increased. Besides, this study shows the feasibility of culture tambaqui, Amazon river prawn, and curimbata in integrated farming, at least in the nursery phase.

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Future studies should focus on the stocking densities and the proportion of each species in the

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culture in the different grow-out phases.

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Acknowledgments

The authors thank the colleagues and the technicians from the Aquaculture Center of UNESP

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- CAUNESP, Prawn Culture Sector. The authors also thank the São Paulo Research

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Foundation – FAPESP (Grant No. 10/51271-6), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) (Finance Code 001), and the National Council for

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Scientific and Technological Development – CNPq (Grant No. 306361/2014-0 and

References

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428628/2018-4) for the financial support.

APHA 2005. Standard Methods for the Examination of Water and Wastewater, 1st ed. American Public Health Association/American Water Works Association/Water Environment Federation, Washington Araújo-Lima, C.A.R.., Goulding, M., 1998. Os frutos do tambaqui: ecologia, conservação e cultivo na Amazônia. Sociedade Civil Mamirauá/Cnpq, Tefé/Brasília. Arbeláez-Rojas, G.A., Fracalossi, D.M. and Fim, J.D.I. 2002. Composição Corporal de Tambaqui, Colossoma macropomum, e Matrinxã, Brycon cephalus, em Sistemas de Cultivo Intensivo, em Igarapé, e Semi-Intensivo, em Viveiros. Rev Bras Zootec 31:1059–1069. doi: 10.1590/S1516-35982002000500001 Boyd C.E. (2015) Water quality: an introduction. Springer.

Journal Pre-proof

12

Brandão, F.R., Gomes, L.D.C., Chagas, E.C. and Araújo, L.D. 2004. Densidade de estocagem de juvenis de tambaqui durante a recria em tanques-rede. Pesqui Agropecuária Bras 39:357–362. doi: 10.1590/S0100-204X2004000400009 Chagas, E.C. and Val, A.L., 2003. Effect of vitamin C on weight and hematology of tambaqui. Pesqui. Agropecu. Bras. 38, 397–402. https://doi.org/10.1590/S0100204X2003000300009 Chopin, T., Cooper, J.A., Reid, G., Cross, S., Moore, C., 2012. Open-water integrated multitrophic aquaculture: environmental biomitigation and economic diversification of fed aquaculture by extractive aquaculture. Rev. Aquac. 4, 209–220. https://doi.org/10.1111/j.1753-5131.2012.01074.x

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Dantas, D.P., Flickinger, D.L., Costa, G.A., Batlouni, S. R., Moraes-Valenti, P., Valenti, W. 2020. Technical feasibility of integrating Amazon river prawn culture during the first phase of tambaqui grow-out in stagnant ponds, using nutrient-rich water. Aquaculture, 516, 1 February, 734611.

e-

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David, F.S.; Proença, D.C. and Valenti, W.C. 2017a. Nitrogen budget in integrated aquaculture systems with Nile tilapia and Amazon River prawn. Aquaculture international, 25:1733-1746. DOI 10.1007/s10499-017-0145-y.

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David, F.S.; Proença, D.C. and Valenti, W.C. 2017b. Phosphorus Budget in Integrated MultiTrophic Aquaculture Systems with Nile Tilapia (Oreochromis niloticus) and Amazon River Prawn (Macrobrachium amazonicum). Journal of the World Aquaculture Society, 48(3):402-414.

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FAO (2020). FishStatJ. FAO Global Fishery and Aquaculture Production Statistics. http://www.fao.org/fishery/statistics/software/fishstatj/en

Jo u

rn

Ferrari, V. A., Lucas, A. F. and Gaspar, L. A. 1991. Desenpenho do tambaqui. Colossoma macropomum, Cuvier, 1818, em monocultura experimental sob condições de viveiroestufa (1ª. fase) e viveiro convencional (2ª. fase) no sudeste do Brasil. Boletim Tecnico do CEPTA, 4(2):23-37. Flickinger, D.L., Costa, G.A., Dantas, D.P., Moraes-Valenti, P., Valenti, W., 2019a. The budget nitrogen in the grow-out of the Amazon river prawn (Macrobrachium amazonicum Heller) and tambaqui (Colossoma macropomum Cuvier) farmed in monoculture and integrated multitrophic aquaculture systems. Aquaculture Research, 00:1-18. https://doi.org/10.1111/are.14304. Flickinger, D.L., Dantas, D.P., Proença, D.C., David, F.S., Valenti, W.C., 2019b. Phosphorus in the culture of the Amazon river prawn (Macrobrachium amazonicum) and tambaqui (Colossoma macropomum) farmed in monoculture and in integrated multitrophic systems. Journal of the World Aquaculture Society, In Press. Freire, K. M. F., Machado, M. L. and Crepaldi, D. 2012: Overview of Inland Recreational Fisheries in Brazil. Fisheries, 37:11, 484-494. Gomes, L.C. and Silva, C.R. (2009). Impact of pond management on tambaqui, Colossoma macropomum (Cuvier), production during growth-out phase. Aquac Res 40:825–832. doi: 10.1111/j.1365-2109.2009.02170.x

Journal Pre-proof

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Kalous, L., Bui, A.T., Petrtýl, M., Bohlen, J., Chaloupková, P., 2012. The South American freshwater fish Prochilodus lineatus (Actinopterygii: Characiformes: Prochilodontidae): New species in Vietnamese aquaculture. Aquac. Res. 43, 955–958. https://doi.org/10.1111/j.1365-2109.2011.02895.x Marques, H.L.A., New, M.B., Boock, M.V., Barros, H.P., Mallasen, M., Valenti, W.C., 2016. Integrated freshwater prawn farming: State-of-the-art and future potential. Rev. Fish. Sci. Aquac. 24, 264–293. https://doi.org/10.1080/23308249.2016.1169245 Moraes-Valenti, P. M. C. and Valenti, W. C. 2007. Effect of Intensification on Grow Out of the Amazon River Prawn, Macrobrachium amazonicum. Journal of the World Aquaculture Society, v. 38, p. 516-526.

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Moraes-Valenti, P., Valenti, W.C., 2010. Culture of the Amazon river prawn Macrobrachium amazonicum. In: New, M.B., Valenti, W.C., Tidwell, J.H., D’abramo, L.R., Kutty, M.N. (Eds.), Freshwater Prawns: Biology and Farming. Oxford, Wiley-Blackwell, pp. 485– 501. Merola, N. and Pagán-Font, F. A. 1988. Pond culture of the Amazon fish tambaqui, Colossoma macropomum: A pilot study. Aquacultural engineering, 7(2), 113-125.

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New, M.B. and Valenti, W.C. 2017. Tilapia-Macrobrachium Polyculture. In: Perschbacher, P.W. and Stickney, R.R. Tilapia in intensive co-culture. Oxford, Wiley-Blackwell. p. 165-184.

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Oliveira, A.C.B., Soares, M.G.M., Martinelli, A., Moreira, M.Z., 2006. Carbon sources of fish in an Amazonian floodplain lake. Aquat. Sci. 68 (2), 229–238.

rn

al

Rodrigues, C. G.; Garcia, B. F.; Verdegem, M.; Santos, M, R.; Amorim, R. V.; Valenti, W. C. 2019. Integrated culture of Nile tilapia and Amazon river prawn in stagnant ponds, using nutrient-rich water and substrates. Aquaculture, 503:111-117.

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Saint-Paul, U. 2017. Native fish species boosting Brazilian’s aquaculture development. Acta of Fisheries and Aquatic Resources, 5(1), 1-9. Sampaio, L. A., Ono, E., Routledge, E.A.B., Correia, E.S., Moraes-Valenti, P. and Martino, R.C. 2010. Brazilian Aquaculture Update. Journal of the world Aquaculture Society, p. 32 – 42. Taylor, B. W. Taylor, Flecker, A. S. , Hal Jr. R. O. 2006. Loss of a Harvested Fish Species, Disrupts Carbon Flow in a Diverse Tropical River. Science 313, 833. Teichert-Coddington, D.R. 1996. Effect of stocking ratio on semi-intensive polyculture of Colossoma macropomum and Orechromis niloticus in Honduras, Central America. Aquaculture 143:291-302. Tortolero, S.A.R., Cavero, B.A.S., Brito, J.G., Soares, C.C., Silva Junior, J.L., Barbosa, H.T.B., Gangadhar, B., Keshavanath, P., 2015. Periphyton-based polyculture of Jaraqui, Semaprochilodus insignis (Schomburhk, 1841) and Tambaqui, Colossoma macropomum (Cuvier 1816) with feed supplementation. J. Aquac. Trop. 30, 111–132. Valenti, W.C., Kimpara, J.M., Preto, B. de L., Moraes-Valenti, P., 2018. Indicators of sustainability to assess aquaculture systems. Ecol. Indic. 88, 402–413. https://doi.org/10.1016/j.ecolind.2017.12.068

Journal Pre-proof

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Valladão, G. M. R., Gallani, S. U., and Pilarski, F. 2018. South American fish for continental aquaculture. Reviews in Aquaculture, 10(2), 351-369. Wright, J.P. and Flecker, A.S. 2004. Deforesting the riverscape: the effects of wood on fish diversity in a Venezuelan piedmont stream. Biological Conservation 120 (2004) 439– 447.

Tables and Figure Captions Table 1: Methods used for water quality variables analyses.

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Table 2: The mean ± standard deviation of the productive performance in different treatments. TP: tambaqui and prawn; TPC: tambaqui, prawn, and curimbata. Different letters on the same row represent significant difference at 5% level by Student´s t-test. NA: not applicable.

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Table 3: The mean ± standard deviation of the water quality parameters, measured in the integrated culture of tambaqui and prawn (TP), and tambaqui, prawn, and curimbata (TPC).

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Figure 1: The principal component analysis (PCA) of water quality between treatments and the collection period. The variation of data captured 56% by PC1 and PC2. Red dots represent TP, and blue dots represent TPC. The numbers 1, 2, 3, and 4 represent 1, 15, 30, and 45 farming days samples, respectively.

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Figure 1: The principal component analysis (PCA) of water quality between treatments and the collection period. The variation of data captured 56% by PC1 and PC2. Red dots represent TP and blue dots represent TPC. The numbers 1, 2, 3 and 4 represent 1, 15, 30 and 45 farming days samples, respectively.

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Table 2: Methods used for water quality variables analyses. TAN = total ammonia nitrogen Methodology (APHA 2005)

TAN

4500-NH3 F. Phenate Method

N-nitrate

4500-NO3 – E. Cadmium Reduction Method

N-nitrite

4500-NO2 – B. Colorimetric Method

Total nitrogen Total phosphorus Chlorophyll-a

4500-Norg -B. Macro-Kjeldahl Method 4500-P D. Stannous Chloride Method 10200-H. Spectrophotometric determination

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Water variables

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Table 3: The mean ± standard deviation of the water quality parameters measured in the integrated farming tambaqui and prawn (TP), and tambaqui, prawn, and curimbata (TPC). TP

TPC

28.0 ± 0.1

27.9 ± 0.2

7.70 ± 0.34

7.30 ± 0.33

99.2 ± 4.3

93.4 ± 5.6

Conductivity (µS cm )

99.2 ± 4.3

93.7 ± 11.5

pH

8.27 ± 0.20

8.13 ± 0.12

18 ± 10.0

17 ± 10

7±5

6±5

Temperature (ºC) -1

DO (mg L ) Saturation (%) -1

-1

N-Ammonia (µg L ) -1

N-Nitrite (µg L ) -1

64 ± 22

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N-Nitrate (µg L )

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Variables

-1

Total Nitrogen (µg L ) -1

Total Phosphorus(µg L )

249 ± 137

305 ± 152

44 ± 9

45 ± 19

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-1

8±4

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Chlorophyll-a (µg L )

82 ± 54

9±6

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Table 2: The mean ± standard deviation of the organism productive performance to different treatments. TP: tambaqui and prawn ; TPC: tambaqui, prawn and curimbata. Different letters on the same row represent significant difference at 5% level by Student's t-test,

TP

TPC Stocking Amazon river prawn

Tambaqui

5.99 ± 0.83

1.47 ±0.25

5.99 ± 0.83

Total mass (g)

3.93 ± 1.63

0.02 ± 0.02

3.93 ± 1.63

3.11 ± 2.61

82.4 ± 10.1

81.6 ± 7.4

Total length (cm)

13.1 ± 2.1

6.7 ± 0.3

12.4 ± 2.5

6.3 ± 0.3

7.5 ± 1.5

Body mass(g)

50.0 ± 19.9

2.1 ± 0.3

39.0 ± 23.0

1.74± 0.2

8.1 ± 5.5

Body mass gain (g)

46.1 ± 20.0

2.1 ± 0.3

35.1 ± 23.0

1.7 ± 0.2

5.0 ± 1.4

Yield (kg.ha-1 )

516 ± 297

218 ± 27

499 ± 81

158 ± 32

333 ± 72

FCR tambaqui

1.27 ± 0.59

0.80 ± 0.20

NA

NA

NA: not applicable

45.5 ± 27.7

Pr

al NA

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Total yield (kg.ha -1 )

a

0.61 ± 0.16

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FCR total species

pr

92.9 ± 3.7

e-

39.2 ± 37.7

734 ± 252

a

b

5.95 ± 1.27

0.02 ± 0.02

Harvesting

Survival (%)

1.47 ± 0.25

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Total length (cm)

Amazon Curimbatá river prawn

f

Tambaqui

b

b

0.42 ± 0.07

991 ± 126a

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Declaration of interests

☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

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Highlights



A large quantity of nutrients and energy accumulates in the pond bottom of integrated fish-prawn aquaculture.



The addition of an iliophagus species may transform these wastes into valuable biomass.

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When Curimbatá (Prochilodus lineatus) were integrated into tambaqui (Colossoma

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macropomum) and Amazon river prawn (Macrobrachium amazonicum) culture, yield

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increased ~35%, and FCR decreased by ~31%.

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