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Effect of wastewater from a pikeperch (Sander lucioperca L.) recirculated aquaculture system on hydroponic tomato production and quality
Agricultural Water Management 226 (2019) 105814
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Effect of wastewater from a pikeperch (Sander lucioperca L.) recirculated aquaculture system on hydroponic tomato production and quality
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Boris Delaide , Stefan Teerlinck, An Decombel, Peter Bleyaert INAGRO, Ieperseweg 87, Rumbeke-Beitem, B-8800, Belgium
A R T I C LE I N FO
A B S T R A C T
Keywords: Aquaponics Hydroponics RAS Greenhouse Manganese Blossom-end rot
Decoupled aquaponic systems (DAPS) use the wastewater of recirculated aquaculture systems (RAS) as water source for plant production in recirculated hydroponic systems. RAS wastewater is complemented with macroand micronutrients to obtain equivalent concentrations and pH as in standard hydroponic nutrient solutions (NS). Unlike in single recirculating aquaponic systems, optimal growth conditions can be established in each production part of a DAPS (i.e. fish and plant parts) avoiding compromises. DAPS design seems more adapted for commercial farming operations but feasibility studies on large-scale systems are lacking. Therefore, the production of tomatoes (Solanum lycopersicum L., cv. Foundation) grown in a NS based on complemented pikeperch RAS wastewater (i.e. AP treatment) has been compared to that of tomatoes grown in conventional hydroponic NS (i.e. HP treatment), in semi-practice conditions. During 3 consecutive years, tomatoes were grown on rockwool slabs, in a large-scale Venlo-type climate-controlled greenhouse, using a recirculated drip irrigation system identical to the ones used by the professionals of the hydroponic tomato sector. While the electroconductivity was significantly higher in the AP treatment due to the presence of NaCl in the RAS wastewater, no significant differences for the total and marketable fruit yields, fruit number, and size were found between the AP and HP treatments. However, while the level of blossom-end rot (BER) varied substantially (0.9–18.6 %) in the HP treatment, it was remarkably constant and low (0.2-0.4%) over the years in the AP treatment, suggesting a beneficial effect of RAS wastewater. Our results clearly indicate the suitability of complemented pikeperch RAS wastewater as feeding water for professional HP tomato production using drip irrigation for DAPS. As RAS water contains a diversity of microorganisms and dissolved organic matter, it is assumed that some of these acted as plant biostimulants and mitigated the salinity stress and the BER symptoms.
1. Introduction To balance the fish demand of a growing population while respecting the fishing quotas, the aquaculture sector has seen a rapid expansion in these last 30 years (Pulvenis, 2016). Lately, recirculating aquaculture systems (RAS) have been developed, allowing to drastically reduce the water consumption per kilo of fish produced (e.g. less than 100 L in RAS while several thousands of litre in conventional systems) (Martins et al., 2010). Integrating aquaculture with other food production methods is under development in order to reuse the aquaculture wastes (Klinger and Naylor, 2012; Turcios and Papenbrock, 2014) and to close the nutrient cycle. The potential for more efficient use of resources through the tightening of nutrient cycles and reuse of aquaculture wastewater may explain the increasing interest in aquaponics (AP) (Love et al., 2015a). The AP concept is to combine RAS and recirculated hydroponic systems (RHS) for fish and horticultural plant
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production. The integration of RAS and RHS aims to reuse the aquaculture wastewater for irrigating the crops while converting the otherwise wasted nutrients excreted by fish into valuable plant biomass. Hence, the reuse of fish wastewater could significantly reduce the environmental impact of aquaculture and hydroponic plant production. The most common design of the AP system is the integration of hydroponic beds into the water loop of a RAS (Delaide et al., 2015; Rakocy, 2012) and may be called single recirculating aquaponic system (SRAP) (Suhl et al., 2016). SRAP can be complex to manage as three different biological systems (fish, plants and microorganisms) are merged in a single water loop. Decoupled aquaponic systems (DAPS) (Goddek et al., 2016) or double recirculating aquaponic systems (DRAPS) (Suhl et al., 2016) present an alternative design to overcome the disadvantages of SRAP. In these decoupled systems, the RAS wastewater goes to the hydroponic part (i.e. the RHS part) and does not return to the fish. The water would
Corresponding author at: INAGRO, Ieperseweg 87, Rumbeke-Beitem, B-8800, Belgium. E-mail addresses: [email protected] (B. Delaide), [email protected] (P. Bleyaert).
https://doi.org/10.1016/j.agwat.2019.105814 Received 16 November 2018; Received in revised form 13 September 2019; Accepted 20 September 2019 0378-3774/ © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
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by a conventional standard hydroponic NS. The drain water of each treatment was collected separately in a 1 m³ drain water storage tank. Intermittently, their entire content was sand filtrated, and UV disinfected. The disinfected drain waters were stored in their corresponding disinfected drain water storage tank (Fig. 1). The filtration event only happened when a disinfected drain water storage tank became empty. The same sand filtration and UV disinfection device was used for AP and HP drain waters, but the system automatically cleaned and flushed the filter and pipes with the new incoming solution before each use. The disinfected drain solution was thus reused into its respective fertigation loop each time a batch of new feeding solution was made (i.e. from once per week to once per day depending on daylight duration and intensity). The tomato plants were cultivated in a compartment of a Venlo-type climate-controlled greenhouse of 352 m². The greenhouse had a column height of 4 m, covered with 4 mm glass and warmed by a conventional floor level pipe heating system. The experiment was conducted during 3 consecutive seasons of tomato production, from 06.01.2015 to 07.11.2017. The cultivar Foundation (Bayer-Nunhems, Haelen, The Nederlands) was used in 2015, 2016 and 2017. In 2017, the cultivars Axxy (Axia, Naaldwijk, The Netherlands) and Merlice (De Ruiter, Bergschenhoek, The Netherlands) were tested also. The cultivars were all grafted on rootstock Maxifort (De Ruiter, Bergschenhoek, The Netherlands) in 2015 and on DR 0141TX (De Ruiter, Bergschenhoek, The Netherlands) in 2016 and 2017.
then leave the hydroponic part only by evaporation (almost negligible) and plant transpiration. Optimal growing conditions can then be established in each production part (i.e. in RAS and RHS parts) avoiding compromises. In the hydroponic part, the RAS wastewater is complemented with macro- and micronutrients to obtain equivalent concentrations, pH and EC as in the standard RHS nutrient solutions (Goddek et al., 2016). With this design the production and some sanitary aspects (e.g. cleaning, quarantine, etc.) can be more easily controlled making the system more adapted for commercial farming operations (Vermeulen and Kamstra, 2013). Also, the existing professional techniques can be easily used in the respective fish and plant parts without high technological innovations. Just a few AP designs have been tested and only in lab conditions or small scale (Delaide et al., 2017; Love et al., 2015b; Suhl et al., 2016), but studies on large-scale systems remain scarce (Rakocy et al., 2004), especially with DAPS. Moreover, comparisons of production in AP and hydroponics under the same conditions as with the techniques used in professional operations are lacking. Despite a few pioneer publications (Delaide et al., 2016a; Saha et al., 2016), the effects of fish water on the yields and quality of the plant products remain unknown, which hinders the adoption of AP by professionals of the horticultural sector. The feasibility of properly complementing the fish water with conventional commercial fertilisers needs to be investigated. Therefore, this study aimed to compare the tomato production of a decoupled aquaponic system to a conventional recirculated hydroponic system in a semi-practice scale. Special attention was given to plant health and physiological disorders as blossom-end rot (BER). The macro and micronutrient content in the nutrient solutions was closely monitored with a specific regard to sodium and chloride levels. It is the first time a reliable comparison of tomato production in complemented RAS wastewater has been achieved and repeated for 3 years.
2.2. Tomato growing conditions An average temperature (T) of 18.0 °C was targeted in the greenhouse. The set-points of the heating system were defined as 20.0 °C and 15.5 °C for day and night, respectively and the ventilation was opened at 22 °C to cool the greenhouse. From mid-May until September, the ventilation was opened at 19 °C. To control the greenhouse climate and irrigation, a computed integrated management software was used (PRIVA Connect, De Lier, The Netherlands). The outside light intensity was measured with a PAR sensor (PRIVA, De Lier, The Netherlands) and a total irradiation sum of 4280.5, 3970.9 and 4011.8 MJ/m² was measured from planting until the last harvest in 2015, 2016, and 2017, respectively. For the experiment in 2015 and 2016, a net surface of 329 m² housed 909 tomato stems (i.e.180 m² for 498 stems and 149 m² for 411 stems, for the HP and AP treatments, respectively). For 2017, a net surface of 658 m² spread over two greenhouse compartments, housed 1818 tomato stems. There were 2 stems per tomato plant and they were topped in early September, each year. The hydroponic cultivation method was the drip irrigation method as described in Heuvelink (2005). The substrate used was rockwool, with slabs of 1 × 0.20 x 0.075 m (Grodan Vital, Roermond, The Netherlands). The slabs were renewed every year. Two plants were set per slab and one dripper was stuck close to the foot of each plant. The slabs were placed on drainage gutters (Meteor Systems BV., Breda, The Netherlands) allowing to recover the drain water for reuse. The space in between plants on the gutters was 0.55 m with 0.80 m distance between gutters, giving a plant density of 2.27 stems per square meter. For both treatments, the pH target of the NS was 5.6. The irrigation pace of the NS was regulated in function of the daily radiation by the computer climate software (PRIVA, De Lier, The Netherlands) aiming a drain water quantity comprised in a range of 20–40 % of the inflow. For each season, studied tomatoes were sown in November and inserted in the drip irrigation system upon the rockwool slabs in January, when the first truss was visible. The fruits were harvested from March to November. The plant pruning, harvesting and support were conducted as in normal tomato greenhouse professional operation as described by Heuvelink (2005).
2. Material and methods 2.1. Experimental setup and operation The experiments were carried out in the facilities of the Inagro research institute located in Rumbeke-Beitem, Belgium (50°54′06.2″N, 3°07′28.0″E). The experimental setup was a semi-practice combination of tomato (Solanum lycopersicum L., cv. Foundation) and pikeperch (Sander lucioperca L.) production. It aimed to combine the techniques already used by professional farmers in Flanders (Belgium). Part of the fish wastewater that otherwise would be flushed to the sewage was used for irrigating the tomatoes. The pikeperch were reared in an indoor recirculating aquaculture system (RAS) operated as a professional farm. The facility had a surface of 700 m² for a total water volume of 160 m³. The RAS had an average fish load of 15 kg/m³ and was able to produce 2000–4000 kg of pikeperch per year. The fish were fed with a fish protein-based meal containing 56% protein and 16% fat (Skretting, Fontaine les Vervins, France). The average daily water exchange rate of 15% was relatively high because the system was conducted in such a way that the water discharged to the sewage had a NO3 content lower than 2.42 mmol/L in order to meet the wastewater disposal regional regulations. The wastewater delivered by the drum filters was decanted and the supernatant was stored in a 15 m³ tank prior to be discharged in the sewage. At regular intervals, part of this water was pumped to the tomato greenhouse facility. This water was then filtrated with a TAF filter (TAF 750, Amiad water system, Chargè, France) and complemented in macro- and micronutrients to reach the standard hydroponic concentrations. The so prepared nutrient solution (NS) was stored in a feeding sump tank of 0.4 m³ (Fig. 1). The water from this sump was used to irrigate the tomato plants and this treatment was called the aquaponic (AP) treatment. The tomato production in the AP treatment was compared to a standard hydroponic (HP) treatment in which the plants were irrigated 2
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Fig. 1. Experimental setup. The wastewater coming from the RAS was pumped to the fish water storage tank. It was filtrated (T) and complemented (N) for tomato drip irrigation (feeding water). The tomato production of plants irrigated with the RAS wastewater (i.e. AP treatment) was compared to that of others irrigated by conventional standard hydroponic solution formulated with a mixture of rainwater and tap water and commercial fertilisers (i.e. HP treatment). The irrigation drain waters were reinserted into their respective fertigation loop, after passing intermittently through a sand filter (S) and a UV-disinfection unit (UV). Both sand filter and UV unit were cleaned automatically before each filtration-disinfection event in order to avoid cross contamination of the respective solutions.
Phosphorus, Potassium, Calcium, Magnesium, and Sulphates), micronutrients (i.e. Iron, Boron, Copper, Zinc, and Manganese), chlorides, sodium and alkalinity was monitored in the slabs and in the drain water once every two weeks for both treatments. The feeding NS were controlled once per month. Every time a new batch of water was pumped from the RAS (i.e. supernatant from the drum filter wastewater) to the fish water storage tank, a new sample was taken for analysis prior to the calculation of the salt complementation. The water samples were brought to the lab for proceeding analysis immediately after the sampling. The concentrations of the nitrogen compounds were determined with a continuous flow analyser (SFA type 4000, Skalar Analytical B.V., Breda, The Netherlands). Total ammoniacal nitrogen (TAN) was determined by the reaction with salicylate, nitroprusside and dichlororisocyanurate reagents in a buffer solution. The nitrite (NO2) was determined with the sulphanilamide and N-(1-naphthyl)ethylenediamine dihydrochloride reagents. Separately, the nitrite plus nitrate (NO2−+NO3−) were reduced in NO2− with the cadmium reduction method and determined with the precited reagents. The NO3- was calculated by subtracting the NO2− concentration determined with the first described method from the concentration obtained with the cadmium reduction method. Concentrations of P ions (H2PO4−, HPO42-, PO43-), K ion (K+), Mg ion (Mg2+), Ca ion (Ca2+), Fe ions (Fe3+, Fe2+), Cu ions (Cu2+, Cu+), Mn ion (Mn2+), Zn ion (Zn2+), B oxides (BO32−, B4O72−), and Na ion (Na+) were determined by inductively coupled plasma-optical emission spectroscopy (optima 8300, PerkinElmer, Zaventem, Belgium). Chloride (Cl−) and sulphate (SO42-) were determined by liquid chromatography (850 Professional IC anion, Metrohm, Antwerpen, Belgium) with a 150 mm column (Metrosep A SUPP 5-150/4.0, Metrohm, Antwerpen, Belgium), following the ISO 10304-1:2007 method. Alkalinity was determined by titration following the ISO 99631:1994 method.
2.3. Determination of tomato production Four randomized plots, comprising ten tomato stems each, were defined per treatment area in the greenhouse. The production of the tomatoes from these plots was followed. This gave an experimental setup of four replicates for each season of production. The plots were located around the centre of the greenhouse to prevent border effects and to assure all plants were studied under the same temperature and lighting conditions. The tomatoes were harvested every 3–4 days. To compare the total yield, the harvested fruits of each plot were counted and weighed. The fruit quality was evaluated, and the fruits were categorized into marketable and non-marketable. Within the non-marketable category, the fruits were sub-categorized into blossom-end rot (BER), cracks due to disturbed moisture balance, and other (damaged during manipulation, not properly ripe, too small, etc.). Unlike the other sub-categories, BER occurred only at specific periods with a higher risk to reduce the weekly marketable yields. Therefore, its yield percentage was calculated only based on these periods. Once a week, the diameter of the second tomato fruit of each truss within each plot was measured. The average fruit diameter was calculated per treatment for each year. The stem growth of the tomato plant was followed weekly by measuring the stem length gain of three plants per plot. 2.4. Water quality measurement The EC and pH of the NS were monitored once a week in the feeding tank, in the slabs and in the drain water. EC was measured with a conductivity tester (ProfiLine Cond 3110, WTW, Weilheim, Germany), and pH with a pH-meter (ProfiLine pH 3110, WTW, Weilheim, Germany). The solution content in macronutrients (i.e. Ammonium, Nitrate, 3
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nutrient content of the RAS wastewater and the drain water, the amount of fertilisers needed was calculated with a specific software (Yarasoft dealerversie 3.0 beta, Yara, Rotterdam, The Netherlands). In 2015, a constant EC was aimed in both objects. In 2016 and 2017, a higher EC in the AP was tolerated, in order to obtain a better reuse of drainwater. Addition of the calculated amounts of fertiliser to the mixture of new water and drain water happened automatically by the Nutronic device (PRIVA, De Lier, The Netherlands), in combination with the PRIVA connect software.
2.5. Sodium monitoring The AP feeding water had a highly variable EC because NaCl was intermittently inserted into the RAS water to prevent fish health problems. It was decided not to dilute the RAS water and thus not to control the EC in the AP feeding NS, leading to a different EC of that in the HP. The fish water was then, independently of its EC, complemented with the macro- and micronutrients to meet the concentration targets (i.e. same as for the HP treatment). It was aimed also to apply in both treatments the same rate of reused drain water. This resulted in a higher EC in the AP treatment compared to conventional hydroponic standards. Occasionally, when weekly growth measurements indicated a reduced growth, the AP drain water was flushed, and the irrigation system was rinsed with the standard solution.
2.7. Statistical analysis The statistical analysis was carried out with the AGROVA statistical package software, developed and validated by Inagro. The experimental data were tested for the null hypothesis that the use of complemented RAS wastewater for the cultivation of tomatoes did not cause any effect as compared to the HP control. For growth, fruit size and yield, combined analysis of variance over 3 years was applied, years being considered as a random variable, and the effect of the treatments being tested against the interaction “years x treatments”. Multiple comparison of means was carried out with the Duncan test. The average nutrient concentrations in the feeding NS and in the slabs, and the results of the Brix measurements (n = 120) were compared with a Duncan test, in addition to ANOVA. As for each time point only one analysis was available per treatment, successive time points were taken as replicates.
2.6. Nutrient solution formulation The standard feeding NS for the HP treatment was formulated with 20% tap water and 80% rain water and by the addition of the following commercial fertilisers (Yara, Rotterdam, The Netherlands): Amnitra (ammoniumnitrate), Calsal (calciumnitrate), Magnesul (magnesiumsulfate), Baskal (potassiumhydroxyde), BFK (potassiumpolyphosphatehydroxyde), Sulfakal (potassiumsulfate), SZ-38 (Nitric acid), DTPA-Fe, Fervent Mn (manganesesulfate), Fervent Zn (Zincsulfate), Fervent B (Boronpotassiumhydroxyde), Fervent Cu (coppersulfate) and Fervent Mo (Molybdenumoxide). The targeted nutrient concentrations for the feeding solutions were as follows, in accordance to general practice in Flanders, for macronutrients (mmol/l): 16 NO3, 1.2 TAN, 1.4 PO4, 9.5 K, 5.4 Ca, 2.4 Mg, 4.4 SO4 and for micronutrients (μmol/L): 30 B, 15 Fe, 0.75 Cu, 10 Mn; 5 Zn, 0.5 Mo. …. The formulation was slightly adjusted during the season according to the plant development following the recommendations of Heuvelink (2005). The NS for the AP treatment was formulated with RAS water and the same commercial fertilisers were added to reach concentrations in macro- and micronutrients equivalent to the standard hydroponic NS. Prior to the experiment, the content in macro- and microelements of RAS water was regularly measured and was found to be relatively constant (Table 1). Every two weeks the NS in both treatments was adjusted using new measurements of the drain water. Based on the desired EC and the
3. Results 3.1. Tomato production For the 3 years studied, the total yields (not shown) and marketable yields (Fig. 2) of tomato fruits of the AP and the HP treatments were not significantly different (Duncan test, p > 0.05). No significant interaction was found between the NS type and the years. Over the overall experiment, the average total yield and the average marketable yield respectively were 48.3 ± 2.4 and 47.3 ± 2.4 kg/m² for the AP treatment, 48.0 ± 1.8 and 46.3 ± 1.8 kg/m² for the HP treatment. Hence, in both treatments there was only a small difference (0,0 to 2,0%) between total and marketable yield. When BER occurred, depending on the year, the yields were affected more strongly (Fig. 3). While the level of BER varied substantially (i.e. range of 0.9–18.6 %) in the HP
Table 1 Nutrient concentrations in RAS wastewater, in AP and HP feeding solutions. RAS wastewater (n = 43)
AP feeding (n = 24)
HP feeding (n = 24)
1.24 ± 0.41 7.85 ± 0.10
3.40 ± 0.70 6.34 ± 0.33
3.15 ± 0.53 6.24 ± 0.32
Macroelements (mmol/L) TAN 0.26 ± 0.31 K 0.30 ± 0.13 Ca 3.58 ± 0.41 Mg 0.71 ± 0.14 NO3 1.52 ± 0.81 SO4 1.03 ± 0.21 PO4 0.07 ± 0.03 Cl 3.58 ± 3.79 Na 3.82 ± 3.73
1.16 ± 0.74 8.60 ± 2.87 6.38 ± 1.60 2.61 ± 0.80 16.97 ± 4.59 4.69 ± 1.35 1.54 ± 0.42 3.58 ± 3.14 4.32 ± 3.04
1.10 ± 0.66 8.84 ± 3.96 6.60 ± 1.37 2.65 ± 0.72 17.93 ± 3.92 4.52 ± 1.15 1.47 ± 0.38 0.60 ± 0.12 1.49 ± 0.35
Microelements (μmol/L) Fe 1.04 ± 1.23 Mn 0.62 ± 0.94 Zn 0.73 ± 0.75 B 6.07 ± 2.38 Cu 0.15 ± 0.22 Mo –
45.01 ± 13.59 12.22 ± 2.70 6.99 ± 2.04 45.01 ± 13.59 0.95 ± 0.39 –
22.45 ± 7.50 12.67 ± 3.25 7.36 ± 2.28 45.50 ± 10.92 0.99 ± 0.31 –
EC (dS/m) pH
60
50
a
a
a
a
a
a
HP AP
40
30
20
10
0 2015
2016
2017
Fig. 2. Yearly average of the marketable yields of tomato for the 4 plots studied. AP: aquaponic treatment, HP: hydroponic treatment. The Duncan test was performed, and different small letters indicate significant differences (p < 0.05).
*Average over the overall experiment ± standard deviation. n = number of measurements; TAN = total ammoniacal nitrogen; - = no measurement. 4
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Fig. 3. Percentage of tomato yields affected by blossom-end rot (BER) during its occurring period for the 4 plots studied. BER occurred from 29/06 to 03/09 in 2015, from 23/05 to 07/09 and from 03/10 to 31/10 in 2016 and from 27/06 to 04/09 in 2017. The Duncan test was performed, and different small letters within the same year indicate significant differences (p < 0.05).
deviated from them with a quite constant value: on average -4.89 mmol/L for AP and -4.25 mmol/L for HP. In addition, analysis of the macro- and micronutrients in solution in slabs revealed significant difference between both treatments only for the Mn in 2016 and 2017 (Table 2). Mn was less concentrated in the AP slabs. In 2015 also, Mn was less concentrated in AP slabs but not significantly. Overall in both treatments, the nutrients were more concentrated in slabs than in the feeding NS, except for TAN. Only in 2017, Mg and pH were significantly higher in the AP slabs.
treatment, it was remarkably constant and low (i.e. range of 0.2 to 0.4%) over the years in the AP treatment. Although in each year, the incidence of BER was lowered in the AP treatment, the difference between both treatments was significant in 2016 and 2017. Combined ANOVA could not detect any significant effect of the NS type because the mean square value of the interaction (years x NS type), used to calculate the F value, was relatively large to the mean square value of NS type. For the number of fruits produced and for the tomato fruit diameter, no significant difference was found between both treatments) (results not shown). The fruit diameter was remarkably constant over the years with an overall average of 67 ± 3 mm. At some point during the production seasons, some wilting at the top of the tomato stems and inferior weekly growth was observed in the AP treatment. This was always consistent with the sodium peaks in the AP slabs, and was reflected in a lower total stem length for AP (average final stem size over 3 years being 868.6 cm) than for HP (average final stem size of 878.64 cm), although the difference was not significant.
4. Discussion 4.1. Tomato production In our experimental design, the AP treatment differed from the HP only by its water origin. We aimed to have a similar feeding regime in both treatments (i.e. equivalent nutrient supply and pH in the respective feeding solutions). This goal was achieved, as no significant pH, macro- and micronutrient concentration differences between the AP and the HP treatment were found in the feeding NS. The only detected difference was the higher concentration of Na+ and Cl− for the AP treatment. Consequently, a significantly higher EC (+1.2 dS/m in 2016, and +1.3 dS/m in 2017) was detected in the AP than in the HP slabs (Table 2 and Fig. 4). Indeed, Na and Cl were present in substantial concentrations in the pikeperch water. The reason was that NaCl salt was directly added in the RAS water to prevent fish health issues due to stress occurring at fish grading. Frequent fish grading was done for research purposes and NaCl was applied directly after grading at concentrations of up to 34 mmol/L. Cl concentrations in slabs were always lower than Na ones with an approximately constant value, giving some evidence for plant uptake to be the cause. After correction for the difference between Cl and Na concentrations already present in the feeding NS, the remaining difference caused by plant uptake was 4.08 mmol/L for AP, and 3.29 mmol/L for HP. While high Cl and Na contents can induce salt stress, high Na contents can induce a supplemental deleterious effect due to the antagonism with K and Ca uptake. Indeed, during two short periods in 2016 and 2017, a reduced plant growth was noticed. To prevent further growth reduction, the drain water was discharged. It is commonly admitted that plant growth and yield are adversely influenced by salinity stress (Cuartero et al., 1999; Kanayama and Kochetov, 2015; Soria and Cuartero, 1998; Zhai et al., 2015) or by high root zone concentrations of Na (Cuartero and Fernández-Muñoz, 1998).
3.2. Water quality The pH and macro- and micronutrient concentrations in the AP feeding NS were maintained close to the targeted HP concentrations and on the average over all growing periods no significant differences were found between both treatments (Table 1). Only a difference in Na and Cl was observed, with on average 2.90 times more Na and 5.97 times more Cl in the AP. Na concentration in AP feeding NS variated from 1.31 to 11.84 mmol/L with an average of 4.32 mmol/L. In the HP feeding solution Na concentration (?) variated only from 0.87 to 2.23 mmol/L, with an average of 1.49 mmol/L. Cl concentrations approximately showed the same variability. The higher Na and Cl contents in the AP feeding solution resulted in the AP slabs in 2016 and 2017 in persistently higher concentrations of these elements and a significantly higher EC. Fig. 4 shows EC and measured Na contents. Some high peaks of Na (e.g. up to 35 mmol/L) were observed in the AP slabs, especially in 2016 and 2017. Because of these peaks, the AP drain water was flushed and the slabs were rinsed on the 28th of April and 25th of July in 2016 and on the 26th of April and 24th of September in 2017. On average, Na content in AP slabs was 11.48 ± 7.32 mmol/L. Average Na concentration in HP slabs was much lower (4.44 ± 1.71 mmol/L), but was quite constant over the growing period. Cl concentrations in the slabs showed the same variability as Na concentrations – high for AP and low for HP – and 5
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Fig. 4. Na+ concentrations and EC in the hydroponic (HP) and aquaponic (AP) slabs for each year studied.
tomato fruit yields and fruit number were not significantly different between the AP and the HP treatment. Slightly more marketable fruits were recorded in the AP treatment in 2015 and 2017 but this yield increase was not significant. This slight yield difference is presumably linked to the incidence of BER that was always lower (significantly lower in 2016 and 2017) and remarkably constant through the seasons and years (i.e. < 0.4%) in the AP treatment (Fig. 3). We only found two experiments comparing aquaponic tomato
In addition, the stress induced by salinity is known to increase BER symptoms and so to further reduce the marketable yields (Kanayama and Kochetov, 2015; Zhai et al., 2015). Consequently, because of the higher average EC, a lower fruit yield would have been expected in the AP treatment for both 2016 and 2017. Some EC peaks even were higher than 9 dS/m in the AP slabs. Although a slightly weekly lower yield has been observed after these peaks (result not shown), no significant reduction of the total yearly production occurred. Total stem length, total 6
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Table 2 Average nutrient concentrations in the hydroponic (HP) and aquaponic (AP) slabs. 2015 (n = 6)
EC (dS/m) pH TAN K Ca Mg NO3 SO4 PO4 Cl Fe Mn Zn B Cu
mmol/L
μmol/L
2016 (n = 11)
2017 (n = 14)
AP
HP
AP
HP
AP
HP
4362 ± 383 6.46 ± 0.71 0.19 ± 0.40 10.02 ± 4.13 8.32 ± 0.94 5.08 ± 0.64 21.25 ± 5.65 8.31 ± 1.74 1.58 ± 0.59 6.19 ± 8.15a 77.38 ± 52.99 8.32 ± 3.26 7.17 ± 3.54 76.29 ± 12.83 1.45 ± 0.67
4577 ± 662 6.05 ± 0.73 0.03 ± 0.03 10.37 ± 3.51 11.48 ± 2.47 5.79 ± 1.18 24.62 ± 5.44 9.60 ± 2.20 1.74 ± 0.69 0.18 ± 0.16b 102.72 ± 107.36 11.28 ± 5.70 6.32 ± 3.91 92.02 ± 25.25 1.73 ± 0.87
6806 ± 1590a 6.48 ± 0.81 0.20 ± 0.36 14.53 ± 5.78 14.48 ± 2.83 6.86 ± 1.62 36.72 ± 6.85 13.16 ± 3.38 1.68 ± 1.16 8.72 ± 6.98a 38.36 ± 21.71 5.51 ± 2.76a 10.33 ± 5.40 120.93 ± 53.57 1.40 ± 1.13
5539 ± 635b 6.08 ± 0.94 0.18 ± 0.21 14.04 ± 4.76 13.72 ± 3.94 6.87 ± 1.71 34.64 ± 5.98 11.95 ± 3.05 2.05 ± 1.16 0.19 ± 0.13b 51.06 ± 31.40 14.65 ± 9.67b 13.41 ± 7.62 115.65 ± 54.51 1.95 ± 1.63
6963 ± 1957a 6.28 ± 0.63a 0.12 ± 0.20 15.96 ± 5.76 14.47 ± 4.82 7.66 ± 2.99a 36.31 ± 13.08 13.62 ± 5.68 2.29 ± 1.48 7.49 ± 9.07a 75.51 ± 26.39 8.42 ± 10.20a 12.98 ± 5.62 161.51 ± 63.27 2.88 ± 1.25
5593 ± 1328b 5.58 ± 0.58b 0.22 ± 0.26 17.08 ± 6.31 12.03 ± 5.09 6.02 ± 3.07b 35.31 ± 9.63 10.14 ± 5.32 3.03 ± 1.67 0.18 ± 0.11b 80.51 ± 41 14.76 ± 12.32b 16.21 ± 6.41 140.31 ± 53.58 2.76 ± 1.23
*Yearly average concentration ± standard deviation, n is the number of measurements. The concentrations were compared using the Duncan test and significant differences between treatments are indicated in bold and by different small letters (p < 0.05). TAN = total ammoniacal nitrogen.
humic acid-like organic molecules (Hambly et al., 2015). Microorganisms and/or DOM may have acted as tomato plant biostimulants (du Jardin, 2015), providing possibilities to overcome the salinity stress and keep productivity as high, and sometimes higher, than in the HP treatment. At the end of each cultivation period, slightly more roots were observed on the side of the AP slabs, however for technical reasons it was not possible to weigh or score it. Such increase of root development is in accordance with the observations of Delaide et al. (2016a, 2016b) for lettuce in complemented RAS water. Indeed, microorganisms settled in the rhizosphere can beneficially interact with the plants (Bartelme et al., 2018) and promote root development (Amin et al., 2015; Wienhausen et al., 2017). Further experiments with a close monitoring of the root mass, plant biostimulating microorganisms and DOM presence are needed to confirm our assumptions.
production to a hydroponic control. Suhl et al. (2016) compared tomato production in NFT with complemented RAS water solution to that in hydroponic solution and also obtained similar yields in both treatments and lower BER in the complemented RAS water treatment. Crappé et al. (2017) compared complemented RAS water to hydroponics with drip irrigation and obtained similar yields. BER incidence was higher for the complemented RAS water treatment, but this was due to an excess of K, leading to an unfavourable K/Ca ratio. However, these studies were based only on one season of production, without succeeding to have similar (i.e. without significant differences) macro- and micronutrient concentrations in the feeding solutions of both treatments, making the interpretation of tomato production and BER symptoms, in our opinion, not sufficiently trustable. Regarding the statistical analysis, the experimental setup of 4 replicates studied for 3 years gave only 2 degrees of freedom for the interaction, years x treatment, against which the effect of the treatments was tested. This is quite low from a statistical point of view, but increasing this number of degrees of freedom for such large-scale semipractice experiment would require still more years of experiment, or a higher number of treatments. While the first solution was out of question, a higher number of treatments would have been at the expense of the semi-practice scale of the treatment. A few studies have reported higher yields (i.e. in vegetative mass) in complemented RAS water compared to hydroponic control for leafy vegetables as lettuce (Delaide et al., 2016b; Goddek and Vermeulen, 2018) and basil (Saha et al., 2016). For tomatoes however, no significant increase in tomato vegetative mass has yet been reported in literature. It was also not measured in our study, butit is important to notice that during tomato cultivation, the plants were continuously pruned to keep only two stems. Old leaves and suckers were thus continuously removed, and this biomass has not been quantified. As the observed increase of salinity and Na content in the AP treatment were supposed to reduce the plant production and increase BER symptoms, an important question is what can explain the absence of stress and this apparent resistance to salinity. The only possible answer is that RAS wastewater used in the AP treatment should contain factors that were not present in the HP water. Indeed, RAS water is charged with a variety of microorganisms (bacteria, fungi, protozoa, etc.) (Rurangwa and Verdegem, 2015; Schmautz et al., 2017; Schreier et al., 2010) and dissolved organic molecules (DOM). The latter are released by physicochemical degradation of the fish feed and the fish excretions, or by microorganisms (e.g. organic molecule alteration, triggering molecules for quorum sensing, etc.). Hence, a broad variety of DOM can be present as peptides, amino-acids, phytohormones-like,
4.2. Blossom-end rot and Mn Interestingly, Mn had a significant difference in concentration between treatments in the slabs. No technical intervention (i.e. unlike for Cl) could explain this difference. Mn was always lower in the AP slabs and this was repeated through the years (Table 2). On average, Mn was 1.9 times less concentrated in the AP than in the HP slabs. Compared to the feeding solution, Mn was slightly more concentrated in the HP slabs but 1.7 times less concentrated in the AP slabs. No significant differences were found between both treatments for the concentration of Mn in the feeding NS nor for the pH in the slabs, thus excluding the possibility of Mn loss by switching to an insoluble form (e.g. precipitation). As such, the lower concentration of Mn in the AP slabs indicates that AP tomato plants assimilated more Mn than the HP ones. This higher Mn assimilation then should be due to microorganisms that colonized the rhizosphere and improved the nutrient use efficiency (Meena et al., 2017) or increased the root mass. Silber et al. (2009) and Aktas et al. (2005) demonstrated that higher Mn content in fruit was correlated to reduced BER symptoms, and as we observed reduced BER and high Mn uptake, we suspect the tomato plants to have had a higher Mn content in their fruits. Unfortunately, in our study the Mn content in tomato leaves and fruits was not quantified. This should be achieved in further research to verify our assumption. Finally, as some authors claimed the low Ca concentration in the fruit tip, accompanying BER, to be a consequence of a metabolic disorder, related with an increase of reactive oxygen species (De Freitas et al., 2011; Saure, 2014), it is possible that microorganisms and/or DOM have interacted with the tomato plant metabolism and promoted 7
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resistance against BER via other ways than by only enhancing Mn uptake (Canellas et al., 2015; Mangmang et al., 2015).
A., 2015. Humic and fulvic acids as biostimulants in horticulture. Sci. Hortic. (Amsterdam) 196, 15–27. https://doi.org/10.1016/j.scienta.2015.09.013. Crappé, S., Buysens, S., Gobin, B., 2017. Vergelijkende studie: teelt van tomaat in een hydroponic en aquaponic teeltsysteem. Kruishoutem. Cuartero, Â., Ferna, R., Experimental, Â., Mayora, L., 1999. Tomato and salinity. Sci. Hortic. (Amsterdam) 78, 83–125. Cuartero, J., Fernández-Muñoz, R., 1998. Tomato and salinity. Sci. Hortic. (Amsterdam) 78 (1-4), 83–125. https://doi.org/10.1016/S0304-4238(98)00191-5. De Freitas, S.T., Shackel, K.A., Mitcham, E.J., 2011. Abscisic acid triggers whole-plant and fruit-specific mechanisms to increase fruit calcium uptake and prevent blossom end rot development in tomato fruit. J. Exp. Bot. 62 (8), 2645–2656. https://doi.org/10. 1093/jxb/erq430. Delaide, B., Delhaye, G., Dermience, M., Gott, J., Soyeurt, H., Jijakli, M.H., 2017. Plant and fish production performance, nutrient mass balances, energy and water use of the PAFF Box, a small-scale aquaponic system. Aquac. Eng. 78, 130–139. https://doi.org/ 10.1016/j.aquaeng.2017.06.002. Delaide, B., Goddek, S., Gott, J., Soyeurt, H., Jijakli, M.H., 2016a. Lettuce (Lactuca sativa L. var. Sucrine) growth performance in complemented aquaponic solution outperforms hydroponics. Water (Switzerland) 8. https://doi.org/10.3390/w8100467. Delaide, B., Goddek, S., Gott, J., Soyeurt, H., Jijakli, M.H., 2016b. Lettuce (Lactuca sativa L. var. Sucrine) growth performance in complemented aquaponic solution outperforms hydroponics. Water (Switzerland) 8. https://doi.org/10.3390/w8100467. Delaide, B., Goddek, S., Mankasingh, U., Ragnarsdottir, K.V., Jijakli, H., Thorarinsdottir, R., 2015. Challenges of sustainable and commercial aquaponics. Sustainability 7, 4199–4224. https://doi.org/10.3390/su7044199. du Jardin, P., 2015. Plant biostimulants: definition, concept, main categories and regulation. Sci. Hortic. (Amsterdam) 196, 3–14. https://doi.org/10.1016/j.scienta.2015. 09.021. Goddek, S., Espinal, C.A., Delaide, B., Jijakli, M.H., Schmautz, Z., Wuertz, S., Keesman, K.J., 2016. Navigating towards decoupled aquaponic systems: a system dynamics design approach. Water (Switzerland) 8. https://doi.org/10.3390/W8070303. Goddek, S., Vermeulen, T., 2018. Comparison of Lactuca sativa growth performance in conventional and RAS-based hydroponic systems. Aquac. Int. 26 (6), 1377–1386. https://doi.org/10.1007/s10499-018-0293-8. Hambly, A.C., Arvin, E., Pedersen, L.-F., Pedersen, P.B., Seredyńska-Sobecka, B., Stedmon, C.A., 2015. Characterising organic matter in recirculating aquaculture systems with fluorescence EEM spectroscopy. Water Res. 83, 112–120. https://doi. org/10.1016/j.watres.2015.06.037. Heuvelink, E., 2005. Tomatoes, Crop Production Science in Horticulture Series. Kanayama, Y., Kochetov, A., 2015. Abiotic Stress Biology in Horticultural Plants. Abiotic Stress Biology in Horticultural Plants.https://doi.org/10.1007/978-4-431-55251-2. Klinger, D., Naylor, R., 2012. Searching for Solutions in Aquaculture: Charting A Sustainable Course. https://doi.org/10.1146/annurev-environ-021111-161531. Love, D.C., Fry, J.P., Li, X., Hill, E.S., Genello, L., Semmens, K.J., Thompson, R.E., Johnson, G.E., Buzby, K.M., Semmens, K.J., Holaskova, I., Waterland, N.L., Cerozi, B., da, S., Fitzsimmons, K., America, A., Ayre, J.M., Moheimani, N.R., Borowitzka, M.A., Love, D.C., Fry, J.P., Genello, L., Hill, E.S., Frederick, J.A., Li, X., Semmens, K.J., 2015a. An international survey of aquaponics practitioners. PLoS One 9, e102662. https://doi.org/10.1371/journal.pone.0102662. Love, D.C., Uhl, M.S., Genello, L., 2015b. Energy and water use of a small-scale raft aquaponics system in Baltimore, Maryland, United States. J. Aquac. Eng. Fish. Res. 68, 19–27. https://doi.org/10.1016/j.aquaeng.2015.07.003. Mangmang, J.S., Deaker, R., Rogers, G., 2015. Response of cucumber seedlings fertilized with fish effluent to Azospirillum brasilense. Int. J. Veg. Sci. 5260, 150409121518007. https://doi.org/10.1080/19315260.2014.967433. Martins, C.I.M., Eding, E.H., Verdegem, M.C.J., Heinsbroek, L.T.N., Schneider, O., Blancheton, J.P., d’Orbcastel, E.R., Verreth, J.A.J., 2010. New developments in recirculating aquaculture systems in Europe: a perspective on environmental sustainability. J. Aquac. Eng. Fish. Res. 43, 83–93. https://doi.org/10.1016/j.aquaeng.2010. 09.002. Meena, V.S., Meena, S.K., Verma, J.P., Kumar, A., Aeron, A., Mishra, P.K., Bisht, J.K., Pattanayak, A., Naveed, M., Dotaniya, M.L., 2017. Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review. Ecol. Eng. 107, 8–32. https://doi.org/10.1016/j.ecoleng.2017.06.058. Pulvenis, J.-F., 2016. Fisheries and Aquaculture Topics. The State of World Fisheries and Aquaculture (SOFIA). Topics Fact Sheets. Fisheries and Aquaculture Department, Rome. Rakocy, J.E., 2012. Aquaponics-Integrating Fish and Plant Culture. Wiley-Blackwell, pp. 344–386. https://doi.org/10.1002/9781118250105.ch14. Rakocy, J.E., Bailey, D.S., Shultz, R.C., Thoman, E.S., 2004. Update on tilapia and vegetable production in the UVI aquaponic system. New dimensions on farmed tilapia. Proceedings from the 6th International Symposium on Tilapia in Aquaculture 1–15. Rurangwa, E., Verdegem, M.C.J., 2015. Microorganisms in recirculating aquaculture systems and their management. Rev. Aquacult. 7, 117–130. https://doi.org/10.1111/ raq.12057. Saha, S., Monroe, A., Day, M.R., 2016. Growth, yield, plant quality and nutrition of basil (Ocimum basilicum L.) under soilless agricultural systems. Ann. Agric. Sci. 61, 181–186. https://doi.org/10.1016/j.aoas.2016.10.001. Saure, M.C., 2014. Why calcium deficiency is not the cause of blossom-end rot in tomato and pepper fruit – a reappraisal. Sci. Hortic. (Amsterdam) 174 (1), 151–154. https:// doi.org/10.1016/j.scienta.2014.05.020. Schmautz, Z., Graber, A., Jaenicke, S., Goesmann, A., Junge, R., Smits, T.H.M., 2017. Microbial diversity in different compartments of an aquaponics system. Arch. Microbiol. Manuscript. https://doi.org/10.1007/s00203-016-1334-1. 0. Schreier, H.J., Mirzoyan, N., Saito, K., 2010. Microbial diversity of biological filters in recirculating aquaculture systems. Curr. Opin. Biotechnol. 21, 318–325. https://doi.
5. Conclusion In our study, we compared the production of tomatoes grown in a NS based on complemented RAS wastewater to tomatoes grown in conventional hydroponic NS. We especially achieved, for the first time, to accurately complement RAS water with macro- and micronutrient concentrations equivalent (i.e. no significant difference observed) to the hydroponic NS and this during 3 seasons of production. Our results clearly indicate the suitability of complemented pikeperch RAS wastewater as feeding water for professional HP tomato production using drip irrigation as similar growth and yields were obtained in AP and HP treatments. While a significant higher EC was recorded in the AP treatment, due to intermittent NaCl addition in the RAS water, the tomato yields did not diminish. Interestingly, symptoms of BER were even reduced in this treatment. As RAS water contains a diversity of microorganisms (e.g. bacteria, fungi, protozoa, etc.) and DOM (e.g. amino acid-like, phytohormones-like, humic acid-like organic molecules, etc.), it is presumed that some of these beneficially interacted with the plant metabolism (e.g. by promoting the root growth) and mitigated the salinity stress and the BER symptoms. This study delivered also much evidence that this was achieved by the promotion of Mn uptake which has been reported as a BER reducing factor. Further experiments with a close monitoring of the root mass, the nutrient content in leaves and fruits, especially Mn, would be needed to confirm our assumptions. The simultaneous identification and count of microorganisms present in the plant root zone using advanced technology such as flow cytometry and metagenomic techniques should be envisaged. Methods to identify plant promoting DOMs should also be applied. Funding This research was done in the frame of the INAPRO project funded by the European Union’s Seventh Framework Programme for research, technological development and demonstration under grant agreement number 619137. This research was also partly funded by the European Regional Development Fund via Aquavlan2 (Interreg V program Flanders - The Netherlands). Declaration of Competing Interest None. Acknowledgements The authors would like to acknowledge the European Commission via INAPRO and AquAVlan² for funding support. The authors also thank Ronny Versyck, Roger Houthoofd, Sofie Verhelst and Laurens Buyse for taking care of the experiment and the Inagro lab staff for the water quality analysis. References Aktas, H., Karni, L., Chang, D.C., Turhan, E., Bar-Tal, A., Aloni, B., 2005. The suppression of salinity-associated oxygen radicals production, in pepper (Capsicum annuum) fruit, by manganese, zinc and calcium in relation to its sensitivity to blossom-end rot. Physiol. Plant. 123, 67–74. https://doi.org/10.1111/j.1399-3054.2004.00435.x. Amin, S.A., Hmelo, L.R., van Tol, H.M., Durham, B.P., Carlson, L.T., Heal, K.R., Morales, R.L., Berthiaume, C.T., Parker, M.S., Djunaedi, B., Ingalls, A.E., Parsek, M.R., Moran, M.A., Armbrust, E.V., 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98. Bartelme, R.P., Oyserman, B.O., Blom, J.E., Sepulveda-Villet, O.J., Newton, R.J., 2018. Stripping away the soil: plant growth promoting microbiology opportunities in aquaponics. Front. Microbiol. 9. https://doi.org/10.3389/fmicb.2018.00008. Canellas, L.P., Olivares, F.L., Aguiar, N.O., Jones, D.L., Nebbioso, A., Mazzei, P., Piccolo,
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1016/j.agwat.2016.10.013. Turcios, A., Papenbrock, J., 2014. Sustainable treatment of aquaculture effluents—what can we learn from the past for the future? Sustainability 6, 836–856. https://doi.org/ 10.3390/su6020836. Vermeulen, T., Kamstra, A., 2013. The Need for Systems Design for Robust Aquaponic Systems in the Urban Environment. Wienhausen, G., Noriega-ortega, B.E., Niggemann, J., Dittmar, T., 2017. The exometabolome of two model strains of the Roseobacter group : a marketplace of microbial metabolites. Front. Microbiol. 8, 1–15. https://doi.org/10.3389/fmicb.2017.01985. Zhai, Y., Yang, Q., Hou, M., 2015. The effects of saline water drip irrigation on tomato yield, quality, and blossom-end rot incidence: a case study in the South of China. PLoS One 10, 1–17. https://doi.org/10.1371/journal.pone.0142204.
org/10.1016/j.copbio.2010.03.011. Silber, A., Bar-Tal, A., Levkovitch, I., Bruner, M., Yehezkel, H., Shmuel, D., Cohen, S., Matan, E., Karni, L., Aktas, H., Turhan, E., Aloni, B., 2009. Manganese nutrition of pepper (Capsicum annuum L.): Growth, Mn uptake and fruit disorder incidence. Sci. Hortic. (Amsterdam) 123, 197–203. https://doi.org/10.1016/J.SCIENTA.2009.08. 005. Soria, T., Cuartero, J., 1998. Tomato fruit yield and water consumption with salty water irrigation. Acta Hortic. 458, 215–219. https://doi.org/10.17660/ActaHortic.1998. 458.25. Suhl, J., Dannehl, D., Kloas, W., Baganz, D., Jobs, S., Scheibe, G., Schmidt, U., 2016. Advanced aquaponics: evaluation of intensive tomato production in aquaponics vs. conventional hydroponics. Agric. Water Manag. 178, 335–344. https://doi.org/10.
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Effect of wastewater from a pikeperch (Sander lucioperca L.) recirculated aquaculture system on hydroponic tomato production and quality
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Boris Delaide , Stefan Teerlinck, An Decombel, Peter Bleyaert INAGRO, Ieperseweg 87, Rumbeke-Beitem, B-8800, Belgium
A R T I C LE I N FO
A B S T R A C T
Keywords: Aquaponics Hydroponics RAS Greenhouse Manganese Blossom-end rot
Decoupled aquaponic systems (DAPS) use the wastewater of recirculated aquaculture systems (RAS) as water source for plant production in recirculated hydroponic systems. RAS wastewater is complemented with macroand micronutrients to obtain equivalent concentrations and pH as in standard hydroponic nutrient solutions (NS). Unlike in single recirculating aquaponic systems, optimal growth conditions can be established in each production part of a DAPS (i.e. fish and plant parts) avoiding compromises. DAPS design seems more adapted for commercial farming operations but feasibility studies on large-scale systems are lacking. Therefore, the production of tomatoes (Solanum lycopersicum L., cv. Foundation) grown in a NS based on complemented pikeperch RAS wastewater (i.e. AP treatment) has been compared to that of tomatoes grown in conventional hydroponic NS (i.e. HP treatment), in semi-practice conditions. During 3 consecutive years, tomatoes were grown on rockwool slabs, in a large-scale Venlo-type climate-controlled greenhouse, using a recirculated drip irrigation system identical to the ones used by the professionals of the hydroponic tomato sector. While the electroconductivity was significantly higher in the AP treatment due to the presence of NaCl in the RAS wastewater, no significant differences for the total and marketable fruit yields, fruit number, and size were found between the AP and HP treatments. However, while the level of blossom-end rot (BER) varied substantially (0.9–18.6 %) in the HP treatment, it was remarkably constant and low (0.2-0.4%) over the years in the AP treatment, suggesting a beneficial effect of RAS wastewater. Our results clearly indicate the suitability of complemented pikeperch RAS wastewater as feeding water for professional HP tomato production using drip irrigation for DAPS. As RAS water contains a diversity of microorganisms and dissolved organic matter, it is assumed that some of these acted as plant biostimulants and mitigated the salinity stress and the BER symptoms.
1. Introduction To balance the fish demand of a growing population while respecting the fishing quotas, the aquaculture sector has seen a rapid expansion in these last 30 years (Pulvenis, 2016). Lately, recirculating aquaculture systems (RAS) have been developed, allowing to drastically reduce the water consumption per kilo of fish produced (e.g. less than 100 L in RAS while several thousands of litre in conventional systems) (Martins et al., 2010). Integrating aquaculture with other food production methods is under development in order to reuse the aquaculture wastes (Klinger and Naylor, 2012; Turcios and Papenbrock, 2014) and to close the nutrient cycle. The potential for more efficient use of resources through the tightening of nutrient cycles and reuse of aquaculture wastewater may explain the increasing interest in aquaponics (AP) (Love et al., 2015a). The AP concept is to combine RAS and recirculated hydroponic systems (RHS) for fish and horticultural plant
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production. The integration of RAS and RHS aims to reuse the aquaculture wastewater for irrigating the crops while converting the otherwise wasted nutrients excreted by fish into valuable plant biomass. Hence, the reuse of fish wastewater could significantly reduce the environmental impact of aquaculture and hydroponic plant production. The most common design of the AP system is the integration of hydroponic beds into the water loop of a RAS (Delaide et al., 2015; Rakocy, 2012) and may be called single recirculating aquaponic system (SRAP) (Suhl et al., 2016). SRAP can be complex to manage as three different biological systems (fish, plants and microorganisms) are merged in a single water loop. Decoupled aquaponic systems (DAPS) (Goddek et al., 2016) or double recirculating aquaponic systems (DRAPS) (Suhl et al., 2016) present an alternative design to overcome the disadvantages of SRAP. In these decoupled systems, the RAS wastewater goes to the hydroponic part (i.e. the RHS part) and does not return to the fish. The water would
Corresponding author at: INAGRO, Ieperseweg 87, Rumbeke-Beitem, B-8800, Belgium. E-mail addresses: [email protected] (B. Delaide), [email protected] (P. Bleyaert).
https://doi.org/10.1016/j.agwat.2019.105814 Received 16 November 2018; Received in revised form 13 September 2019; Accepted 20 September 2019 0378-3774/ © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
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by a conventional standard hydroponic NS. The drain water of each treatment was collected separately in a 1 m³ drain water storage tank. Intermittently, their entire content was sand filtrated, and UV disinfected. The disinfected drain waters were stored in their corresponding disinfected drain water storage tank (Fig. 1). The filtration event only happened when a disinfected drain water storage tank became empty. The same sand filtration and UV disinfection device was used for AP and HP drain waters, but the system automatically cleaned and flushed the filter and pipes with the new incoming solution before each use. The disinfected drain solution was thus reused into its respective fertigation loop each time a batch of new feeding solution was made (i.e. from once per week to once per day depending on daylight duration and intensity). The tomato plants were cultivated in a compartment of a Venlo-type climate-controlled greenhouse of 352 m². The greenhouse had a column height of 4 m, covered with 4 mm glass and warmed by a conventional floor level pipe heating system. The experiment was conducted during 3 consecutive seasons of tomato production, from 06.01.2015 to 07.11.2017. The cultivar Foundation (Bayer-Nunhems, Haelen, The Nederlands) was used in 2015, 2016 and 2017. In 2017, the cultivars Axxy (Axia, Naaldwijk, The Netherlands) and Merlice (De Ruiter, Bergschenhoek, The Netherlands) were tested also. The cultivars were all grafted on rootstock Maxifort (De Ruiter, Bergschenhoek, The Netherlands) in 2015 and on DR 0141TX (De Ruiter, Bergschenhoek, The Netherlands) in 2016 and 2017.
then leave the hydroponic part only by evaporation (almost negligible) and plant transpiration. Optimal growing conditions can then be established in each production part (i.e. in RAS and RHS parts) avoiding compromises. In the hydroponic part, the RAS wastewater is complemented with macro- and micronutrients to obtain equivalent concentrations, pH and EC as in the standard RHS nutrient solutions (Goddek et al., 2016). With this design the production and some sanitary aspects (e.g. cleaning, quarantine, etc.) can be more easily controlled making the system more adapted for commercial farming operations (Vermeulen and Kamstra, 2013). Also, the existing professional techniques can be easily used in the respective fish and plant parts without high technological innovations. Just a few AP designs have been tested and only in lab conditions or small scale (Delaide et al., 2017; Love et al., 2015b; Suhl et al., 2016), but studies on large-scale systems remain scarce (Rakocy et al., 2004), especially with DAPS. Moreover, comparisons of production in AP and hydroponics under the same conditions as with the techniques used in professional operations are lacking. Despite a few pioneer publications (Delaide et al., 2016a; Saha et al., 2016), the effects of fish water on the yields and quality of the plant products remain unknown, which hinders the adoption of AP by professionals of the horticultural sector. The feasibility of properly complementing the fish water with conventional commercial fertilisers needs to be investigated. Therefore, this study aimed to compare the tomato production of a decoupled aquaponic system to a conventional recirculated hydroponic system in a semi-practice scale. Special attention was given to plant health and physiological disorders as blossom-end rot (BER). The macro and micronutrient content in the nutrient solutions was closely monitored with a specific regard to sodium and chloride levels. It is the first time a reliable comparison of tomato production in complemented RAS wastewater has been achieved and repeated for 3 years.
2.2. Tomato growing conditions An average temperature (T) of 18.0 °C was targeted in the greenhouse. The set-points of the heating system were defined as 20.0 °C and 15.5 °C for day and night, respectively and the ventilation was opened at 22 °C to cool the greenhouse. From mid-May until September, the ventilation was opened at 19 °C. To control the greenhouse climate and irrigation, a computed integrated management software was used (PRIVA Connect, De Lier, The Netherlands). The outside light intensity was measured with a PAR sensor (PRIVA, De Lier, The Netherlands) and a total irradiation sum of 4280.5, 3970.9 and 4011.8 MJ/m² was measured from planting until the last harvest in 2015, 2016, and 2017, respectively. For the experiment in 2015 and 2016, a net surface of 329 m² housed 909 tomato stems (i.e.180 m² for 498 stems and 149 m² for 411 stems, for the HP and AP treatments, respectively). For 2017, a net surface of 658 m² spread over two greenhouse compartments, housed 1818 tomato stems. There were 2 stems per tomato plant and they were topped in early September, each year. The hydroponic cultivation method was the drip irrigation method as described in Heuvelink (2005). The substrate used was rockwool, with slabs of 1 × 0.20 x 0.075 m (Grodan Vital, Roermond, The Netherlands). The slabs were renewed every year. Two plants were set per slab and one dripper was stuck close to the foot of each plant. The slabs were placed on drainage gutters (Meteor Systems BV., Breda, The Netherlands) allowing to recover the drain water for reuse. The space in between plants on the gutters was 0.55 m with 0.80 m distance between gutters, giving a plant density of 2.27 stems per square meter. For both treatments, the pH target of the NS was 5.6. The irrigation pace of the NS was regulated in function of the daily radiation by the computer climate software (PRIVA, De Lier, The Netherlands) aiming a drain water quantity comprised in a range of 20–40 % of the inflow. For each season, studied tomatoes were sown in November and inserted in the drip irrigation system upon the rockwool slabs in January, when the first truss was visible. The fruits were harvested from March to November. The plant pruning, harvesting and support were conducted as in normal tomato greenhouse professional operation as described by Heuvelink (2005).
2. Material and methods 2.1. Experimental setup and operation The experiments were carried out in the facilities of the Inagro research institute located in Rumbeke-Beitem, Belgium (50°54′06.2″N, 3°07′28.0″E). The experimental setup was a semi-practice combination of tomato (Solanum lycopersicum L., cv. Foundation) and pikeperch (Sander lucioperca L.) production. It aimed to combine the techniques already used by professional farmers in Flanders (Belgium). Part of the fish wastewater that otherwise would be flushed to the sewage was used for irrigating the tomatoes. The pikeperch were reared in an indoor recirculating aquaculture system (RAS) operated as a professional farm. The facility had a surface of 700 m² for a total water volume of 160 m³. The RAS had an average fish load of 15 kg/m³ and was able to produce 2000–4000 kg of pikeperch per year. The fish were fed with a fish protein-based meal containing 56% protein and 16% fat (Skretting, Fontaine les Vervins, France). The average daily water exchange rate of 15% was relatively high because the system was conducted in such a way that the water discharged to the sewage had a NO3 content lower than 2.42 mmol/L in order to meet the wastewater disposal regional regulations. The wastewater delivered by the drum filters was decanted and the supernatant was stored in a 15 m³ tank prior to be discharged in the sewage. At regular intervals, part of this water was pumped to the tomato greenhouse facility. This water was then filtrated with a TAF filter (TAF 750, Amiad water system, Chargè, France) and complemented in macro- and micronutrients to reach the standard hydroponic concentrations. The so prepared nutrient solution (NS) was stored in a feeding sump tank of 0.4 m³ (Fig. 1). The water from this sump was used to irrigate the tomato plants and this treatment was called the aquaponic (AP) treatment. The tomato production in the AP treatment was compared to a standard hydroponic (HP) treatment in which the plants were irrigated 2
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Fig. 1. Experimental setup. The wastewater coming from the RAS was pumped to the fish water storage tank. It was filtrated (T) and complemented (N) for tomato drip irrigation (feeding water). The tomato production of plants irrigated with the RAS wastewater (i.e. AP treatment) was compared to that of others irrigated by conventional standard hydroponic solution formulated with a mixture of rainwater and tap water and commercial fertilisers (i.e. HP treatment). The irrigation drain waters were reinserted into their respective fertigation loop, after passing intermittently through a sand filter (S) and a UV-disinfection unit (UV). Both sand filter and UV unit were cleaned automatically before each filtration-disinfection event in order to avoid cross contamination of the respective solutions.
Phosphorus, Potassium, Calcium, Magnesium, and Sulphates), micronutrients (i.e. Iron, Boron, Copper, Zinc, and Manganese), chlorides, sodium and alkalinity was monitored in the slabs and in the drain water once every two weeks for both treatments. The feeding NS were controlled once per month. Every time a new batch of water was pumped from the RAS (i.e. supernatant from the drum filter wastewater) to the fish water storage tank, a new sample was taken for analysis prior to the calculation of the salt complementation. The water samples were brought to the lab for proceeding analysis immediately after the sampling. The concentrations of the nitrogen compounds were determined with a continuous flow analyser (SFA type 4000, Skalar Analytical B.V., Breda, The Netherlands). Total ammoniacal nitrogen (TAN) was determined by the reaction with salicylate, nitroprusside and dichlororisocyanurate reagents in a buffer solution. The nitrite (NO2) was determined with the sulphanilamide and N-(1-naphthyl)ethylenediamine dihydrochloride reagents. Separately, the nitrite plus nitrate (NO2−+NO3−) were reduced in NO2− with the cadmium reduction method and determined with the precited reagents. The NO3- was calculated by subtracting the NO2− concentration determined with the first described method from the concentration obtained with the cadmium reduction method. Concentrations of P ions (H2PO4−, HPO42-, PO43-), K ion (K+), Mg ion (Mg2+), Ca ion (Ca2+), Fe ions (Fe3+, Fe2+), Cu ions (Cu2+, Cu+), Mn ion (Mn2+), Zn ion (Zn2+), B oxides (BO32−, B4O72−), and Na ion (Na+) were determined by inductively coupled plasma-optical emission spectroscopy (optima 8300, PerkinElmer, Zaventem, Belgium). Chloride (Cl−) and sulphate (SO42-) were determined by liquid chromatography (850 Professional IC anion, Metrohm, Antwerpen, Belgium) with a 150 mm column (Metrosep A SUPP 5-150/4.0, Metrohm, Antwerpen, Belgium), following the ISO 10304-1:2007 method. Alkalinity was determined by titration following the ISO 99631:1994 method.
2.3. Determination of tomato production Four randomized plots, comprising ten tomato stems each, were defined per treatment area in the greenhouse. The production of the tomatoes from these plots was followed. This gave an experimental setup of four replicates for each season of production. The plots were located around the centre of the greenhouse to prevent border effects and to assure all plants were studied under the same temperature and lighting conditions. The tomatoes were harvested every 3–4 days. To compare the total yield, the harvested fruits of each plot were counted and weighed. The fruit quality was evaluated, and the fruits were categorized into marketable and non-marketable. Within the non-marketable category, the fruits were sub-categorized into blossom-end rot (BER), cracks due to disturbed moisture balance, and other (damaged during manipulation, not properly ripe, too small, etc.). Unlike the other sub-categories, BER occurred only at specific periods with a higher risk to reduce the weekly marketable yields. Therefore, its yield percentage was calculated only based on these periods. Once a week, the diameter of the second tomato fruit of each truss within each plot was measured. The average fruit diameter was calculated per treatment for each year. The stem growth of the tomato plant was followed weekly by measuring the stem length gain of three plants per plot. 2.4. Water quality measurement The EC and pH of the NS were monitored once a week in the feeding tank, in the slabs and in the drain water. EC was measured with a conductivity tester (ProfiLine Cond 3110, WTW, Weilheim, Germany), and pH with a pH-meter (ProfiLine pH 3110, WTW, Weilheim, Germany). The solution content in macronutrients (i.e. Ammonium, Nitrate, 3
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nutrient content of the RAS wastewater and the drain water, the amount of fertilisers needed was calculated with a specific software (Yarasoft dealerversie 3.0 beta, Yara, Rotterdam, The Netherlands). In 2015, a constant EC was aimed in both objects. In 2016 and 2017, a higher EC in the AP was tolerated, in order to obtain a better reuse of drainwater. Addition of the calculated amounts of fertiliser to the mixture of new water and drain water happened automatically by the Nutronic device (PRIVA, De Lier, The Netherlands), in combination with the PRIVA connect software.
2.5. Sodium monitoring The AP feeding water had a highly variable EC because NaCl was intermittently inserted into the RAS water to prevent fish health problems. It was decided not to dilute the RAS water and thus not to control the EC in the AP feeding NS, leading to a different EC of that in the HP. The fish water was then, independently of its EC, complemented with the macro- and micronutrients to meet the concentration targets (i.e. same as for the HP treatment). It was aimed also to apply in both treatments the same rate of reused drain water. This resulted in a higher EC in the AP treatment compared to conventional hydroponic standards. Occasionally, when weekly growth measurements indicated a reduced growth, the AP drain water was flushed, and the irrigation system was rinsed with the standard solution.
2.7. Statistical analysis The statistical analysis was carried out with the AGROVA statistical package software, developed and validated by Inagro. The experimental data were tested for the null hypothesis that the use of complemented RAS wastewater for the cultivation of tomatoes did not cause any effect as compared to the HP control. For growth, fruit size and yield, combined analysis of variance over 3 years was applied, years being considered as a random variable, and the effect of the treatments being tested against the interaction “years x treatments”. Multiple comparison of means was carried out with the Duncan test. The average nutrient concentrations in the feeding NS and in the slabs, and the results of the Brix measurements (n = 120) were compared with a Duncan test, in addition to ANOVA. As for each time point only one analysis was available per treatment, successive time points were taken as replicates.
2.6. Nutrient solution formulation The standard feeding NS for the HP treatment was formulated with 20% tap water and 80% rain water and by the addition of the following commercial fertilisers (Yara, Rotterdam, The Netherlands): Amnitra (ammoniumnitrate), Calsal (calciumnitrate), Magnesul (magnesiumsulfate), Baskal (potassiumhydroxyde), BFK (potassiumpolyphosphatehydroxyde), Sulfakal (potassiumsulfate), SZ-38 (Nitric acid), DTPA-Fe, Fervent Mn (manganesesulfate), Fervent Zn (Zincsulfate), Fervent B (Boronpotassiumhydroxyde), Fervent Cu (coppersulfate) and Fervent Mo (Molybdenumoxide). The targeted nutrient concentrations for the feeding solutions were as follows, in accordance to general practice in Flanders, for macronutrients (mmol/l): 16 NO3, 1.2 TAN, 1.4 PO4, 9.5 K, 5.4 Ca, 2.4 Mg, 4.4 SO4 and for micronutrients (μmol/L): 30 B, 15 Fe, 0.75 Cu, 10 Mn; 5 Zn, 0.5 Mo. …. The formulation was slightly adjusted during the season according to the plant development following the recommendations of Heuvelink (2005). The NS for the AP treatment was formulated with RAS water and the same commercial fertilisers were added to reach concentrations in macro- and micronutrients equivalent to the standard hydroponic NS. Prior to the experiment, the content in macro- and microelements of RAS water was regularly measured and was found to be relatively constant (Table 1). Every two weeks the NS in both treatments was adjusted using new measurements of the drain water. Based on the desired EC and the
3. Results 3.1. Tomato production For the 3 years studied, the total yields (not shown) and marketable yields (Fig. 2) of tomato fruits of the AP and the HP treatments were not significantly different (Duncan test, p > 0.05). No significant interaction was found between the NS type and the years. Over the overall experiment, the average total yield and the average marketable yield respectively were 48.3 ± 2.4 and 47.3 ± 2.4 kg/m² for the AP treatment, 48.0 ± 1.8 and 46.3 ± 1.8 kg/m² for the HP treatment. Hence, in both treatments there was only a small difference (0,0 to 2,0%) between total and marketable yield. When BER occurred, depending on the year, the yields were affected more strongly (Fig. 3). While the level of BER varied substantially (i.e. range of 0.9–18.6 %) in the HP
Table 1 Nutrient concentrations in RAS wastewater, in AP and HP feeding solutions. RAS wastewater (n = 43)
AP feeding (n = 24)
HP feeding (n = 24)
1.24 ± 0.41 7.85 ± 0.10
3.40 ± 0.70 6.34 ± 0.33
3.15 ± 0.53 6.24 ± 0.32
Macroelements (mmol/L) TAN 0.26 ± 0.31 K 0.30 ± 0.13 Ca 3.58 ± 0.41 Mg 0.71 ± 0.14 NO3 1.52 ± 0.81 SO4 1.03 ± 0.21 PO4 0.07 ± 0.03 Cl 3.58 ± 3.79 Na 3.82 ± 3.73
1.16 ± 0.74 8.60 ± 2.87 6.38 ± 1.60 2.61 ± 0.80 16.97 ± 4.59 4.69 ± 1.35 1.54 ± 0.42 3.58 ± 3.14 4.32 ± 3.04
1.10 ± 0.66 8.84 ± 3.96 6.60 ± 1.37 2.65 ± 0.72 17.93 ± 3.92 4.52 ± 1.15 1.47 ± 0.38 0.60 ± 0.12 1.49 ± 0.35
Microelements (μmol/L) Fe 1.04 ± 1.23 Mn 0.62 ± 0.94 Zn 0.73 ± 0.75 B 6.07 ± 2.38 Cu 0.15 ± 0.22 Mo –
45.01 ± 13.59 12.22 ± 2.70 6.99 ± 2.04 45.01 ± 13.59 0.95 ± 0.39 –
22.45 ± 7.50 12.67 ± 3.25 7.36 ± 2.28 45.50 ± 10.92 0.99 ± 0.31 –
EC (dS/m) pH
60
50
a
a
a
a
a
a
HP AP
40
30
20
10
0 2015
2016
2017
Fig. 2. Yearly average of the marketable yields of tomato for the 4 plots studied. AP: aquaponic treatment, HP: hydroponic treatment. The Duncan test was performed, and different small letters indicate significant differences (p < 0.05).
*Average over the overall experiment ± standard deviation. n = number of measurements; TAN = total ammoniacal nitrogen; - = no measurement. 4
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Fig. 3. Percentage of tomato yields affected by blossom-end rot (BER) during its occurring period for the 4 plots studied. BER occurred from 29/06 to 03/09 in 2015, from 23/05 to 07/09 and from 03/10 to 31/10 in 2016 and from 27/06 to 04/09 in 2017. The Duncan test was performed, and different small letters within the same year indicate significant differences (p < 0.05).
deviated from them with a quite constant value: on average -4.89 mmol/L for AP and -4.25 mmol/L for HP. In addition, analysis of the macro- and micronutrients in solution in slabs revealed significant difference between both treatments only for the Mn in 2016 and 2017 (Table 2). Mn was less concentrated in the AP slabs. In 2015 also, Mn was less concentrated in AP slabs but not significantly. Overall in both treatments, the nutrients were more concentrated in slabs than in the feeding NS, except for TAN. Only in 2017, Mg and pH were significantly higher in the AP slabs.
treatment, it was remarkably constant and low (i.e. range of 0.2 to 0.4%) over the years in the AP treatment. Although in each year, the incidence of BER was lowered in the AP treatment, the difference between both treatments was significant in 2016 and 2017. Combined ANOVA could not detect any significant effect of the NS type because the mean square value of the interaction (years x NS type), used to calculate the F value, was relatively large to the mean square value of NS type. For the number of fruits produced and for the tomato fruit diameter, no significant difference was found between both treatments) (results not shown). The fruit diameter was remarkably constant over the years with an overall average of 67 ± 3 mm. At some point during the production seasons, some wilting at the top of the tomato stems and inferior weekly growth was observed in the AP treatment. This was always consistent with the sodium peaks in the AP slabs, and was reflected in a lower total stem length for AP (average final stem size over 3 years being 868.6 cm) than for HP (average final stem size of 878.64 cm), although the difference was not significant.
4. Discussion 4.1. Tomato production In our experimental design, the AP treatment differed from the HP only by its water origin. We aimed to have a similar feeding regime in both treatments (i.e. equivalent nutrient supply and pH in the respective feeding solutions). This goal was achieved, as no significant pH, macro- and micronutrient concentration differences between the AP and the HP treatment were found in the feeding NS. The only detected difference was the higher concentration of Na+ and Cl− for the AP treatment. Consequently, a significantly higher EC (+1.2 dS/m in 2016, and +1.3 dS/m in 2017) was detected in the AP than in the HP slabs (Table 2 and Fig. 4). Indeed, Na and Cl were present in substantial concentrations in the pikeperch water. The reason was that NaCl salt was directly added in the RAS water to prevent fish health issues due to stress occurring at fish grading. Frequent fish grading was done for research purposes and NaCl was applied directly after grading at concentrations of up to 34 mmol/L. Cl concentrations in slabs were always lower than Na ones with an approximately constant value, giving some evidence for plant uptake to be the cause. After correction for the difference between Cl and Na concentrations already present in the feeding NS, the remaining difference caused by plant uptake was 4.08 mmol/L for AP, and 3.29 mmol/L for HP. While high Cl and Na contents can induce salt stress, high Na contents can induce a supplemental deleterious effect due to the antagonism with K and Ca uptake. Indeed, during two short periods in 2016 and 2017, a reduced plant growth was noticed. To prevent further growth reduction, the drain water was discharged. It is commonly admitted that plant growth and yield are adversely influenced by salinity stress (Cuartero et al., 1999; Kanayama and Kochetov, 2015; Soria and Cuartero, 1998; Zhai et al., 2015) or by high root zone concentrations of Na (Cuartero and Fernández-Muñoz, 1998).
3.2. Water quality The pH and macro- and micronutrient concentrations in the AP feeding NS were maintained close to the targeted HP concentrations and on the average over all growing periods no significant differences were found between both treatments (Table 1). Only a difference in Na and Cl was observed, with on average 2.90 times more Na and 5.97 times more Cl in the AP. Na concentration in AP feeding NS variated from 1.31 to 11.84 mmol/L with an average of 4.32 mmol/L. In the HP feeding solution Na concentration (?) variated only from 0.87 to 2.23 mmol/L, with an average of 1.49 mmol/L. Cl concentrations approximately showed the same variability. The higher Na and Cl contents in the AP feeding solution resulted in the AP slabs in 2016 and 2017 in persistently higher concentrations of these elements and a significantly higher EC. Fig. 4 shows EC and measured Na contents. Some high peaks of Na (e.g. up to 35 mmol/L) were observed in the AP slabs, especially in 2016 and 2017. Because of these peaks, the AP drain water was flushed and the slabs were rinsed on the 28th of April and 25th of July in 2016 and on the 26th of April and 24th of September in 2017. On average, Na content in AP slabs was 11.48 ± 7.32 mmol/L. Average Na concentration in HP slabs was much lower (4.44 ± 1.71 mmol/L), but was quite constant over the growing period. Cl concentrations in the slabs showed the same variability as Na concentrations – high for AP and low for HP – and 5
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Fig. 4. Na+ concentrations and EC in the hydroponic (HP) and aquaponic (AP) slabs for each year studied.
tomato fruit yields and fruit number were not significantly different between the AP and the HP treatment. Slightly more marketable fruits were recorded in the AP treatment in 2015 and 2017 but this yield increase was not significant. This slight yield difference is presumably linked to the incidence of BER that was always lower (significantly lower in 2016 and 2017) and remarkably constant through the seasons and years (i.e. < 0.4%) in the AP treatment (Fig. 3). We only found two experiments comparing aquaponic tomato
In addition, the stress induced by salinity is known to increase BER symptoms and so to further reduce the marketable yields (Kanayama and Kochetov, 2015; Zhai et al., 2015). Consequently, because of the higher average EC, a lower fruit yield would have been expected in the AP treatment for both 2016 and 2017. Some EC peaks even were higher than 9 dS/m in the AP slabs. Although a slightly weekly lower yield has been observed after these peaks (result not shown), no significant reduction of the total yearly production occurred. Total stem length, total 6
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Table 2 Average nutrient concentrations in the hydroponic (HP) and aquaponic (AP) slabs. 2015 (n = 6)
EC (dS/m) pH TAN K Ca Mg NO3 SO4 PO4 Cl Fe Mn Zn B Cu
mmol/L
μmol/L
2016 (n = 11)
2017 (n = 14)
AP
HP
AP
HP
AP
HP
4362 ± 383 6.46 ± 0.71 0.19 ± 0.40 10.02 ± 4.13 8.32 ± 0.94 5.08 ± 0.64 21.25 ± 5.65 8.31 ± 1.74 1.58 ± 0.59 6.19 ± 8.15a 77.38 ± 52.99 8.32 ± 3.26 7.17 ± 3.54 76.29 ± 12.83 1.45 ± 0.67
4577 ± 662 6.05 ± 0.73 0.03 ± 0.03 10.37 ± 3.51 11.48 ± 2.47 5.79 ± 1.18 24.62 ± 5.44 9.60 ± 2.20 1.74 ± 0.69 0.18 ± 0.16b 102.72 ± 107.36 11.28 ± 5.70 6.32 ± 3.91 92.02 ± 25.25 1.73 ± 0.87
6806 ± 1590a 6.48 ± 0.81 0.20 ± 0.36 14.53 ± 5.78 14.48 ± 2.83 6.86 ± 1.62 36.72 ± 6.85 13.16 ± 3.38 1.68 ± 1.16 8.72 ± 6.98a 38.36 ± 21.71 5.51 ± 2.76a 10.33 ± 5.40 120.93 ± 53.57 1.40 ± 1.13
5539 ± 635b 6.08 ± 0.94 0.18 ± 0.21 14.04 ± 4.76 13.72 ± 3.94 6.87 ± 1.71 34.64 ± 5.98 11.95 ± 3.05 2.05 ± 1.16 0.19 ± 0.13b 51.06 ± 31.40 14.65 ± 9.67b 13.41 ± 7.62 115.65 ± 54.51 1.95 ± 1.63
6963 ± 1957a 6.28 ± 0.63a 0.12 ± 0.20 15.96 ± 5.76 14.47 ± 4.82 7.66 ± 2.99a 36.31 ± 13.08 13.62 ± 5.68 2.29 ± 1.48 7.49 ± 9.07a 75.51 ± 26.39 8.42 ± 10.20a 12.98 ± 5.62 161.51 ± 63.27 2.88 ± 1.25
5593 ± 1328b 5.58 ± 0.58b 0.22 ± 0.26 17.08 ± 6.31 12.03 ± 5.09 6.02 ± 3.07b 35.31 ± 9.63 10.14 ± 5.32 3.03 ± 1.67 0.18 ± 0.11b 80.51 ± 41 14.76 ± 12.32b 16.21 ± 6.41 140.31 ± 53.58 2.76 ± 1.23
*Yearly average concentration ± standard deviation, n is the number of measurements. The concentrations were compared using the Duncan test and significant differences between treatments are indicated in bold and by different small letters (p < 0.05). TAN = total ammoniacal nitrogen.
humic acid-like organic molecules (Hambly et al., 2015). Microorganisms and/or DOM may have acted as tomato plant biostimulants (du Jardin, 2015), providing possibilities to overcome the salinity stress and keep productivity as high, and sometimes higher, than in the HP treatment. At the end of each cultivation period, slightly more roots were observed on the side of the AP slabs, however for technical reasons it was not possible to weigh or score it. Such increase of root development is in accordance with the observations of Delaide et al. (2016a, 2016b) for lettuce in complemented RAS water. Indeed, microorganisms settled in the rhizosphere can beneficially interact with the plants (Bartelme et al., 2018) and promote root development (Amin et al., 2015; Wienhausen et al., 2017). Further experiments with a close monitoring of the root mass, plant biostimulating microorganisms and DOM presence are needed to confirm our assumptions.
production to a hydroponic control. Suhl et al. (2016) compared tomato production in NFT with complemented RAS water solution to that in hydroponic solution and also obtained similar yields in both treatments and lower BER in the complemented RAS water treatment. Crappé et al. (2017) compared complemented RAS water to hydroponics with drip irrigation and obtained similar yields. BER incidence was higher for the complemented RAS water treatment, but this was due to an excess of K, leading to an unfavourable K/Ca ratio. However, these studies were based only on one season of production, without succeeding to have similar (i.e. without significant differences) macro- and micronutrient concentrations in the feeding solutions of both treatments, making the interpretation of tomato production and BER symptoms, in our opinion, not sufficiently trustable. Regarding the statistical analysis, the experimental setup of 4 replicates studied for 3 years gave only 2 degrees of freedom for the interaction, years x treatment, against which the effect of the treatments was tested. This is quite low from a statistical point of view, but increasing this number of degrees of freedom for such large-scale semipractice experiment would require still more years of experiment, or a higher number of treatments. While the first solution was out of question, a higher number of treatments would have been at the expense of the semi-practice scale of the treatment. A few studies have reported higher yields (i.e. in vegetative mass) in complemented RAS water compared to hydroponic control for leafy vegetables as lettuce (Delaide et al., 2016b; Goddek and Vermeulen, 2018) and basil (Saha et al., 2016). For tomatoes however, no significant increase in tomato vegetative mass has yet been reported in literature. It was also not measured in our study, butit is important to notice that during tomato cultivation, the plants were continuously pruned to keep only two stems. Old leaves and suckers were thus continuously removed, and this biomass has not been quantified. As the observed increase of salinity and Na content in the AP treatment were supposed to reduce the plant production and increase BER symptoms, an important question is what can explain the absence of stress and this apparent resistance to salinity. The only possible answer is that RAS wastewater used in the AP treatment should contain factors that were not present in the HP water. Indeed, RAS water is charged with a variety of microorganisms (bacteria, fungi, protozoa, etc.) (Rurangwa and Verdegem, 2015; Schmautz et al., 2017; Schreier et al., 2010) and dissolved organic molecules (DOM). The latter are released by physicochemical degradation of the fish feed and the fish excretions, or by microorganisms (e.g. organic molecule alteration, triggering molecules for quorum sensing, etc.). Hence, a broad variety of DOM can be present as peptides, amino-acids, phytohormones-like,
4.2. Blossom-end rot and Mn Interestingly, Mn had a significant difference in concentration between treatments in the slabs. No technical intervention (i.e. unlike for Cl) could explain this difference. Mn was always lower in the AP slabs and this was repeated through the years (Table 2). On average, Mn was 1.9 times less concentrated in the AP than in the HP slabs. Compared to the feeding solution, Mn was slightly more concentrated in the HP slabs but 1.7 times less concentrated in the AP slabs. No significant differences were found between both treatments for the concentration of Mn in the feeding NS nor for the pH in the slabs, thus excluding the possibility of Mn loss by switching to an insoluble form (e.g. precipitation). As such, the lower concentration of Mn in the AP slabs indicates that AP tomato plants assimilated more Mn than the HP ones. This higher Mn assimilation then should be due to microorganisms that colonized the rhizosphere and improved the nutrient use efficiency (Meena et al., 2017) or increased the root mass. Silber et al. (2009) and Aktas et al. (2005) demonstrated that higher Mn content in fruit was correlated to reduced BER symptoms, and as we observed reduced BER and high Mn uptake, we suspect the tomato plants to have had a higher Mn content in their fruits. Unfortunately, in our study the Mn content in tomato leaves and fruits was not quantified. This should be achieved in further research to verify our assumption. Finally, as some authors claimed the low Ca concentration in the fruit tip, accompanying BER, to be a consequence of a metabolic disorder, related with an increase of reactive oxygen species (De Freitas et al., 2011; Saure, 2014), it is possible that microorganisms and/or DOM have interacted with the tomato plant metabolism and promoted 7
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resistance against BER via other ways than by only enhancing Mn uptake (Canellas et al., 2015; Mangmang et al., 2015).
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5. Conclusion In our study, we compared the production of tomatoes grown in a NS based on complemented RAS wastewater to tomatoes grown in conventional hydroponic NS. We especially achieved, for the first time, to accurately complement RAS water with macro- and micronutrient concentrations equivalent (i.e. no significant difference observed) to the hydroponic NS and this during 3 seasons of production. Our results clearly indicate the suitability of complemented pikeperch RAS wastewater as feeding water for professional HP tomato production using drip irrigation as similar growth and yields were obtained in AP and HP treatments. While a significant higher EC was recorded in the AP treatment, due to intermittent NaCl addition in the RAS water, the tomato yields did not diminish. Interestingly, symptoms of BER were even reduced in this treatment. As RAS water contains a diversity of microorganisms (e.g. bacteria, fungi, protozoa, etc.) and DOM (e.g. amino acid-like, phytohormones-like, humic acid-like organic molecules, etc.), it is presumed that some of these beneficially interacted with the plant metabolism (e.g. by promoting the root growth) and mitigated the salinity stress and the BER symptoms. This study delivered also much evidence that this was achieved by the promotion of Mn uptake which has been reported as a BER reducing factor. Further experiments with a close monitoring of the root mass, the nutrient content in leaves and fruits, especially Mn, would be needed to confirm our assumptions. The simultaneous identification and count of microorganisms present in the plant root zone using advanced technology such as flow cytometry and metagenomic techniques should be envisaged. Methods to identify plant promoting DOMs should also be applied. Funding This research was done in the frame of the INAPRO project funded by the European Union’s Seventh Framework Programme for research, technological development and demonstration under grant agreement number 619137. This research was also partly funded by the European Regional Development Fund via Aquavlan2 (Interreg V program Flanders - The Netherlands). Declaration of Competing Interest None. Acknowledgements The authors would like to acknowledge the European Commission via INAPRO and AquAVlan² for funding support. The authors also thank Ronny Versyck, Roger Houthoofd, Sofie Verhelst and Laurens Buyse for taking care of the experiment and the Inagro lab staff for the water quality analysis. References Aktas, H., Karni, L., Chang, D.C., Turhan, E., Bar-Tal, A., Aloni, B., 2005. The suppression of salinity-associated oxygen radicals production, in pepper (Capsicum annuum) fruit, by manganese, zinc and calcium in relation to its sensitivity to blossom-end rot. Physiol. Plant. 123, 67–74. https://doi.org/10.1111/j.1399-3054.2004.00435.x. Amin, S.A., Hmelo, L.R., van Tol, H.M., Durham, B.P., Carlson, L.T., Heal, K.R., Morales, R.L., Berthiaume, C.T., Parker, M.S., Djunaedi, B., Ingalls, A.E., Parsek, M.R., Moran, M.A., Armbrust, E.V., 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98. Bartelme, R.P., Oyserman, B.O., Blom, J.E., Sepulveda-Villet, O.J., Newton, R.J., 2018. Stripping away the soil: plant growth promoting microbiology opportunities in aquaponics. Front. Microbiol. 9. https://doi.org/10.3389/fmicb.2018.00008. Canellas, L.P., Olivares, F.L., Aguiar, N.O., Jones, D.L., Nebbioso, A., Mazzei, P., Piccolo,
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