Aquaponic production of Sarcocornia ambigua and Pacific white shrimp in biofloc system at different salinities

Journal Pre-proof Aquaponic production of Sarcocornia ambigua and Pacific white shrimp in biofloc system at different salinities

Isabela Pinheiro, Ramon Felipe Siqueira Carneiro, Felipe do Nascimento Vieira, Luciano Valdemiro Gonzaga, Roseane Fett, Ana Carolina de Oliveira Costa, Francisco Javier MagallónBarajas, Walter Quadros Seiffert PII:

S0044-8486(19)31611-4

DOI:

https://doi.org/10.1016/j.aquaculture.2019.734918

Reference:

AQUA 734918

To appear in:

aquaculture

Received date:

28 June 2019

Revised date:

5 December 2019

Accepted date:

30 December 2019

Please cite this article as: I. Pinheiro, R.F.S. Carneiro, F. do Nascimento Vieira, et al., Aquaponic production of Sarcocornia ambigua and Pacific white shrimp in biofloc system at different salinities, aquaculture (2019), https://doi.org/10.1016/ j.aquaculture.2019.734918

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© 2019 Published by Elsevier.

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Aquaponic production of Sarcocornia ambigua and Pacific white shrimp in biofloc system at different salinities

Isabela Pinheiroa, Ramon Felipe Siqueira Carneiro a, Felipe do Nascimento Vieiraa, Luciano Valdemiro Gonzaga b, Roseane Fettb, Ana Carolina de Oliveira

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Costab, Francisco Javier Magallón-Barajasc , Walter Quadros Seifferta

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a

Universidade Federal de Santa Catarina, Centro de Ciências Agrárias,

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Departamento de Aquicultura, Laboratório de Camarões Marinhos. Serv. dos

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Coroas, 503, Barra da Lagoa, Florianópolis, SC, Brazil. CEP. 88061-600

b

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Universidade Federal de Santa Catarina, Centro de Ciências Agrárias,

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Departamento de Ciência e Tecnologia de Alimentos, Laboratório de Química

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CEP. 88034-000

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de Alimentos. Rod. Admar Gonzaga, 1346, Itacorubi, Florianópolis, SC, Brazil.

Centro de Investigaciones Biologicas del Noroeste (CIBNOR). Av. Instituto

Politécnico Nacional 195, Playa Palo Santa Rita Sur, La Paz, Baja California Sur, CP. 23096, Mexico.

Correspondent author: Isabela Pinheiro. Servidão dos Coroas, 503, Barra da Lagoa, Florianópolis, SC, Brazil. CEP: 88061-600. E-mail: [email protected]. Phone: +55 48 37214118.

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Abstract This study aimed to evaluate the relationship between salinity in the performance of marine shrimp Litopenaeus vannamei and halophyte plant Sarcocornia ambigua in an aquaponic system with biofloc. The experiment was conducted for 57 days, and four treatments were evaluated: 8 psu (practical salinity unity), 16 psu, 24 psu, and 32 psu, with three replicates. Each

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experimental unit consisted of an 800 L tank for shrimp rearing, a 40 L settling

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chamber and a hydroponic bench of 0.3 m2 of planting area and density of 40

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plants m-2. The tank water was continuously pumped to the settling chamber,

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and the supernatant was distributed on the hydroponic bench to irrigate the plants, returning to the tank by gravity. The tanks were stocked with 300 shrimp

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m-3 (1.6±0.1 g). The shrimp were fed four times daily with a commercial diet

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containing 38% crude protein. Salinity affected shrimp survival, which was lower

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in 8 psu treatment (56.3±4.7%). No salinity relationships were detected with any of the plant performance parameters; however, the highest biomass was

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produced at 16 psu, which is close to the isosmotic point of S. ambigua. The lowest concentrations of ammonia and nitrite and the highest concentrations of nitrate were found, through the interpolation of the data, near the 18 psu salinity. So, it is suggested that in this salinity, the absorption of ammonia by the plants is favored. The salinity also affected the concentration of dissolved orthophosphate. There was no relationship between salinity and the production of phenolic compounds and antioxidant activity in plants. The integrated cultivation of L. vannamei with S. ambigua can be carried out between salinities of 16 and 24 psu since the performance of the shrimp is not impaired, and the

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growth of the plants and the removal of nitrogen and phosphate compounds are favored in this range of salinity. Keywords: integrated culture; Litopenaeus vannamei; marine aquaponic; water quality; IMTA. 1. Introduction

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Aquaculture has great importance in eliminating hunger, improving

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health, and providing employment. However, to use the resources more

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efficiently, integrating food production systems can reduce inputs and waste,

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and increase earnings and sustainability (FAO, 2016). This integration can be made through aquaponics, which is the simultaneous production of aquatic

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animals (aquaculture) and cultivation of plants without soil (hydroponics) in a recirculating system (Love et al., 2015; Rakocy, 2012).

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In an aquaponic system, there is a symbiotic relationship between the

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fish or shrimp cultivated, bacteria, and plants (Wongkiew et al., 2017). Bacteria

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transform the nitrogen and phosphate compounds excreted by the animals into forms that can be absorbed by plants (Cerozi and Fitzsimmons, 2017; Hu et al., 2015). Besides improving nutrient removal efficiency, this system can also reduce the use of water and the effluent disposal to the environment, and increase profitability through the joint production of two crops (Endut et al., 2013; FAO, 2019). Additionally, in the presence of a diverse microbial community, the aquaponics can be more efficient (Emerenciano et al., 2013; Kotzen et al., 2019). The biofloc technology system (BFT) was created to maximize the

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aquaculture production with less environmental impact (Crab et al., 2012), and has as characteristics high stocking densities, limited water exchange and the accumulation of microbial flakes (Avnimelech, 2015; Ebeling et al., 2006). In this system, one of the pathways to ammonia removal is through autotrophic conversion to nitrate (Martínez-Córdova et al., 2015). So, at the end of the culture, less effluent is formed, but with higher concentrations of nitrogen

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compounds (Quintã et al., 2015). Thus, an alternative is to recycle the nutrients in aquaponics to produce vegetables (Pinheiro et al., 2017; Pinho et al., 2017;

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Rocha et al., 2017).

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For the integration of hydroponics with marine aquaculture, salt-tolerant plants, or halophytes, must be used (Buhmann and Papenbrock, 2013).

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Halophytes such as Sarcocornia ambigua, also known as salicornia or

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samphire, occurring in Santa Catarina, Brazil, (Bertin et al., 2014; Piirainen et

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al., 2017) are recognized for being cultivated in areas where salt concentration would be lethal to most of the other species (Flowers and Colmer, 2008). The

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successful development of halophyte plants in aquaponics with marine shrimp Litopenaeus vannamei in bioflocs has already been demonstrated. Pinheiro et al. (2017) reported productivity of 8 kg m-2 of S. ambigua, equivalent to 2 kg of plant for each kilo of shrimp produced. Many species of halophytes are not only able to tolerate salinity, but their growth is stimulated by the presence of salt and can retain high amounts of Na + and Cl-, especially in shoots (Flowers and Colmer, 2008; Kudo and Fujiyama, 2010). However, some species differ in their degree of tolerance to salinity and the ideal saline concentration for the development of these plants is that equal

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to or less than that of seawater (Redondo-Gómez et al., 2006; Ventura et al., 2014). Furthermore, in a marine aquaponic system, both plant and shrimp development can be affected. The salinity of the solution may interfere with the preference of S. ambigua in the absorption of different forms of nitrogen because this genus can use both nitrate and ammonium (Quintã et al., 2015). In

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conditions of moderate salinity, NO3 uptake can be decreased, and NH4 use becomes more favorable for halophyte growth (Kudo and Fujiyama, 2010).

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Also, shrimp require minerals to maintain basal metabolism and growth

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(Valenzuela-Madrigal et al., 2017). L. vannamei can survive and grow well in low-salinity water when the ionic proportion is close to seawater (Davis et al.,

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2005). Nevertheless, the growth of white shrimp is improved in salinities

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between 15 and 25 psu (practical salinity unit) (Boyd, 1989). Thus, this work

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aimed to evaluate the relation of salinity in the performance of Pacific white

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shrimp and Sarcocornia ambigua cultured in an aquaponic system with bioflocs. 2. Material and methods 2.1. Biological material 2.1.1. Shrimp The experiment was conducted at the Marine Shrimp Laboratory (LCM) of the Federal University of Santa Catarina, southern Brazil. Post-larvae of Litopenaeus vannamei were purchased from a commercial hatchery (Aquatec Ltda., RN, Brazil) and the nursery phase was under an intensive biofloc system (stocking density of 1000 shrimp m-3) in a circular fiberglass tank with useful volume of 40 m³ with an average salinity of 33 psu until they reached about 1 g.

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Shrimp were fed six times daily with a commercial diet containing 40% crude protein (Poti Mirim PL40, Guabi, Brazil). An organic carbon source (sugarcane molasses) was added when total ammonia nitrogen was above 1 mg L -1, in a proportion of 6 grams of carbon to neutralize each gram of ammonia. The temperature was maintained at 28±1°C and dissolved oxygen above 5 mg L -1. One week before the start of the experiment, the shrimp were acclimated to 20

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psu. 2.1.2. Plants

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Seedlings were grown through vegetative propagation by cuttings. Plants

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of Sarcocornia ambigua from a plant bed at LCM were cut into 10 cm cuttings of

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the main stem without branches and beveled at the top. These cuttings were planted in polystyrene trays with 128 cells, using fertile soil, sand, and perlite as

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a substrate, in a ratio of 1:1:1. The trays were placed in a dark room, and the

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cuttings were irrigated with tap water every two days. After one month the

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seedlings began to receive sunlight in the morning and were irrigated every two days with seawater diluted to 50% concentration, remaining in these conditions for another 30 days. After this period, 144 seedlings were weighed individually (mean weight 3.9 ± 0.9 g) and transferred to the aquaponic system. 2.2 Experimental design, experimental units, and system management The experiment consisted of evaluating four different salinities in the cultivation of shrimp L. vannamei and halophyte S. ambigua in aquaponics: 8 psu, 16 psu, 24 psu, and 32 psu. Each treatment had three replicates, totaling twelve experimental units that were randomized in a 243 m² greenhouse.

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Each experimental aquaponic unit consisted of an 800 L circular polyethylene tank with a titanium heater, aeration, and artificial substrates for the shrimp cultivation; a 40 L settling chamber and a hydroponic bench for the plants (Fig. 1). The tanks were covered with a shade net (50% shading). Figure 1. One day before the start of the experiment, the tanks were filled with 400

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L of water from the biofloc nursery tank, with a salinity of 20 psu. This water had a concentration of total suspended solids of 460.0 mg L−1, total ammonia

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nitrogen of 1.0 mg L−1, nitrite of 0.5 mg L−1, nitrate of 9.8 mg L−1 and

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orthophosphate of 2.2 mg L−1. This biofloc was already in the chemoautotrophic

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stage, with the nitrification process established. Thus, during the trial, the addition of organic carbon was not necessary for the maintenance of water

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quality parameters (Ebeling et al., 2006).

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Each tank was stocked with 240 shrimp with an average weight of

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1.6±0.1 g, representing a stocking density of 300 shrimp m−3. Then, shrimp were slowly acclimated. Tap freshwater and filtered seawater were added to the tanks to reach 800 L volume and the desired salinity in each treatment at a rate of 2 psu per hour, according to the protocol proposed by Van Wyk (1999a). Major cations (Na+, Ca2+, K+, and Mg2+) were analyzed to characterize the mineral content in the water of each treatment and the seawater used in the experiment (Table 1). Water samples were collected and frozen at the beginning of the experiment. Before the assay, the samples were centrifuged at 14,000 RPM (model MiniSpin Plus, Eppendorf, Germany) and then diluted with deionized water (Milli-Q system, Millipore, USA). The assays were conducted in

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a capillary electrophoresis system (model 7100, Agilent Technologies, USA), following the methodology proposed by Rizelio et al. (2012). Table 1. The aquaponic structure was constructed and operated according to Pinheiro et al. (2017). In the hydroponic bench for growing plants, the irrigation channels were formed by four PVC pipes of 75 mm diameter and 1.10 m length,

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arranged side by side, placed on wooden supports with a 4% slope. Each bench had 0.3 m2 of planting area, and twelve S. ambigua seedlings were used

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in each experimental unit, which corresponds to a density of 40 plants m -2. A 40

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L settling chamber was used before irrigation to protect roots from excess solids

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from shrimp tanks. The tank water was pumped continuously to the settling chamber at a flow rate of 3.0 L min-1 using a submerged pump (model SB650,

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Sarlo Better, Brazil), and distributed in each channel by gravity. After irrigating

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the plants, the water returned to the tank by gravity. To maintain the adequate

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concentration of suspended solids in the water for shrimp culture (Schveitzer et al., 2013) every 30 minutes the sludge accumulated in the settling chamber was pumped for 40 seconds back into the tank through an electric pump (model EBE 01, Emicol, Brazil) connected to the bottom outlet of the settling chamber, at a flow rate of 15 L min-1. Shrimp were fed four times daily (8 a.m., 11 a.m., 2 p.m. and 5 p.m.) with a commercial diet containing 38% crude protein (Poti Mirim QS 1.6 mm, Guabi, Brazil). The quantity was supplied according to the feed table proposed by Van Wyk (1999b). About 20% of each ration was put on feed trays to evaluate consumption. Every week 24 shrimp from each experimental unit were sampled

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and weighed to make feeding adjustments. Calcium hydroxide was added when alkalinity was below 120 mg CaCO3 L-1, at a ratio of 20% of daily feed intake. Throughout the experimental period, there was no renewal of water, and only the volume lost by evaporation was replaced, to maintain the salinity of each treatment. The experiment lasted eight weeks and was conducted from February 23, 2018, to April 23, 2018, totaling 57 days. The light intensity above

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the plants was measured hourly every day (between 8 a.m. and 6 p.m.) and

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ranged from 96.0 to 1360.3 μmol photons m-2 s-1. The photoperiod during the

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experiment was 13 h light and 11 h dark.

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2.3 Water quality variables

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During the experiment, dissolved oxygen and temperature were measured twice per day, at 8 a.m. and 5 p.m. (oxygen meter model Pro20, YSI,

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USA). Salinity was measured daily in the morning (conductivity meter model

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EC300A, YSI, USA). The analysis of pH (pH meter model TEC-11, Tecnal,

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Brazil), total suspended solids (TSS), volatile suspended solids (VSS), alkalinity (APHA, 2005), total ammonia nitrogen (TAN) and nitrite (Strickland and Parsons, 1972) were conducted twice a week. Nitrate (cadmium reduction method NitraVer® 5, Hach, USA) and dissolved orthophosphate (Strickland and Parsons, 1972) were analyzed once a week. 2.4 Performance indexes of shrimp After the experimental period, the following zootechnical indexes were evaluated: 

Survival (%) = [final number of animals / initial number of animals]*100

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

Average final weight (g) = biomass (g) / final number of animals

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Weekly weight gain (grams per week) = {[average final weight (g) – average initial weight (g)] / days of culture}*7 Final biomass (g tank-1) = total biomass harvested per tank

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Productivity (kg m-3) = final biomass (kg) / tank volume (m³)

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Feed conversion ratio (FCR) = feed intake (g) / biomass gain (g)

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Feed intake (kg tank-1) = total amount of feed added per tank

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

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2.5 Plant production indexes

At the end of the cultivation, the aerial part of each plant was weighed

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individually. The roots were discarded for having a tangle of roots, perlite, and

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support screen that could not be quantified. The average final weight (g), final biomass (kg), and yield (g m-2) were then calculated.

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2.6 Nitrogen and phosphorus use efficiency To determine the total Kjeldahl nitrogen content (TKN) (AOAC

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International, 2005) and total phosphorus (Instituto Adolfo Lutz, 2008), 50 grams of the feed were sampled and, after the harvest, 100 grams of shrimp and 50 grams of Sarcocornia were collected from each experimental unit. Nitrogen use efficiency (NUE,%) and phosphorus use efficiency (PUE,%) were calculated using the biomass gain of shrimp (g), fresh biomass of plants (aerial part, in grams), feed intake (g) and the content of TKN (%) and phosphorus (%) of shrimp, plant and feed. 2.7 Analysis of antioxidant activity and total phenolic compounds of Sarcocornia ambigua

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Samples of S. ambigua were first prepared by separating the branches from the stems and ground in a mortar with liquid nitrogen. Plant extracts from each experimental unit were prepared using 10 g of fresh sample (aerial part) with 25 mL of methanol in an ultrasonic bath (model 1400a, Unique, Brazil) at room temperature for one hour. Subsequently, they were centrifuged at 10,000 RPM for 5 minutes (model MiniSpin Plus, Eppendorf, Germany). The

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supernatant was then recovered for the analysis. Antioxidant capacity was estimated by the DPPH (2,2-diphenyl-1-

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picrylhydrazyl) radical-scavenging method according to Brand-Willians et al.

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(1995) and was expressed in fresh weight as micromoles of Trolox equivalent antioxidant capacity per 100 g of fresh matter (µmol TEAC 100 g−1 FM) (Bertin

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et al., 2014).

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Total phenolic content was determined spectrophotometrically according

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to the Folin-Ciocalteu method (Singleton and Rossi, 1965). Absorbance was read at 765 nm, and results were compared to a standard curve of the gallic

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acid solution and expressed in fresh weight as milligrams of gallic acid equivalents per 100 g of fresh matter (mg GAE 100 g−1 FM). 2.8 Statistical analysis

Data were submitted to second-order polynomial regression analysis (α=0.05) (Yossa and Verdegem, 2015) using GraphPad Prism software version 6.01, and the interpolated salinities (that is, the maximum or minimum points of each variable) were estimated by deriving the quadratic equation. 3. Results

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3.1 Performance of Litopenaeus vannamei Salinity affected the survival of the shrimp, and the maximum values, according to the interpolation, were found in the salinity 25.7 psu (Fig. 2). The average final weight and weekly weight gain were not affected by the salinities evaluated (Table 2).

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Table 2.

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Figure 2.

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3.2 Performance of Sarcocornia ambigua

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parameters for S. ambigua (Table 3).

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No salinity relationships (p>0.05) were detected with any of the analyzed

Table 3.

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3.3 Water quality parameters

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The salinity was controlled daily and remained within the range

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determined for each treatment. The temperature was similar in all tanks, and the dissolved oxygen remained within the comfort range for L. vannamei (Boyd, 1989). The pH remained constant throughout the experiment period and did not present a significant relationship between the salinities of the treatments (p>0.05). There is no relationship between salinity and alkalinity values (Table 4). Table 4. The concentration of TSS increased over the weeks in all treatments, but there was no relation between the different salinities. The same trend was

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observed in the concentration of VSS (p>0.05). Concentrations of TAN and nitrite remained stable throughout the experimental time in all treatments (p>0.05) (Fig. 3a and 3b), and the minimum concentrations were found in the interpolated salinities 18.0 psu and 18.8 psu, respectively. There was an accumulation of nitrate in all treatments during the weeks of cultivation (p<0.05) (Fig 3c), reaching its maximum point in salinity 18.1 psu

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(Fig 4). The salinity also affected the concentration of dissolved orthophosphate, and the maximum concentration was reached at salinity 13.5

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psu.

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Figure 3.

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Figure 4.

3.4 Nitrogen and phosphorus use efficiency

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Nitrogen contents in the feed, shrimp, and plant were 6.2±0.2%,

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2.8±0.1%, and 0.8±0.0%, respectively. Phosphorus content was 3.6±0.1%,

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1.0±0.1%, and 0.2±0.0% in the feed, shrimp, and plant, respectively. Table 5 shows the data of N and P recovery in each treatment. There is a relationship between the salinities in the phosphorus use efficiency (p=0.0021; y=12.66+0.4101x–0.0068x²; R²=0.38), and its maximum point was estimated in the salinity 30.2 psu. However, the nitrogen use efficiency was not affected by salinity (p=0.2656; R²=0.53). Table 5. 3.5 Total phenolic compounds and antioxidant activity in Sarcocornia ambigua

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The phenolic content of S. ambigua extract determined from the standard curve of gallic acid was 16.6±3.3; 19.6±5.3; 15.2±2.6 and 13.2±2.2 mg GAE 100 g−1 FM in the treatments 8, 16, 24 and 32 psu respectively. The antioxidant activity measured by DPPH was 20.3±2.7; 17.0±9.9; 12.2±1.2 and 18.7±5.2 µmol TEAC 100 g-1 FM in the treatments 8, 16, 24 and 32 psu respectively. No statistical relationships were found between phenolic compounds (p=0.1285;

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R²=0.2414) and antioxidant activity (p=0.2201; R²=0.1880) and the tested salinities.

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4. Discussion

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The shrimp Litopenaeus vannamei inhabits natural environments with a

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salinity range of 1 to 50 psu (Perez-Velazquez et al., 2013). In this experiment, a direct relationship was found between the reduction of salinity and the

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increase in shrimp mortality. The same behavior was also observed by Decamp

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et al. (2003), Maicá et al. (2012) and Zacarias et al. (2019). This low survival

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may be related to the mineral composition of the water. Since the waters were prepared using a biofloc inoculum with a salinity of 20 psu, the concentration of ions in the 8 psu treatment, and also the ratio between sodium and potassium (Na:K), is much lower than that found in the other treatments, as shown in Table 1. Even though it is a euryhaline species, to ensure satisfactory survival and growth of L. vannamei in low salinity the proportions of ions such as sodium, potassium, and magnesium should be close to those found in seawater (Boyd and Thunjai, 2003; Roy et al., 2010; Valenzuela-Madrigal et al., 2017). Although they had no significant relationship with salinity, other parameters of zootechnical performance were affected by survival on 8 psu

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treatment. Possibly the decrease in density caused by mortality improved the space available in these tanks, resulting in higher average final weight and weekly weight gain (Araneda et al., 2008; Samocha et al., 2004). Furthermore, according to the interpolation, the maximum survival was found at salinity 25.7 psu, which is close to the isosmotic point of L. vannamei (24.7 to 26 psu) (Castille and Lawrence, 1981).

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The productive potential of halophyte plants can be determined by the species and the salinity to which it is subjected during cultivation (Ventura et al.,

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2011; Ventura and Sagi, 2013). Halophytes of the Amaranthaceae family, such

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as S. ambigua, have their growth stimulated in the presence of NaCl, with the salinity being between 150 and 300 mM NaCl ideal for their development

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(approximately 8 to 17 psu) (Rozema and Schat, 2013; Ventura et al., 2011).

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Although there was no significant relationship between plant performance and

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salinity, the highest yield was achieved in the 16 psu treatment, and the maximum productivity and final weight were estimated at salinities close to that

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(17.5 psu and 16.4 psu respectively). Species of Salicornia and Sarcocornia genera are characterized by low growth and productivity when irrigated with full marine water (Ventura et al., 2011). In the same aquaponic system using seawater, Silva (2016) and Soares (2017) reached a productivity of 1.9 and 1.1 kg m-2 of plants, respectively. In general, plants can absorb nitrogen in the form of nitrate or ammonia (Barker and Pilbeam, 2015), but in saline environments, with high chloride (Cl-) concentrations, NH4+ uptake may predominate, and NO3 use is inhibited (Cartaxana et al., 1999; Kudo and Fujiyama, 2010). In this experiment, the

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lowest concentrations of ammonia and nitrite and the highest concentrations of nitrate were found near the 16 psu salinity. So, it is suggested that in this salinity, the absorption of ammonia by the plants is favored. In aquaponics systems, nitrate accumulation can occur when the rate of NO3 generation exceeds the amount of that nutrient the plant can use (Rakocy, 2012; Seawright et al., 1998). Therefore, the increase in NO3 concentrations in the treatments

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during the cultivation may also have occurred because the plants stop absorbing nitrate when they reach the requirement of this nutrient (Wongkiew et

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al., 2017).

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In systems with low water exchange, such as BFT, the increase in orthophosphate concentrations is expected because, unlike ammonia,

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phosphorus is not lost to the atmosphere and elimination through water renewal

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is practically non-existent (Silva et al., 2013). In this study, the low concentrations of PO43- did not affect the development of S. ambigua, since

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values as low as 0.3 mg L-1 are sufficient for the development of halophytic

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plants (Buhmann et al., 2015). The orthophosphate accumulation during the weeks of cultivation occurred due to shrimp metabolism and feed intake. We used a feed table to determine the daily amount of feed to be added in the tanks, and since we couldn’t see feed leftover in the trays of the 8 psu treatment tanks, despite the mortality which kept adding the quantity determined by the feed table. So, the significant relationship between orthophosphate concentrations and salinity may be related to higher shrimp mortality in the 8 psu treatment, since the primary source of phosphorus in the culture water is the decomposition of not consumed feed (Páez-Osuna et al., 1997; Silva et al.,

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2013). The same behavior was reported by Maicá et al. (2012), who observed an orthophosphate increase in treatments with lower salinity and higher mortality. The use efficiency of nitrogen and phosphorus can be determined as the amount (or percentage) of these nutrients that are recovered as a final product (Barker and Pilbeam, 2015). Thus, the efficiency of an aquaculture system can

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be evaluated based on the conversion of N and P into harvested biomass (Endut et al., 2013). In this experiment, the recovery of N in L. vannamei

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biomass (26.3 ± 2.3%) was similar to that found in intensive cultures of penaeid

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shrimp (Funge-Smith and Briggs, 1998; Thakur and Lin, 2003). In aquaponics systems, the use of N may be increased by up to 25% (Hu et al., 2015).

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Nitrogen uptake by the plant is influenced by factors such as the concentration

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of this nutrient in the water and the age of the plant (Barker and Pilbeam, 2015;

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Mariscal-Lagarda et al., 2012). Pinheiro et al. (2017) after 73 days of aquaponic production of S. ambigua with L. vannamei were able to increase the NUE of

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the system by almost 10% due to the high productivity of plants (8.2 ± 0.3 kg m 2

) and higher concentration of nitrate in the water (21.4 ± 17.0 mg N-NO3 L-1).

Therefore, the low S. ambigua production achieved in this experiment, and the low N content in the plant was probably not enough to increase the NUE of the system. Phosphorus recovery in shrimp biomass was higher (17.4 ± 2.2%) than those reported by Casillas-Hernández et al. (2006) (13.6%) and Páez-Osuna et al. (1997) (6.1%). The concentration of phosphorus in S. ambigua shoots was 0.20 ± 0.09% and is within the expected range since in plants they vary from

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0.1% to 1%, and new and succulent tissues present a more considerable amount of P than those that are already lignified (Barker and Pilbeam, 2015). The significant relationship between PUE and salinity is unclear, but may be related to the increase of shrimp biomass at higher salinities and, consequently, higher consumption of feed with high phosphorus content as was used in this experiment (Casillas-Hernández et al., 2006).

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The production of antioxidant compounds is one of the responses of plant metabolism to oxidative stress (Bertin et al., 2014; Ksouri et al., 2008).

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The production of these compounds may vary according to the species and

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environmental conditions to which the plants are submitted, like salinity, availability of water and nutrients, and light intensity (Buhmann and

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Papenbrock, 2013; Ventura and Sagi, 2013). Growth under conditions other

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than those considered ideal may induce stress and, consequently, increase

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secondary metabolites, such as antioxidants (Boestfleisch et al., 2014). In the S. ambigua samples analyzed at the end of the experiment, both the phenolic

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compounds content and the antioxidant activity were below that reported by other authors in the same culture system (Pinheiro et al., 2017; Silva, 2016). 5. Conclusion

The cultivation of L. vannamei integrated with S. ambigua can be performed between salinities of 16 and 24 psu since the performance of the shrimp is not impaired and the growth of the plants and the removal of nitrogen and phosphate compounds are favored in this salinity range. 6. Acknowledgments

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The authors would like to thank Ângela Kugelmeier, Matheus Rocha, Moisés Poli, Esmeralda Chamorro Legarda, Bruno Pierri, Paulo Pinto, and Claudia Machado for invaluable support conducting the experiment. 7. Funding This work was supported by the Coordenação de Aperfeiçoamento de

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Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 (the

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scholarships were to the first two authors) and by Conselho Nacional de

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Desenvolvimento Científico e Tecnológico – CNPq (Ciências do Mar 2 Project 43/2013 AUXPE 1969/20). Felipe Vieira, Ana Carolina Costa, Roseane Fett,

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and Walter Seiffert received productivity research fellowships from CNPq.

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8. References

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Yossa, R., Verdegem, M., 2015. Misuse of multiple comparison tests and underuse of contrast procedures in aquaculture publications. Aquaculture 437, 344–350. https://doi.org/10.1016/j.aquaculture.2014.12.023

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Zacarias, S., Schveitzer, R., Arantes, R., Galasso, H., Pinheiro, I., Santo, C.E., Vinatea, L., Espirito Santo, C., Vinatea, L., 2019. Effect of different concentrations of potassium and magnesium on performance of Litopenaeus vannamei postlarvae reared in low-salinity water and a biofloc system. J. Appl. Aquac. 31, 85–96. https://doi.org/10.1080/10454438.2018.1536009

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Fig. 1. The experimental aquaponic unit used in the experiment. Adapted from Pinheiro et al. (2017).

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Fig. 2. Quadratic regression of survival data of Litopenaeus vannamei cultured at salinities 8 psu, 16 psu, 24 psu, and 32 psu. The dotted vertical line indicates the maximum point obtained by deriving the equation. Fig. 3. (a) Total ammonia nitrogen, (b) nitrite and (c) nitrate in tanks of Litopenaeus vannamei cultured in the aquaponic system at different salinities for eight weeks. Fig. 4. Quadratic regression of (a) TAN, (b) NO2, and (c) NO3 concentrations in water of Litopenaeus vannamei cultivation at different salinities. The dotted vertical line indicates the interpolated salinities obtained by deriving the equation.

Table 1. Concentrations (mean ± standard deviation) and ratios of major ions of seawater and water in tanks of Litopenaeus vannamei in the aquaponic system at different salinities.

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Table 2. Production indexes of Litopenaeus vannamei cultured in the aquaponic system at different salinities during 57 days at a stock density of 300 shrimp m3 . Data are a mean ± standard deviation. ns: not significative. Feed intake was not submitted to statistical analysis. Table 3. Production indexes of Sarcocornia ambigua cultured in the aquaponic system at different salinities for eight weeks. Data are a mean ± standard deviation.

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Table 4. Water quality variables in tanks of Litopenaeus vannamei cultured in the aquaponics at different salinities during 57 days, at a stocking density of 300 shrimp m-3. Data are a mean ± standard deviation. Temperature, dissolved oxygen, and salinity were not submitted to statistical analysis. ns: not significative.

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Table 5. Nitrogen and phosphorus use efficiency in shrimp and plants after 57 days of cultivation in the aquaponic system at different salinities. Data are a mean ± standard deviation.

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Table 1. Concentrations (mean ± standard deviation) and ratios of major ions of seawater and water in tanks of Litopenaeus vannamei in the aquaponic system at different salinities. Major Ions

Treatment

Seawater

16 psu

24 psu

32 psu

K+ (mg L1 )

366.8 ± 72.4

285.0 ± 32.1

734.0 ± 2.3

797.8 ± 7.4

Na+ (mg L-1)

3145.9 ± 305.1

5365.2 ± 309.6

11208.0 ± 359.3

13735.3 ± 616.5

18644 ±

Ca (mg L-1)

318.5 ± 47.9

406.4 ± 18.7

1007.0 ± 47.7

1033.8 ± 64.2

1164.4 ± 43.2

Mg2+ (mg L-1)

357.6 ± 62.1

679.8 ± 27.3

1319.2 ± 43.8

1448.0 ± 155.5

2166.4 ±

Na:K

8.7:1

18.9:1

15.3:1

17.2:1

27.9:1

Ca:K

0.9:1

1.4:1

1.4:1

1.3:1

1.8:1

Mg:Ca

1.1:1

1.7:1

1.3:1

1.4:1

1.9:1

Mg:K

1.0:1

2.4:1

1.8:1

1.8:1

3.3:1

674.0 ± 126.4

1644.8

100.2

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2+

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8 psu

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Table 2. Production indexes of Litopenaeus vannamei cultured in the aquaponic system at different salinities during 57 days at a stock density of 300 shrimp m3

.

Parameter

Treatment 8 psu

16 psu

24 psu

32 psu

pvalue

Quadratic effect

0.038 9

y= 26.47 + 4.674x – 0.091x² R² = 0.8427

56.3 ± 4.7

83.3 ± 1.2

82.6 ± 4.3

84.0 ± 4.0

Average final weight (g)

12.7 ± 0.3

11.5 ± 0.4

11.6 ± 0.2

11.8 ± 0.5

0.308 2

ns

Weekly weight gain (g week-1)

1.4 ± 0.0

1.2 ± 0.0

1.2 ± 0.0

1.2 ± 0.1

0.524 2

ns

Final biomass (g tank-1)

1826.7 ± 223.7

2190.0 ± 151.0

2296.7 ± 159.5

2376.7 ± 83.3

0.597 8

ns

Productivity (kg m -3)

2.3 ± 0.3

2.7 ± 0.2

3.0 ± 0.1

0.597 8

ns

Feed conversion ratio

2.0 ± 0.1

1.8 ± 0.1

1.6 ± 0.1

1.6 ± 0.1

0.833 5

ns

Feed intake (kg tank-1)

2.8 ± 0.2

3.1 ± 0.0

3.1 ± 0.0

-

-

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2.9 ± 0.2

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3.0 ± 0.1

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Survival (%)

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Data are a mean ± standard deviation. ns: not significative. Feed intake was not submitted to statistical analysis.

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Table 3. Production indexes of Sarcocornia ambigua cultured in the aquaponic system at different salinities for eight weeks. Treatment

pvalue

Parameter 16 psu

24 psu

32 psu

Average final weight (g)

17.3 ± 13.4

21.4 ± 11.1

13.7 ± 9.0

12.2 ± 9.3

0.3554

Final biomass (g tank-1)

138.2 ± 36.0

182.4 ± 34.6

138.0 ± 14.2

114.3 ± 14.9

0.1672

Productivity (kg m -2)

0.46 ± 0.12

0.61 ± 0.12

0.46 ± 0.05

0.38 ± 0.05

0.2838

Survival (%)

66.7 ± 0.0

61.1 ± 4.8

61.1 ± 25.5

63.9 ± 21.0

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8 psu

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Data are a mean ± standard deviation.

0.2843

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Table 4. Water quality variables in tanks of Litopenaeus vannamei cultured in the aquaponics at different salinities during 57 days, at a stocking density of 300 shrimp m-3. Treatment

pvalu e

Quadratic effect

16 psu

24 psu

32 psu

Salinity (psu)

8.4 ± 0.2

16.4 ± 0.2

24.5 ± 0.3

32.4 ± 0.5

-

-

Temperatur e (°C)

29.3 ± 0.2

29.2 ± 0.2

29.5 ± 0.2

29.4 ± 0.3

-

-

Dissolved oxygen (mg L-1)

6.35 ± 0.21

5.97 ± 0.10

5.62 ± 0.10

5.47 ± 0.06

-

-

pH

8.07 ± 0.10

7.98 ± 0.02

8.01 ± 0.03

8.00 ± 0.04

0.31 29

ns

Alkalinity (mg CaCO 3 L-1)

123.9 ± 2.4

125.9 ± 2.5

136.4 ± 3.2

0.64 04

ns

Total suspended solids (mg L1 )

251.9 ± 30.2

344.1 ± 28.3

329.0 ± 36.5

308.2 ± 62.1

0.37 01

ns

82.9 ± 2.4

69.5 ± 3.4

68.5 ± 0.7

73.3 ± 1.5

0.40 82

ns

0.30 ± 0.06

0.22 ± 0.02

0.24 ± 0.02

0.39 ± 0.09

0.91 78

ns

0.20 ± 0.02

0.20 ± 0.03

0.46 ± 0.05

0.39 05

ns

Nitrite (mg NO2-N L-1) Nitrate (mg NO3-N L-1) Orthophosp hate (mg PO43--P L-1)

0.35 ± 0.04

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151.2 ± 5.0

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TAN (mg L-1)

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Volatile suspended solids (%)

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8 psu

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Parameter

6.32 ± 0.65

8.58 ± 0.94

6.55 ± 0.90

5.86 ± 1.16

0.04 78

y= 3.993 + 0.4184x – 0.01153x² R² = 0.4155

2.34 ± 0.19

2.86 ± 0.09

1.89 ± 0.11

1.88 ± 0.13

0.00 01

y= 2.167 + 0.05404x – 0.002x² R² = 0.5037

Data are a mean ± standard deviation. Temperature, dissolved oxygen , and salinity were not submitted to statistical analysis. ns: not significative.

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Table 5. Nitrogen and phosphorus use efficiency in shrimp and plants after 57 days of cultivation in the aquaponic system at different salinities. Treatment

Parameter

8 psu

16 psu

173.1 ± 17.7

187.5 ± 4.5

192.7 ± 1.0 193.8 ± 0.0

Total N in shrimp biomass (g)

40.7 ± 5.2

50.3 ± 5.8

51.7 ± 4.0

54.9 ± 0.5

Total N in salicornia biomass (g)

1.1 ± 0.3

1.1 ± 0.3

0.7 ± 0.5

0.7 ± 0.3

Nitrogen use efficiency shrimp + salicornia (%)

24.1 ± 0.7

27.4 ± 2.4

27.2 ± 2.2

28.7 ± 0.4

P intake by feed (g)

99.3 ± 10.1

107.5 ± 2.6

110.5 ± 0.6 111.1 ± 0.0

Total P in shrimp biomass (g)

14.6 ± 2.1

20.5 ± 1.8

18.3 ± 1.7

Total P in salicornia biomass (g)

0.26 ± 0.07

Phosphorus use efficiency shrimp + salicornia (%)

14.9 ± 0.7

32 psu

pr

21.4 ± 0.6

0.17 ± 0.11 0.14 ± 0.05

19.3 ± 1.3

16.7 ± 1.5

e-

0.27 ± 0.09

19.4 ± 0.6

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al

Pr

Data are a mean ± standard deviation.

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N intake by feed (g)

24 psu

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December 5th, 2019.

Dear editorial board of Aquaculture,

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This manuscript has not been published or presented elsewhere in part or entirety and is not under consideration by another journal. All the authors have approved the manuscript and agree with submission to your esteemed journal. There are no conflicts of interest to declare.

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Sincerely,

Laboratório de Camarões Marinhos

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Universidade Federal de Santa Catarina

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Isabela Pinheiro

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Beco dos Coroas, n 503, Barra da Lagoa, Florianópolis, SC. Brazil.

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Phone number: +55 48 37214118. E-mail: [email protected]

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CRediT author statement

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Isabela Pinheiro: Conceptualization, Methodology, Formal Analysis, Investigation, Writing – Original Draft. Ramon Carneiro: Investigation, Writing – Original Draft, Visualization. Felipe Vieira: Conceptualization, Methodology, Formal Analysis, Writing – Review & Editing. Luciano Gonzaga: Resources, Writing – Original Draft. Roseane Fett: Resources, Supervision. Ana Carolina Costa: Resources, Supervision. Francisco Magallón-Barajas: Conceptualization, Validation, Writing – Review & Editing, Supervision. Walter Seiffert: Conceptualization, Methodology, Writing – Review & Editing, Project Administration.

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Highlights 

Sarcocornia ambigua and Litopenaeus vannamei can be cultivated in aquaponics in salinity from 16 psu.



At intermediate salinities, between 16 and 24 psu, S. ambigua can absorb nitrogen as ammonium rather than nitrate. An aquaponic culture of shrimp and S. ambigua can be an alternative to

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recycle the nutrients of the biofloc system.

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

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Figure 1

Figure 2

Figure 3

Figure 4