water

Article Tomato Productivity and Quality in Aquaponics: Comparison of Three Hydroponic Methods

Zala Schmautz 1,*, Fionna Loeu 2, Frank Liebisch 2, Andreas Graber 1, Alex Mathis 1, Tjaša Griessler Bulc 3 and Ranka Junge 1,*

1 Institute of Natural Resource Sciences, Zurich University of Applied Sciences, Grüental, 8820 Wädenswil, Switzerland; fi[email protected] (A.G.); [email protected] (A.M.) 2 Institute of Agricultural Sciences, ETH Zurich, Universitätsstrasse 2, 8092 Zurich, Switzerland; fi[email protected] (F.L.); [email protected] (F.L.) 3 Faculty of Health Sciences, University of Ljubljana, Zdravstvena pot 5, 1000 Ljubljana, Slovenia; [email protected] * Correspondence: [email protected] (Z.S.); [email protected] (R.J.); Tel.: +41-589-345-928 (Z.S.); +41-589-345-922 (R.J.)

Academic Editor: M. Haïssam Jijakli Received: 14 September 2016; Accepted: 9 November 2016; Published: 16 November 2016

Abstract: Aquaponics (AP) is a food production system that combines hydroponic (HP) crop production with recirculating aquaculture. Different types of hydroponic systems have been used for growing crops in aquaponics. However, very few studies have compared their suitability and efficiency in an aquaponic context. The study presented here compares tomato yield, morphological (external) and biochemical (internal) fruit quality, and overall tomato plant vitality from three different HP systems (nutrient film technique, drip irrigation system, and floating raft culture) and examines the distribution of nutrients in different parts of the tomato plant. Three replicate AP systems were set up, each incorporating the three different HP systems coupled with a separate recirculating aquaculture unit growing Nile tilapia. The results showed that the choice of the cultivation system had little influence on most of the above-mentioned properties. Tomato fruit mineral content was found to be in similar range for N, P, K, Ca, Mg, Fe, and Zn as reported in the literature. Yield and fruit quality were similar in all three systems. However, the drip irrigation system did perform slightly better. The slightly higher oxygen radical absorbance capacity (ORAC) of the fruits grown in AP in comparison to commercially produced and supermarket derived tomatoes might indicate a potential for producing fruits with higher health value for humans.

Keywords: aquaponics; hydroponics; drip irrigation; floating raft culture; nutrient film technique; tomato; tilapia

1. Introduction Due to the increasing demand for food and the need to save freshwater, food production efficiency must be increased. Currently, more than 70% of the world’s freshwater resources are used for agricultural purposes [1], increasing the need for improved water use efficiency and the recycling of water in semi- or closed production systems. Food provision has a significant impact on the environment through greenhouse gas emissions, depletion of phosphorus, use of land and water resources, and release of chemical products [2]. On the other hand, today more than 54% of the world’s population lives in urban areas. It is expected that the urbanization trend will increase to 66% of the global population by 2050 [3]. Urban agriculture can produce food locally, uses resources very efficiently and has a minimum negative impact on the environment [4]. Food producers not only face the challenge of supplying

Water 2016, 8, 533; doi:10.3390/w8110533 www.mdpi.com/journal/water Water 2016, 8, 533 2 of 21 staple foods to meet caloric demand, but also the challenge of producing a wide variety of high quality foods with good nutritional properties. Therefore, it is important to find sustainable food production systems which can also be maintained within settlements or cities. Aquaponics (AP) is one of the most promising sustainable systems for food production that combines hydroponic systems (HP) with recirculating aquaculture systems (RAS). It has the potential to play a major role in food provision and tackling global challenges such as water scarcity, food security, water pollution, high energy use and excessive food transport miles [5]. If AP is operated in a closed water loop, it has little environmental impact because the food is produced with low water consumption [6,7]. Plant production yields in AP have been reported to be higher than for crops grown in soil [8,9], however data are scarce. In AP, nutrients enter the system in the form of fish feed. The feed is ingested and metabolized by the fish. The remains of the feed and the metabolic products from the fish dissolve in the water creating an aquaculture effluent that provides most of the nutrients required for plant growth in a HP part of the system. Microorganisms in the biofilter, on plant roots, and in the recirculating water release and convert the nutrients (e.g., phosphates from the debris, and ammonium to nitrate) and the plants assimilate them, thus treating the water, which flows back to the aquaculture component of the system [5,8]. In AP, fish, plants, and bacteria coexist in the same water, albeit in different compartments of the system [10]. Different types of HP systems have been used for growing crops in AP: (i) drip irrigation; (ii) floating raft culture; (iii) gravel bed; and (iv) nutrient film technique (NFT) [5–8,11–14], however very few studies have compared different HP production systems in an AP context. The only paper we are aware of is by Lennard and Leonard [15] compares floating rafts, gravel beds, and NFT for growing lettuce in AP and found that NFT produced significantly less biomass and removed the nutrients from fish water less efficiently than the other two systems. Generally, all plant species that can be adapted to growth in HP systems can also be grown in AP [16], meaning there is an extremely wide variety of choices. Savidov [17] reported growing over 60 different types of plant species in AP. Lettuce, specialty greens and herbs (chives, basil, spinach, and watercress) have low to medium nutritional requirements and are well adapted to AP [16]. Fruit yielding plants (tomato, bell pepper, cucumber, and squash) have a higher nutritional demand and perform better in heavily stocked AP systems. In indoor systems, the most commonly used tomatoes are greenhouse varieties which are better adapted than field cultivars to low light and high humidity conditions [16]. According to FAOstat [18], tomatoes are worldwide the second most important vegetable crop after potatoes. Tomatoes are rich in nutrients and vitamins which are associated with healthy food, i.e., carotenoids, flavonoids and lycopene [19,20]. Leaf nutrient concentrations can be used to detect the mineral nutritional status of the plants and thus might help to reveal differences in nutrient availability in different growing systems, whereas fruit nutrient content indicates the nutritional value for human consumption [21]. Graber and Junge [5] compared four varieties of tomatoes (Grapella, Rose of Berne, Frog King Golden Orb, and Sweet from Hungary) in AP, and in commercial HP cultivation with applications of mineral fertilizer according to Resh [22]. They found that all varieties performed better in AP. The purpose of this study was to compare tomato yields, morphological (external) and biochemical (internal) quality, and overall plant vitality in three different HP systems (NFT system, drip irrigation system, and floating raft culture). In addition, nutrient uptake and distribution within the tomato plants was also to be determined.

2. Material and Methods The experiment was conducted from 31 March to 5 November 2014 (220 days) in a double plastic covered greenhouse at the Zurich University of Applied Sciences (ZHAW) in Wädenswil, Switzerland. From 31 March to 11 June, the systems were operated as HP systems, with nutrient supplements added directly to the sump (Figure1). The required amount of nutrient supplements was calculated based on Water 2016, 8, 533 3 of 21 the water volume in the HP unit. On 12 June, the HP units were connected with the aquaculture unit Waterand the 2016 system, 8, 533 started to work as a quasi-closed loop AP. 3 of 21

Figure 1.1. PlanPlan of of the the experimental experimental subunits subunits in the in aquaponic the aquaponic laboratory, laboratory, from 31 from March 31 to 5March November to 5 November2014, with three2014, replicateswith three (A, replicates B, and C) (A, at B, the and Zurich C) at University the Zurich of University Applied Sciencesof Applied in Wädenswil,Sciences in Wädenswil,Switzerland. Switzerland. Framing line styleFraming indicates line whichstyle subunitindicates is connectedwhich subunit to which is component.connected to While which the component.elements are While drawn the to elements scale, the are distances drawn between to scale, themthe distances are not to between scale. them are not to scale.

2.1. The Aquaponic System Three identicalidentical experimental experimental recirculating recirculating AP systemsAP systems (A, B, (A, and C)B, wereand installedC) were in installed a greenhouse, in a 2 greenhouse,covering 270 covering m2 in total 270 (Figure m in 1total). Each (Figure AP system 1). Each (Figure AP system2) was (Figure composed 2) was of a composed fish holding of a tank fish holding(2700 L), tank a solids (2700 removal L), a solids unit (drum removal filter) unit with (drum water filter) level with sensor water (230 level L), solidssensor thickening (230 L), solids unit, thickeningi.e., radial flowunit, settler i.e., radial (45 L), flow a moving settler (45 bed L), biofilter a moving (580 bed L), biofilter an oxygenation (580 L), an zone oxygenation (30 L), a collection zone (30 L),sump a collection with water sump level with sensor water (470 level L), pipingsensor (65(470 L) L), and piping a HP (65 unit L) (730 and L). a HP The unit HP (730 unit L). in eachThe HP of three unit inAP each replicate of three systems AP replicate consisted systems of three consisted subunits: of three (i) NFT subunits: channel (i) (4 NFT m × channel0.2 m) (4 with m × four 0.2 m) coconut with fourfiber coconut slabs for fiber plant slabs support; for plant (ii) floating support; raft (ii) culture floating basin raft (650 culture L; 4 m basin× 1 m (650× 0.2 L; m)4 m with × 1 anm × aeration 0.2 m) −1 withpipe toan provideaeration additional pipe to provide oxygen additional to the roots oxygen (25 L ·tomin the−1 )roots and floating(25 L∙min rafts) and (Dryhydroponics, floating rafts (Dryhydroponics,BV’s-Gravenhage, BV’s The‐ Netherlands);Gravenhage, The and Netherlands); (iii) a drip irrigation and (iii) system a drip (4 irrigation m × 2 m) system with four (4 m coconut × 2 m) withfiber slabsfour coconut for plant fiber support slabs and for 20 plant narrow support tubes and delivering 20 narrow water tubes directly delivering to the plants.water directly Each replicate to the 3 2 plants.AP system Each had replicate a water AP volume system of had 4.85 a mwater3 and volume a surface of of4.85 35 m m2 and. a surface of 35 m . The climate in the greenhouse was controlled and recorded by a greenhouse climate computer (MasterClim 4 4 Zones, Zones, Anjou Anjou Automation, Automation, Mortagne Mortagne-sur-Sèvre,‐sur‐Sèvre, France). France). During During the day the day(start (start 1 h after 1 h astronomicalafter astronomical sunrise), sunrise), the heating the heating was was activated activated if the if the inside inside temperature temperature was was below below 18 18 °C◦C and aeration (openings in the greenhouse roof and additional ventilation) started if the temperature was above 20 °C.◦C. During the night (start 1 h after astronomical sunset), the heating was activated if the temperature was below 16 °C◦C and aeration started if the temperature was above 20 °C.◦C. The The sprinkling sprinkling system (CoolNet, (CoolNet, Netafim Netafim Ltd., Ltd., Tel Tel viv, Aviv, Israel) Israel) came came into into operation operation if the if the temperature temperature was was above above 27 °C27 ◦orC the or the humidity humidity below below 40% 40% (Figure (Figure 3).3 ).

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In Inorder order to tomake make a comparison a comparison to tocommercial commercial produc production,tion, four four tomato tomato plants plants of ofthe the same same cultivar cultivar InIn order orderIn order order to to tomake make to make make a a comparison comparison a a comparisoncomparison to to commercial commercial to to commercial commercial produc production, produc production,tion,tion, four four four tomato tomato four tomato tomato plants plants plants of plantsof the the of samethe same of same the cultivar cultivar samecultivar werewere grown grown hydroponically hydroponically on on rock rock wool wool using using dr ipdr ipirrigation irrigation in ina commerciala commercial greenhouse greenhouse (Meier (Meier werewerecultivarwere grown grown weregrown hydroponically hydroponically grown hydroponically hydroponically on on rock onrock rock wool onwool rockwool using using woolusing dr drip usingip dr irrigation irrigationip dripirrigation irrigation in in a ain commercial commercial a commercial in a commercial greenhouse greenhouse greenhouse greenhouse (Meier (Meier (Meier Gemüse,Gemüse, Paul Paul und und Ruedi Ruedi Meier, Meier, Rütihof, Rütihof, Switzerland). Switzerland). For For this this comparison comparison group, group, tomato tomato cultivation cultivation Gemüse,(MeierGemüse,Gemüse, Gemüse,Paul Paul Paul und und und Ruedi PaulRuedi Ruedi undMeier, Meier, Meier, Ruedi Rütihof, Rütihof, Rütihof, Meier, Switzerland). Switzerland). Switzerland). Rütihof, For Switzerland).For Forthis this thiscomparison comparison comparison For group, group, this group, comparison tomato tomato tomato cultivation cultivation cultivation group, measuresmeasures such such as aspesticide pesticide application application were were performed performed according according to toestablished established management management measuresmeasurestomatomeasures cultivation suchsuch such asas pesticide measuresaspesticide pesticide application suchapplication application as pesticide werewere were application performedperformed performed were accordingaccording according performed toto establishedtoestablished according established tomanagementmanagement establishedmanagement practicespractices in inSwitzerland Switzerland [24]. [24]. In Inaddition, addition, two two different different cherry cherry tomato tomato cultivars cultivars were were also also bought bought in in practicespracticesmanagementpractices in in Switzerland Switzerlandin practices Switzerland in [24]. [24]. Switzerland [24]. In In addition, addition,In addition, [24]. two two In addition,two different different different two cherry cherry differentcherry tomato tomato tomato cherry cultivars cultivars cultivars tomato were were cultivars were also also also bought bought were bought also in in in a supermarketa supermarket on on 15 15October October to tocompare compare internal internal fruit fruit quality quality traits traits from from the the experimental experimental system system aabought supermarket supermarketa supermarket in a supermarket onon 15 on15 October 15October October on 15 to to October compare compareto compare to internal compareinternal internal fruit fruit internal fruit qualityquality quality fruit traits traits quality traits fromfrom traitsfrom thethe fromthe experimentalexperimental experimental the experimental system system system withwith different different cultivars cultivars grown grown in inan an unknown unknown commercial commercial system. system. withwithsystemwith different different withdifferent different cultivars cultivars cultivars cultivars grown grown grown in in grown an anin unknown anunknown in unknown an unknown commercial commercial commercial commercial system. system. system. system.

Water 2016, 8, 533 5 of 21 Water 2016, 8, 533 5 of 21

Figure 3. FigureWeekly 3. Weekly mean valuesmean values for temperature for temperature (T), (T), and and relative humidity humidity (RH) (RH) in the in greenhouse, the greenhouse, and and electrical conductivity (EC) in the system water; n = 1 for RH and T and n = 3 for EC. electrical conductivity (EC) in the system water; n = 1 for RH and T and n = 3 for EC. 2.2. Stocking of the System 2.2. Stocking of the System In spring 2014, the AP system was stocked with tomato plants (Solanum lycopersicum L. cv. In spring“Gardenberry 2014, F1” the (Hild)) AP system and Nile was tilapia stocked (Oreochromis with niloticus tomato). Tomato plants seedlings (Solanum were lycopersicum obtained on L. cv. 28 February from Tozer Seeds Ltd. (Pyports, UK) and were supplied by Max Schwarz AG (Villigen, “Gardenberry F1” (Hild)) and Nile tilapia (Oreochromis niloticus). Tomato seedlings were obtained on Switzerland) before being cultivated further in the greenhouse. Seedlings were transplanted into the 28 FebruaryHP units from on Tozer 31 March. Seeds Initially, Ltd. (Pyports,each HP unit UK) hosted and seven were tomato supplied plants by with Max 24 shoots Schwarz (31 March– AG (Villigen, Switzerland)12 June). before On being 12 June, cultivated one random further healthy in the shoot greenhouse. per HP unit Seedlings was removed were to transplanted assess total green into the HP units on 31biomass March. in each Initially, HP unit, each leaving HP unit 23 shoots hosted per seven unit. To tomato ensure plantsequality with between 24 shoots HP units, (31 on March–12 25 July, June). On 12 June,one one shoot random per channel healthy was removed, shoot per leaving HP unit22 healthy was removedshoots, with to each assess tomato total plant green occupying biomass an in each average area of 1.1 m2. The tomato plants were cultivated using a high wire system [25], with the HP unit, leaving 23 shoots per unit. To ensure equality between HP units, on 25 July, one shoot per supporting wire at a height of 4.20 m. The growth period after transplanting was 31 weeks. The channel wastomato removed, plant tips leaving were cut 22 nine healthy weeks before shoots, the with end of each the experiment tomato plant to prevent occupying further an elongation. average area of 1.1 m2. ThePlant tomato protection plants with were beneficial cultivated organisms using (Encarsia a high formosa wire, system Ichneumons [25, ],and with Phytoseiulus the supporting persimilis) wire at a height ofand 4.20 pesticides m. The (Natural, growth Pegasus, period and after Envidor) transplanting was performed was 31 dependent weeks. on The the tomato needs (Table plant A1) tips were cut nine weeksand according before to the integrated end of thepest experiment management toprinciples prevent using further beneficial elongation. organisms Plant and protectionproducts with registered for organic production as standard pest control measures. Other chemical pesticides were beneficial organisms (Encarsia formosa, Ichneumons, and Phytoseiulus persimilis) and pesticides (Natural, only applied to control high pest pressure situations. Bumblebees provided by Andermatt Biocontrol Pegasus, andAG (Grossdietwil, Envidor) was Switzerland) performed were dependent used to support on the pollination. needs (Table In June, A1 a high) and occurrence according of spider to integrated pest managementmites was principlesobserved in usingthe greenhouse, beneficial with organisms one of the and raft culture products HP registeredsubunits (C9) for being organic the most production as standardaffected pest channel control (Figure measures. 1 and Other Figure chemical A1). However, pesticides a rating were of spider only mite applied damage to control on leaves high pest pressure situations.sampled for nutrient Bumblebees analysis provided did not show by Andermatt severe damage Biocontrol or significant AG differences (Grossdietwil, between Switzerland) the treatments. Towards the end of September blossom‐end rot was observed on some fruits in all of the were usedHP to units support (Figure pollination. A2). From July In onwards June, a regular high occurrence cutting of the of roots spider in the mites NFT was channels observed was in the greenhouse,necessary. with one Inside of thethe raftchannels, culture increasing HP subunits root biomass (C9) being was the blocking most affectedthe water channel flow, causing (Figure 1 and Figure A1leakages,). However, and clogging a rating the of pipes. spider The mite roots damage were cut on both leaves sides sampled of the channel for nutrient over a period analysis of a did not show severefew damagedays to cause or significant less stress to differences the plants, as between shown in the Figure treatments. A3. Rotten Towards roots were the observed end of after September blossom-endremoving rot was roots observed from the raft on culture some and fruits NFT in channels all of the in November. HP units The (Figure most damagedA2). From roots July were onwards found in the corners of the raft culture (Figure A4), probably resulting from insufficient aeration, and regular cuttingin the NFT of thechannels roots under in the the NFT coconut channels fiber slabs was (Figure necessary. A5). Inside the channels, increasing root biomass wasNile blocking tilapia the larvae water were flow, obtained causing from Til leakages,‐Aqua International and clogging (Velden, the The pipes. Netherlands). The roots On were 12 cut on both sidesJune, of theeach channel fish tank was over stocked a period with of300 a tilapias few days (approximate to cause 67.8 less g per stress fish). to The the fish plants, were fed as ad shown in Figure A3libitum. Rotten (i.e., roots to apparent were observed satiation) three after times removing a day (8:00, roots 13:00, from and the 17:00) raft with culture a swimming and NFT pelleted channels in November.feed The (Table most A2). damaged While nutrient roots wereuptake found by the intomato the corners plants remained of the raft more culture or less (Figure stable after A4), 12 probably resulting from insufficient aeration, and in the NFT channels under the coconut fiber slabs (Figure A5). Nile tilapia larvae were obtained from Til-Aqua International (Velden, The Netherlands). On 12 June, each fish tank was stocked with 300 tilapias (approximate 67.8 g per fish). The fish were fed ad libitum (i.e., to apparent satiation) three times a day (8:00, 13:00, and 17:00) with a swimming pelleted feed (Table A2). While nutrient uptake by the tomato plants remained more or less stable after 12 June, the fish biomass increased. Gained fish biomass over the entire aquaponic experiment was 59.0 ± 5.0 kg. Water 2016, 8, 533 6 of 21

To balance the feed input demand of the fish with nutrient demand of the plants, fish were harvested three times between 12 June and 5 November, according to the ZHAW internal standard operating procedure.

2.3. System Monitoring and Determination of Nutrient Supplementation for the HP System Electrical conductivity (EC), pH, dissolved oxygen, and temperature were measured continuously in the fish tank and logged every 15 min with SC1000 sensors from HACH Lange (Loveland, CO, USA). Calcium hydroxide and potassium hydroxide were used to adjust pH during the experiment. Weekly system water analyses of total phosphorus (TP), nitrate-nitrogen (NO3-N), nitrite-nitrogen (NO2-N), ammonium-nitrogen (NH4-N), potassium (K), iron (Fe), calcium (Ca), magnesium (Mg), and boron (B) were performed with a DR 3800 VIS Spectrophotometer and LCK tests (HACH Lange). Each week (1 April–5 November), one sample from each fish tank (A, B, and C) was taken in 500 mL plastic bottles. Nutrient target values for system water (Table1) were determined according to standard tomato nutrient requirements [26]. In mid-September, the parameters were adjusted to lower target values. HydroBuddy free software [27] was used to calculate the amount of nutrient supplementation needed to reach system water target values using Iron DTPA and Multi Micro Mix (Ökohum GmbH, Herrenhof, Switzerland), Krista SOP, Krista MKP, and YaraLiva® Calcinit (Yara UK Limited, Grimsby, UK), and EPSO TOP® (K + S Kali GmbH, Kassel, Germany). The target values for EC and pH were 2500 µS cm and 6.5, respectively throughout the entire experiment.

Table 1. Targeted levels (mg·L−1) for each measured parameter in the aquaponic system, and the corresponding HACH Lange LCK test numbers.

Parameter TP NO3-N NO2-N NH4-N K Fe Ca Mg B HACH Lange test number 349 339 341 304 328 321 327 326 307 31 March 2014 until 14 September 2014 40 160 0 0 250 3 200 50 0.2 15 September 2014 until 5 November 2014 40 160 0 0 234 3 130 24 0.2

2.4. Tomato Harvest and Biomass Sampling The fresh weight of removed biomass (pruned biomass, unripe tomato fruits, and roots) was recorded from 31 March to 5 November. Ripe (i.e., fully red) tomatoes were harvested twice a week from 15 May till 5 November. Harvested fruits were classified into three categories according to the current market requirements for cherry tomatoes (Table2)[ 28], and subsequently counted and weighed for each HP unit separately. Starting from 6 June, the tomato plants were pruned weekly by removing the side branches and old leaves, leaving 12–15 completely developed leaves on the shoots, and shortening the flower clusters to 15 tomatoes per cluster. The pruned biomass dry weight was determined twice, on 12 June and 25 July. After the final harvest on 5 November, the remaining biomass was weighed. To determine the dry weight, one tomato plant from each HP unit was used. Fresh samples were cut into pieces of approximately 2–4 cm with garden scissors, and oven-dried at 105 ◦C until they reached a constant weight (24–48 h). The dried samples were ground into a powder, which was later used to determine the total biomass nutrient content, as described below. To determine the leaf chlorophyll status (a plant vitality parameter), the leaf and fruit mineral nutrient concentrations, the internal fruit quality, the leaves and the fruits were measured and sampled on three dates (12 June, 7 August, and 16 October), after the respective fruit harvest. To analyze the leaf mineral nutrient content, the leaves located between the two trusses, where actual harvesting took place, were sampled from four plants. The chlorophyll status was estimated using a chlorophyll meter (SPAD-502, Minolta Corporation, Ramsey, NJ, USA) measuring the five leaflets at the tip of each leaf. Subsequently, leaves were cut and stored in a cooling box for later processing on the same day. Leaf stomatal conductance and temperature were measured with a steady state diffusion leaf porometer, SC-1 (Decagon Devices, Pullman, WA, USA) on the tip leaflet. Chlorophyll fluorescence was measured on the same five leaflets where the SPAD measurements were taken using a portable chlorophyll fluorometer (MiniPAM, Waltz Water 2016, 8, 533 7 of 21

GmbH, Effeltrich, Germany). Fluorescence was only measured for the second and third sampling harvest. To analyze the fruit, 16 random first category tomato fruits were selected from each HP unit and were analyzed as described below. To estimate the cumulative tomato fruit nutrient uptake for the tomato fruits harvested from 15 May to 10 July, results from the harvest on 12 June were used. Samples taken on 7 August were used for the period from 11 July to 12 September, and samples taken on 16 October were used for the last harvest period from 13 September to 5 November.

Table 2. Tomato quality classifications according to Swiss market quality norms for cherry tomatoes [28].

Category Criteria Fruit Quality Category 1 diameter: 20–35 mm marketable Category 2 diameter: >35 or <20 mm non-marketable, edible rotten, cracked, damaged, blossom-end rot, Category 3 non-marketable, not edible green or yellow colored (compost)

2.5. Leaf and Fruit Analysis To analyze the leaf mineral nutrients, the four sampled leaves and four fruits from each HP subunit channel were pooled and dried in an oven at 60 ◦C until a constant weight was reached. Prior to drying the fruits were cut into halves and the dried samples were ground to powder. To determine phosphorus (P), K, Ca, copper (Cu), sulfur (S), Mg, manganese (Mn), zinc (Zn) and Fe, 200 mg of dried powder was ◦ weighed into a Teflon tube and dissolved in 15 mL of nitric acid (HNO3, 70%) at 120 C for 90 min. After cooling down for 30 min, 3 mL of H2O2 was added and the solutions were incubated for another 90 min at 120 ◦C. After cooling down for a further 30 min, the solutions were transferred into 50 mL tubes and filled up to 50 mL with nanopure water. For measurement purposes, the solutions were diluted tenfold and analyzed with an axial ICP OES (Varian Vista MPX, Waldbronn, Germany). To obtain the carbon (C) and nitrogen (N) concentration, 2.5 mg of dried powder was weighed out into tin capsules and analyzed in a CHNSO analyzer EURO EA (HEKAtech GmbH, Wegberg, Germany). For sugar and acidity measurements, two freshly harvested tomato fruits were squeezed and blended (Moulinex, Glattpark, Switzerland) in four replicates for each HP subunit. The sugar content was then measured by a reflectometer (HR75, Fa. A. Krüss Optronic GmbH, Hamburg, Germany) using nanopure water as a blank. Acidity (fruit pH) was measured with a pH meter (Metrohm 632, Herisau, Switzerland). The remaining four tomato fruits were freeze-dried (Christ Freeze Dryers, Beta 2–8 L Dplus, Osterode am Harz, Germany). Prior to freeze-drying, several tiny holes were pierced into the tomato fruit skin to allow better evaporation. Afterwards, the tomatoes were ground up. The measurement of the fruit lycopene content was adapted from the protocol by Anthon and Garrett [29]. For this purpose, 25 mg of tomato powder was dissolved in 1.5 mL HEA (Hexane:Ethanol:Acetone, 2:1:1) and centrifuged. After centrifugation, the supernatant containing the lycopene was removed. To obtain all of the potential lycopene, this extraction step was repeated. Then, 0.45 mL of H2O was added to the pooled supernatant to reach phase separation. From the upper part, containing hexane with dissolved lycopene, 200 µL was placed in a transparent 96-well plate and measured in the Enspire 2300 multimode plate reader (Perkin-Elmer, Schwerzenbach, Switzerland) at 503 nm. A correction function for the organic solvents used was established using cuvette spectrophotometer (UV-1800, Shimadzu Manufacturing Inc., Canby, OR, USA) and a crystal glass cuvette. The optical absorbance of the lycopene solution is proportional to the lycopene concentration, which was calculated for each sample weight using the Equation (1) established by Anthon and Garrett [29].

  1.717 × A × V Lycopene mg·kg−1 = 503 (1) W where V is a volume of HEA solution (mL) and W is a sample weight (mg). Oxygen radical absorbance capacity (ORAC) was adapted from the protocol developed by Garrett et al. [30] For this purpose, 25 mg of tomato powder was dissolved in 1.5 mL MetOH Water 2016, 8, 533 8 of 21

(MetOH:H2O, 1:1), mixed and centrifuged. The supernatant that contained the antioxidants was removed. This extraction step was repeated three times. The removed supernatants were pooled into one sample. For measurement purposes, 20 µL of the sample were added to 200 µL of Fluorescein (Fluorescein Sodium Salt) and incubated at 37 ◦C for 10 min. After the incubation step, 75 µL of 2,20-azobis(2-amidino-propane) dihydrochloride were added before the absorption was measured in an Enspire 2300 multimode plate at a wavelength of 485 nm using an emission wavelength of 528 nm. A calibration curve was created using Trolox (Trolox (±)-6-Hydroxy-2,5,7,8-tetramethylchromane-2- carboxylic acid, 97%). The ORAC concentration is given as mmol TE L−1 where TE is the Trolox equivalent. The method for determining the total phenolic content (TPC) was adapted from the method developed by Waterhouse [31], using pooled extracts from the ORAC measurement. Thirty microliters of the sample was added to 30 µLH2O and 50 µL of FCR (Folin-Ciocalteau, 10%). After 1 min, 80 µL Na2CO3 were added. The plate was incubated for 2 h at room temperature before measuring at 765 nm in an Enspire 2300 multimode plate reader. A calibration curve was made using Gallic acid and measured together with the samples.

2.6. Statistical Analysis The data were statistically analyzed in R-project using the R-studio software (R version 3.0.2, 2013) [32]. The total fruit yield and biomass parameters were calculated, using a one-way Analysis of Variance (ANOVA) with the HP system as a factor. For the leaf and fruit analysis and the plant vitality parameters, a two-way ANOVA was performed using HP system and time of harvest as factors. If significant effects were found, a Tukey’s test (HSD test) with a p-value of p < 0.05 was performed.

3. Results

3.1. Tomato Yield and External Fruit Quality The tomato fruits measured approximately 25 mm in diameter, had a strawberry shape and a deep red color, a sweet flavor and firm consistency (Figure A6). The marketable yield (fruits of the category 1) was significantly highest in the drip irrigation and the non-marketable yield (category 2) was significantly higher in the raft culture system (Table3). The total cumulative yield per HP unit showed significantly better performance for the drip irrigation system (Figure A7). This was also observed for single harvests where the drip irrigation system often had the highest weekly yields and the raft culture provided the lowest ones (however, not always significantly different). The number of tomato fruits in category 1 was significantly highest in the drip irrigation system and the category 2 yield was significantly higher in the raft culture. Fruit fresh weight decreased significantly during the season but no differences were observed between the HP systems. The negligible difference in dry matter was only detected in category 1 where mean weight was highest in the drip irrigation system (19.4 ± 3.2 g) and lowest in the raft culture (18.8 ± 4.3 g).

Table 3. Average cumulative and total yield (g·m−2) and average number of tomato fruits (±SD) shown for three quality categories (Table2) in drip irrigation system, raft culture system, and nutrient film technique (NFT) system. Different letters indicate significant differences (Tukey’s HSD, n = 3, p < 0.05).

Fruit Quality Class Drip Irrigation System Raft Culture System NFT System Average cumulative yield (g·m−2) Category 1 18,323 ± 667 16,857 ± 341 17,176 ± 364 Category 2 86 ± 220 b 156 ± 290 a 73 ± 110 b Category 3 248 ± 108 371 ± 177 255 ± 650 Total 18,657 ± 568 a 17,383 ± 242 b 17,503 ± 339 b Average cumulative number of fruits Category 1 936 ± 350 877 ± 500 869 ± 350 Category 2 11 ± 400 b 20 ± 4.00 a 10 ± 200 b Category 3 15 ± 7.00 21 ± 900 16 ± 400 Total 963 ± 350 918 ± 580 895 ± 340 Water 2016, 8, 533 9 of 21 Water 2016, 8, 533 9 of 21

3.2.3.2. Internal Internal Fruit Fruit Quality Quality Parameters Parameters TheThe fruit fruit sugar sugar content content was was at at its its lowest lowest in in June, June, and and significantlysignificantly highest in the August August harvest harvest (Figure(Figure4A). 4A). The The significantly significantly highest highest sugar sugar content content was was measured measured in in the the NFT NFT system, system, andand the lowest inin the the drip drip irrigation irrigation system system (Figure (Figure4A). 4A). The The sugar sugar content content of of the the fruits fruits from from commercialcommercial HP control waswas in in the the same same range range as foras for the the drip drip irrigation. irrigation. The The fruit fruit sugar sugar content content of theof the October October harvest harvest was was not measurednot measured because because of low of number low number of fruits of and fruits other and fruit other analyses fruit analyses were prioritized. were prioritized. Fruit pH Fruit (acidity) pH was(acidity) significantly was significantly lowest in the lowest October in the harvest. October Pronounced harvest. Pronounced differences between differences the HPbetween systems the were HP onlysystems observed were in only the firstobserved harvest, in the when first the harvest, raft culture when showedthe raft culture significantly showed higher significantly fruit pH higher values thanfruit NFT pH (Figure values 4thanB). NFT (Figure 4B).

FigureFigure 4. Fruit4. Fruit internal internal quality quality parameters parameters sugar sugar content content (A); fruit (A); pH fruit (B );pH sugar–acid (B); sugar–acid ratio (C );ratio lycopene (C); contentlycopene (D); content total phenolic (D); total compounds phenolic (E compounds); and oxygen (E radical); and absorbanceoxygen radical capacity absorbance (F) compared capacity for raft(F) culture,compared drip irrigation,for raft culture, nutrient drip film irrigation, technique (NFT)nutrient and film a control technique group (NFT) cultivated and ina acontrol commercially group operatedcultivated hydroponic in a commercially system atoperated three sampling hydroponic points system in at summer. three sampling Error barspoints represent in summer. standard Error deviation.bars represent Different standard uppercase deviation. and lowercase Different letters uppercase indicate and significant lowercase differences letters (Tukey’sindicate significant HSD, n = 3, p

Water 2016, 8, 533 10 of 21

The fruits from commercial HP control had pH values similar to the aquaponically grown tomatoes. The ratio of the sugar to acidity ratio (Figure4C) showed similar tendencies, being lowest in June and highest in August; the NFT system delivered higher values and the drip irrigation system significantly lower values. Again, commercially produced tomato had similar values to the drip irrigation system. The fruit lycopene content was observed to be significantly highest in the August harvest (Figure4D), while only in the June harvest, were pronounced differences between the HP systems observed. At this time, the NFT system had significantly lower values compared to the raft and drip irrigation systems. The lycopene content measured in the commercially produced tomatoes was higher than in the aquaponically grown tomatoes throughout the entire season. The TPC was significantly higher in the October harvest compared to the June and August harvests. However, only in the August harvest, were significant differences between HP systems observed, when the drip irrigation system had the highest TPC (Figure4E). The commercially produced tomatoes had a lower TPC in the June and August harvests than in October. The ORAC changed significantly between harvests, with the highest ORAC observed in August and the lowest in October. No significant differences between HP systems were observed (Figure4F). However, commercially produced tomatoes had lower ORAC values. The comparison of fruit quality parameters from AP grown tomato (this study) and tomatoes bought in the supermarket with Swiss and Dutch origin revealed similar sugar contents, fruit pH and sugar content to pH ratios (Figure5). For lycopene and TPC, we observed slightly higher values in the supermarket tomato from the Netherlands, whereas Swiss supermarket and the AP system grown tomatoes had similar values. In terms of ORAC, we observed slightly higher values in the AP system grown tomatoes. In terms of fruit mineral concentrations, the most variance was found between harvests (Table4). While C, N, P and S concentrations in fruits decreased over time, the concentrations of K, Mg, Fe, Ca, Cu, Mn, and Zn increased significantly. Significant differences between the HP systems were only found for Mn, where the raft culture exhibited significantly higher concentrations in all three harvests compared to the drip irrigation and the NFT systems (Table5).

Table 4. Average fruit mineral concentrations (±SD) shown for the three harvests and the corresponding ANOVA results. Different letters indicate significant differences (Tukey’s HSD, n = 3, p < 0.05) for harvests. The factors, harvest (H) and treatment (T), and their interaction (H*T) were reported by “***” for p < 0.001, “**” for p < 0.01, “*” for p < 0.05 and “.” for p < 0.1.

Mineral Nutrient 1st Harvest 2nd Harvest 3rd Harvest ANOVA Result C (mg·g−1) 397.6 ± 2.20 A 408.5 ± 2.20 B 408.3 ± 3.10 B H: *** N (mg·g−1) 17.4 ± 0.8 A 15.4 ± 0.6 B 14.6 ± 0.5 B H: *** P (mg·g−1) 1.6 ± 0.1 A 3.8 ± 0.1 B 3.8 ± 0.1 B H: *** K (mg·g−1) 10.6 ± 0.3 B 28.6 ± 0.40 B 34.9 ± 2.5 A H: *** S (mg·g−1) 0.6 ± 0.0 A 1.5 ± 0.1 AB 1.4 ± 0.1 B H: **, HxT: . Mg (mg·g−1) 0.3 ± 0.0 B 1.1 ± 0.1 A 1.1 ± 0.0 A H: *** Fe (µg·g−1) 4.0 ± 2.0 C 24.7 ± 2.80 B 39.2 ± 15.3 A H: ***, T: . Ca (mg·g−1) 0.3 ± 0.1 AB 1.0 ± 0.3 A 0.6 ± 0.2 B H: *** Cu (mg·g−1) 1.2 ± 0.3 B 8.5 ± 4.6 A 8.9 ± 1.4 A H: ** Mn (µg·g−1) 4.1 ± 0.8 B 22.6 ± 9.6 A 27.3 ± 10.3 A H: ***, T: ***, HxT: * Zn (µg·g−1) 6.0 ± 0.5 B 16.2 ± 1.9 A 18.3 ± 1.60 A H: ***

Table 5. Average manganese fruit mineral concentrations (±SD) in µg·g−1 shown for the three harvests from each of the three hydroponic systems. Different letters indicate significant differences (Tukey’s HSD, n = 3, p < 0.05) between HP systems.

Harvest Drip Irrigation System Raft Culture System NFT System 1st (12 June 2014) 2.6 ± 0.1 b 4.2 ± 0.1 a 2.6 ± 0.1 b 2nd (7August 2014) 12.0 ± 5.1 b 31.4 ± 3.0 a 24.3 ± 5.8 b 3rd (16 October 2014) 20.2 ± 2.3 b 39.6 ± 6.7 a 22.2 ± 4.4 b Water 2016, 8, 533 11 of 21 Water 2016, 8, 533 11 of 21

Figure 5. Fruit internal quality parameters sugar content (A); fruit pH (B); sugar–acid ratio (C); lycopene Figure 5. Fruit internal quality parameters sugar content (A); fruit pH (B); sugar–acid ratio (C); content (D); total phenolic compounds (E); and oxygen radical absorbance capacity (F) of market tomatoes lycopene content (D); total phenolic compounds (E); and oxygen radical absorbance capacity (F) of produced in Switzerland (CH) and in The Netherlands (NL) compared to the average from the October marketharvest tomatoes in the produced aquaponic in system. Switzerland Error bars (CH) represent and in Thestandard Netherlands deviation; (NL) n = 4. compared to the average from the October harvest in the aquaponic system. Error bars represent standard deviation; n = 4. 3.3. Plant Productivity and Vitality Parameters 3.3. Plant ProductivityNo significant and differences Vitality Parameterswere observed in dry matter fraction between the HP systems. Whole Nogreen significant biomass results differences showed wereno significant observed differences in dry in matter the fresh fraction weight between between the the HP HP systems. systems. WholeThere green was biomass a difference results between showed the fraction no significant of dry matter differences of the whole in tomato the fresh plant weight at the beginning between the (12 June) and at the end of the experiment (5 November), with dry matter increasing by 40.2%. There HP systems. There was a difference between the fraction of dry matter of the whole tomato plant at were no significant differences in green cut between the HP systems. Plant height constantly the beginning (12 June) and at the end of the experiment (5 November), with dry matter increasing increased during the season with no significant differences between the HP subunits at the end of the by 40.2%.experiment There (data were not no shown). significant The average differences plant in length green of cutthe aquaponically between the grown HP systems. tomatoes Plant was 6.7 height constantlym. The increased weekly growth during rate the decreased season slightly with no over significant time and differencesthe average growth between rate the was HP 22 subunits cm per at the endweek. of the experiment (data not shown). The average plant length of the aquaponically grown tomatoes wasThe 6.7fractional m. The distribution weekly growth of nutrient rate decreasedcontent (C, slightly N, P, K, over Ca, Cu, time Mg, and Mn, the Zn, average and Fe) growth of the rate was 22tomato cm per fruits week. and green biomass in the total output of the HP subunits is presented in Figure 6. TheStatistical fractional analysis distribution only showed of nutrient significant content differences (C, N, in P, the K, Ca,amount Cu, Mg,of Mn Mn, between Zn, and the Fe) drip of the tomatoirrigation fruits andand greenthe floating biomass raft systems. in the total Overall, output there of was the an HP obvious subunits difference is presented between inthe Figure raft 6. culture and the other two HP systems. Statistical analysis only showed significant differences in the amount of Mn between the drip irrigation and the floating raft systems. Overall, there was an obvious difference between the raft culture and the other two HP systems. WaterWater2016 2016,, 88,, 533533 1212 of of 21 21

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channel channel channel channel channel channel channel channel channel channel

irrigation irrigation irrigation irrigation irrigation irrigation irrigation irrigation irrigation irrigation

Raft Raft Raft Raft Raft Raft Raft Raft Raft Raft NFT NFT NFT NFT NFT NFT NFT NFT NFT NFT Drip Drip Drip Drip Drip Drip Drip Drip Drip Drip C N P K Ca Cu Mg Mn Zn Fe Green biomass Tomato fruits

FigureFigure 6. Distribution of total total nutrient nutrient uptake uptake in in the the plant plant in in terms terms of of tomato tomato fruits fruits and and green green biomass biomass inin thethe aquaponicaquaponic system compared between between drip drip irrigation, irrigation, raft raft culture, culture, and and nutrient nutrient film film technique technique (NFT)(NFT) system;system; n = 3.

TheThe significantlysignificantly highest leaf leaf chlorophyll chlorophyll contents contents (SPAD) (SPAD) were were observed observed in in August August (Figure (Figure 7).7 ). However,However, only only in in June, June, did did measurements measurements show show significant significant differences differences between between the APthe systems,AP systems, when thewhen NFT the system NFT hadsystem significantly had significantly higher values higher than values the raft than culture the raft grown culture tomatoes. grown The tomatoes. commercially The growncommercially tomatoes grown were similartomatoes to were the raft similar culture to in the June raft and culture lower in in June August. and In lower October, in August. the relevant In October, the relevant leaf could not be measured due to a severe fungal infection. For leaf stomatal leaf could not be measured due to a severe fungal infection. For leaf stomatal conductance and conductance and leaf temperature (data not shown) significant differences between measurement leaf temperature (data not shown) significant differences between measurement times were found. times were found. However, no differences between the AP systems and the commercially grown However, no differences between the AP systems and the commercially grown tomato were observed. tomato were observed. The leaves of the commercially grown tomatoes showed similar results to the The leaves of the commercially grown tomatoes showed similar results to the AP grown tomatoes AP grown tomatoes except for the 2nd harvest. The electron transport rate of the photo‐system II except for the 2nd harvest. The electron transport rate of the photo-system II (ETR) was significantly (ETR) was significantly highest in August when the only significant AP system differences were highest in August when the only significant AP system differences were found in the raft culture, found in the raft culture, which had a lower ETR compared to the NFT system, while the drip which had a lower ETR compared to the NFT system, while the drip irrigation system values were irrigation system values were between the other two (data not shown). The ETR of the commercially between the other two (data not shown). The ETR of the commercially grown tomatoes tended to be grown tomatoes tended to be lower than in the AP systems. lower than in the AP systems.

Water 2016, 8, 533 13 of 21 Water 2016, 8, 533 13 of 21

Figure 7. Comparison of leaf SPAD values between plants grown in drip irrigation, raft culture, Figure 7. Comparison of leaf SPAD values between plants grown in drip irrigation, raft culture, nutrient film technique (NFT) and a commercial system; n = 3. Error bars represent standard nutrient film technique (NFT) and a commercial system; n = 3. Error bars represent standard deviation. deviation. Different uppercase and lowercase letters indicate significant differences (Tukey’s HSD, n Different= uppercase 3, p < 0.05) for and harvests lowercase and HP letters systems, indicate respectively. significant The differencesfactors, harvest (Tukey’s (H) and HSD, treatmentn = 3, (T),p < 0.05) for harvestsand their and interaction HP systems, (H*T) respectively.were reported by The “***” factors, for p < 0.001 harvest and “**” (H) for and p < 0.01. treatment (T), and their interaction (H*T) were reported by “***” for p < 0.001 and “**” for p < 0.01. 3.4. Plant Nutritional Status (Leaf Mineral Analysis) 3.4. Plant NutritionalIn terms of Status leaf mineral (Leaf Mineral concentrations, Analysis) significant differences were found between the harvests for all nutrients (Table 6). Significant differences between the HP subunits were only observed for C In termsand Mn. of leafThe NFT mineral system concentrations, had significantly significant higher C concentrations differences werethroughout found the between entire growing the harvests for all nutrientsperiod, while (Table the6 raft). Significant culture system differences had significantly between lower the C HP concentrations subunits were in the onlyleaves. observed The drip for C and Mn.irrigation The NFT system system did hadnot differ significantly from the NFT higher and raft C concentrations culture systems. Significant throughout differences the entire in Mn growing period, whileconcentrations the raft were culture observed system between had significantly the HP systems. lower The raft C concentrationsculture had the highest in the and leaves. the drip The drip irrigation the lowest mineral nutrient concentrations in the leaves. The NFT system values were irrigation system did not differ from the NFT and raft culture systems. Significant differences in Mn between the other two (Table 7). concentrations were observed between the HP systems. The raft culture had the highest and the drip irrigationTable the 6. lowest Average mineral leaf mineral nutrient concentrations concentrations (±SD) shown in the for leaves. the three The harvests NFT system and the values were between thecorresponding other two (Table ANOVA7). results. Different letters indicate significant differences (Tukey’s HSD, n = 3, p < 0.05) for harvests. The effect of factors (harvest (H) and treatment (T)) and their interaction (H*T) Table 6. Averagewere reported leaf mineralby “***” for concentrations p < 0.001, “**” for (± pSD) < 0.01, shown “*” for for p the< 0.05 three and harvests“.” for p < and0.1. the corresponding ANOVAMineral results. Nutrient Different letters1st Harvest indicate significant2nd Harvest differences3rd Harvest (Tukey’s HSD,ANOVAn = 3, Resultp < 0.05) for harvests. TheC (mg effect∙g−1 of) factors322.3 (harvest ± 12.1 (H)A and368.7 treatment ± 6.7 (T))B and365.0 their ± 8.2 interaction B (H*T)H: *** were reported N (mg∙g−1) 30.3 ± 0.6 A 37.0 ± 1.0 B 36.0 ± 1.0 B H: *** by “***” for p < 0.001, “**” for p < 0.01, “*” for p < 0.05 and “.” for p < 0.1. P (mg∙g−1) 1.8 ± 0.4 A 3.7 ± 0.6 B 3.3 ± 0.6 B H: *** K (mg∙g−1) 14.7 ± 0.6 B 39.3 ± 0.6 B 77.0 ± 10.5 A H: *** Mineral NutrientS (mg∙g−1) 1st Harvest8.3 ± 1.2 A 2nd22.0 Harvest ± 1.7 AB 23.3 ± 3rd5.1 HarvestB H: **, HxT: ANOVA . Result C (mg·g−1) Mg (mg322.3∙g−1)± 12.1 2.7 ± A0.6 B 368.7 ±5.76.7 ± 0.6 BA 6.0 365.0 ± 1.0± 8.2A BH: *** H: *** N (mg·g−1) Fe (μg30.3∙g−1) ± 0.622.7 ± A 5.5 C 37.0 99.3± 1.0 ± 17.8 BB 191.0 36.0 ± 116.5± 1.0 A BH: ***, T: . H: *** P (mg·g−1) Ca (mg1.8∙g−1)± 0.420.7 ± A 3.2 AB 3.7 ±45.00.6 ± 6.9 BA 58.3 3.3 ± 13.3± 0.6 B BH: *** H: *** K (mg·g−1) Cu (mg14.7∙g−1) ± 0.62.3 ± 0.6 B B 39.3 ±15.30.6 ± 1.5 BA 23.3 77.0 ± ±4.910.5 A AH: ** H: *** S (mg·g−1) Mn (μg8.3∙g−1)± 1.2107.3 ± A 56.2 B 22.0905.3± 1.7 ± 402.1 ABA 1308 23.3 ± 493.2± 5.1 A H: B ***, T: ***, HxT: H: **, * HxT: . Mg (mg·g−1)Zn (μg∙2.7g−1)± 0.69.7 ± 1.5 B B 5.7 ±60.70.6 ± 15.5 AA 156.7 6.0 ± ±10.31.0 A AH: *** H: *** Fe (µg·g−1) 22.7 ± 5.5 C 99.3 ± 17.8 B 191.0 ± 116.5 A H: ***, T: . −1 Ca (mg·g Table) 7. Average20.7 ± 3.2 manganese AB leaf mineral 45.0 ±concentrations6.9 A (±SD) in 58.3 μg∙±g−113.3 shown for the B three harvests H: *** −1 Cu (mg·g comparing) 2.3 all± three0.6 hydroponic B systems. 15.3 ± Different1.5 letters A indicate 23.3 significant± 4.9 differences A (Tukey’s H: ** µ · −1 ± ± ± Mn ( g g HSD,) n =107.3 3, p < 0.05)56.2 betweenB HP systems. 905.3 402.1 A 1308 493.2 A H: ***, T: ***, HxT: * Zn (µg·g−1) 9.7 ± 1.5 B 60.7 ± 15.5 A 156.7 ± 10.3 A H: *** Harvest Drip Irrigation System Raft Culture System NFT System 1st (12 June 2014) 59 ± 8.9 b 169 ± 34 a 94 ± 10.7 ab ± µ · −1 Table 7. Average2nd manganese (7August 2014) leaf mineral1302 concentrations ± 359 b ( SD)498 in± 241g g showna 916 for± 404 the ab three harvests comparing all3rd three (16 hydroponic October 2014) systems. 1870 Different ± 679 lettersb indicate1107 ± 592 significant a differences947 ± 533 (Tukey’sab HSD, n =3, p < 0.05) between HP systems.

Harvest Drip Irrigation System Raft Culture System NFT System 1st (12 June 2014) 59 ± 8.9 b 169 ± 34 a 94 ± 10.7 ab 2nd (7August 2014) 1302 ± 359 b 498 ± 241 a 916 ± 404 ab 3rd (16 October 2014) 1870 ± 679 b 1107 ± 592 a 947 ± 533 ab Water 2016, 8, 533 14 of 21

4. Discussion For the first ten weeks (1 April–12 June 2014), the system was operated as a hydroponic system. This phase of the experiment was mainly for system calibration and to assure that all HP subunits had the same quality of plants at the start of the experiment. After connecting the hydroponic systems with the aquaculture nutrient, target values remained the same as before. The resulting difference for the plants after changing from a HP nutrient solution to the AP nutrition was the source of the nutrients (from mineral to mainly organic, provided through fish feed input) and water temperature. The AP plants received heated water (29 ◦C) due to the fish requirements and the HP water was provided at ambient greenhouse temperatures which were usually lower than those of the aquaculture. Data of average yields of this particular tomato variety are not available. However, this variety could be compared with other cherry tomato varieties. Lattauschke [33] and Testa et al. [34] reported average yields of 15.0 and 16.6 kg·m−2, respectively. The exact durations of the seasons were not declared. The cumulative yield in our study was higher, ranging between 16.8 and 18.3 kg·m−2, depending on the HP system. Lennard and Leonard [15] compared lettuce growth in floating rafts, gravel beds, and NFT in AP. They found that NFT produced significantly less biomass and removed the nutrients from fish water less efficiently than the other two. In this study, also both, cumulative yield and cumulative number of fruits were lowest in the NFT system, and highest in the drip irrigation system. This system was the only HP system with a pulsing water flow, which provided more air and thus oxygen to the roots, which is known to positively affect plant growth and yield [35]. Problems with the floating raft culture (clogging of the aeration pipes) and the NFT system (root biomass blocking the water flow in the channels) during the season must be mentioned. This increased the maintenance work needed to keep the system in optimal condition, but could also have affected the plants. This was most obvious in the raft culture system where the aeration pipes clogged and the water mixing in the basin was hindered, especially in the corners, forcing the plants to continuously develop new roots. The drip irrigation system, which is the most commonly used cultivation method in commercial systems, on the other hand, demands a higher electricity input because of the more powerful pumps required, but nevertheless it was the cultivation system with the lowest maintenance input. The fruit quality in the investigated systems was generally high, reflected by the low proportion of either wrong sized fruits (category 2) or misshapen or damaged fruits (category 3), which were always below 2.5% and 9%, respectively. A higher fraction of non-marketable fruits (higher weight and number) was observed in the raft culture system. This could be related to more cracked fruits harvested at the ripe stage which may have resulted from the unlimited supply of water which has frequently been reported to promote fruit cracking in tomatoes [21,36]. Fruit internal quality is defined by parameters such as the content of fat, lipids, proteins, vitamins, mineral nutrients and pigments [20], as well as health related parameters such as TPC and ORAC [37]. In this study, the sugar content of the investigated fruits was generally high and, as to be expected, the time of harvest had the greatest effect on fruit sugar content. The lowest sugar contents were found when the plants were young, and there was not as much available light (duration and intensity) as in the summer. Although significant, the differences between the HP subunits were small, at less than 0.5%. It is unlikely that this difference can be perceived by consumers, and thus it cannot be truly stated as an advantage or disadvantage for the given HP system. Nevertheless, it seems that the lower fruit sugar content in the drip irrigation system is related to the higher fruit biomass produced (significant only for cumulated yield and fruit number) and thus might be a dilution effect. There were no pronounced differences in fruit pH or sugar-to-fruit pH ratio, indicating that they were very little affected by the HP systems and thus most likely have a negligible effect on internal fruit quality. The observed lycopene concentrations were generally at the upper limit of the reported range of 20 to 400 µg·g−1 [20]. The differences between the HP systems were not consistent in the three harvests, indicating marginal effects of season on the lycopene content of the fruits. The same was true for TPC and ORAC content. The observed TPCs were in the middle of the range of 1.2 to 22 µg·g−1 fresh weight that has been reported for processed tomatoes [38]. The observed ORAC values were in the Water 2016, 8, 533 15 of 21 upper range of 12–323 µmol·TE·g−1 dry weight reported by Li et al. [37] for processed tomatoes and higher than reported in Zhou and Liangli [39]. Fruit mineral contents of P, K, Ca, Mg were found to be in similar range to those reported for tomatoes in general, with Fe and Zn values higher in our study [20]. However, Dobromilska et al. [40] reported similar ranges for N, P, K, Ca, Mg, Fe and Zn in cherry tomato as those found in this study. This indicated that the tomatoes produced in our experiment have the expected mineral nutrient content for market cherry tomatoes. When comparing the HP systems, the only noteworthy difference was found for C and Mn. The lower C concentration in the raft culture is likely to be the result of higher water availability. The higher Mn concentrations found in the raft culture can probably be explained by the altered oxidative conditions in the standing water body rendering Mn to better plant available ions. In general, the fruit quality parameters of the AP and commercially produced fruits were in the same range. Only in terms of lycopene did the commercial fruits tend to have higher contents, where lower ORAC contents were also observed. Whether this observation can be attributed to slightly different ripening stages (commercial fruits were harvested slightly later), fungal fruit infection at the third harvest of the commercially produced fruits, or to the slightly different mineral nutrition (discussed below) is not clear. The higher ORAC observed in the HP systems might indicate that AP production seems to be less stressful for the plants and thus seems to favor the production of high-quality tomatoes. Even though literature [31] indicates that there might be interference between high sugar content and TPC measurements, our extracts were diluted by a high factor so that the sugar showed no effect on the TPC measurement. Therefore, a correction factor was not necessary. The comparison to values obtained from the supermarket tomatoes proved that tomato fruits from the AP systems reach the same or slightly better quality than tomatoes sold in stores. The higher SPAD values that correspond to the higher leaf chlorophyll contents observed in August and partly in October can be related to the N status as reflected by the leaf analysis which showed significantly lower leaf N concentration in June. This conclusion is supported by observations reported from Ulissi et al., and Fontes and de Araujo [41,42]. Fontes and de Araujo [42] reported a critical value of 37 mg·g−1: the values found in the June harvest and the others were close by. However, higher irradiation, as observed in August might also have affected leaf chlorophyll contents [43]. Leaf stomatal conductance and temperature were mostly linked to prevailing environmental conditions reflected by time of harvest in our experiment. The growing systems did not affect either parameter. Despite the fact that commercially grown plants were measured on a different day at similar time, the weather condition values were in the same range. The leaf mineral analysis revealed that mineral nutrition of the AP plants was suboptimal at the beginning of the experiment and the first sampling harvest, when values below the sufficiency range reported by Adams [35] were found for P, K, S, Ca, Mg, Fe, Cu, and Zn. This suboptimal mineral nutrition was very likely caused by the lower productivity (fruit yield), plant vitality (SPAD) and fruit quality (sugar content) observed in the first harvest. Optimizing the nutrient availability during this initial harvesting phase would very likely increase the overall output and quality of tomato fruit from the AP systems. However, providing nutrients in the solution is not enough, it is also important to be aware of the root health status ensuring plants can absorb nutrients efficiently. Deficient leaf mineral concentrations of P were found in the three sampling harvests and were more pronounced in the first harvest. However, in the second and the third sampling harvests, the values of 3.6 and 3.3 mg·g−1, were only slightly below the reported sufficiency range of 4.0 to 6.5 mg·g−1 [35]. The fact that no yield reduction was observed compared to commercial production, where leaf P concentrations of 5.0 mg·g−1 were found (Table A3), indicated that lower leaf P concentrations can be sufficient for high yield cherry tomato production. In contrast, we found very high values for Mn, which even increased to toxic levels above 1000 µg·g−1 [35] during the season. Although, we did not observe negative effects on yield, the higher TPC contents in fruits might be a result of the higher Mn. To avoid negative effects, Mn availability should be better controlled in future studies. Water 2016, 8, 533 16 of 21

5. Conclusions This is, to our knowledge, the first comprehensive study of comparison of different hydroponic methods in aquaponic cultivation that combines the assessment of total yield fruit quality with the distribution of nutrients in the plants, and fruit internal quality of the tomato. As tomatoes have a long vegetation cycle (up to eight months), studies on tomato are generally scarce. In comparison to the literature, the study showed that cherry tomatoes grown in aquaponic systems achieved similar yield and fruit quality to their counterparts grown independent of the method of cultivation implemented. The slightly higher ORAC content of fruits compared to the commercially produced HP control or supermarket derived tomatoes might indicate a potential for producing fruits that are also healthier for the consumer. The drip irrigation system performed better than the raft culture and NFT systems. There were only marginal effects on plant mineral status, indicating that all three systems can be applied successfully. However, the lower dry matter content, fruit quality and potentially increased risk of partly anoxic conditions and slightly altered nutrient availability in the root zone might indicate that the raft culture is less appropriate for the AP production of cherry tomatoes. Future studies should focus on comparisons with commercial production and optimizing nutrient availability to ensure good yields and prevent enrichment of nutrient minerals to toxic levels.

Acknowledgments: We thank ERASMUS Student Mobility Grant for partial financing of Zala Schmautz’s exchange semester at the ZHAW and the ZHAW IUNR for supporting the experiment financially. We would also like to thank Fridolin Tschudi and Max Mayer for planning and building the settlers; Theo H. M. Smits for reading and commenting on the manuscript; Darren Mace for language editing; Gabriela Gottschalk and Beat Häcki, interns at ZHAW for their support during the experiment; Bjørn Studer from the soil protection group of the ETH for support in the mineral nutrient analysis; and Annika Ackermann from the ISO Lab of the ETH Zurich for help with the C and N measurements. Author Contributions: Zala Schmautz, Alex Mathis and Andreas Graber conceived and designed the experiments. Zala Schmautz, Andreas Graber, Alex Mathis, Fionna Loeu and Frank Liebisch performed the experiment. Zala Schmautz, Fionna Loeu and Frank Liebisch performed measurements. Zala Schmautz, Fionna Loeu and Frank Liebisch analyzed the data. Ranka Junge was the main supervisor for the entire project. Tjaša Griessler Bulc supervised the Master’s thesis of Zala Schmautz and Frank Liebisch supervised the Master’s thesis of Fionna Loeu on which this paper is based. All authors contributed to discussions and writing of the paper. Conflicts of Interest: The authors declare no conflict of interest.

Appendix A

Table A1. Application of beneficial organisms, pesticides and their applied concentrations on tomato plants in “Wädenswil aquaponic system” in 2014.

Plant Protection Application Dates Function (Provider) (Day/Month, Where Applicable) and Concentrations Encarsia formosa 22/04, 05/05, 03/06, 17/06, 01/07, Combating white fly (Andermatt Biocontrol) 08/07, 14/07, 29/7, 11/8, 26/8 Ichneumons Combating aphids 22/04, 05/05, 03/06, 17/06, 01/07, 11/8, 26/8 (Andermatt Biocontrol) Phytoseiulus Combating spider mites 01/07, 08/07, 14/07, 29/07 (Andermatt Biocontrol) Bumble bees Pollination 25/03, 11/08 (Andermatt Biocontrol) Natural 24/06 1 (1%), 26/07 1 (1%), 22/07 3 (1%), Combating aphids and spider mites (Andermatt Biocontrol) 29/09 3 (1%), 09/08 1 (1%) Pegasus 14/07 3 (0.15%), 15/07 2 (0.15%), 22/07 2 (0.15%), Combating spider mites (Syngenta) 29/07 2 (0.15%), 09/08 1 (0.075%) Envidor Combating spider mites 09/08 1 (0.04%) (Bayer Crop Science) Notes: 1 Application on the whole plant; 2 Application on the upper half of the plant; 3 Application on the lower half of the plant. Water 2016, 8, 533 17 of 21

Table A2. Fish feed (in kilograms) fed to tilapia during the experiment. Water 2016, 8, 533 17 of 21 Fish Feed Producer System A System B System C Table A2. Fish feed (in kilograms) fed to tilapia during the experiment. Tilapia Vegi 3.0 Hokovit, Hofmann Nutrition AG (Bützberg, CH) 3.83 3.83 3.83 Fish Feed Producer System A System B System C Tilapia Vegi 4.5 Hokovit, Hofmann Nutrition AG (Bützberg, CH) 51.19 51.92 51.96 Tilapia Vegi 3.0 Hokovit, Hofmann Nutrition AG (Bützberg, CH) 3.83 3.83 3.83 Tilapico TEMPOTilapia 4.5 Vegi 4.5 CoppensHokovit, International Hofmann Nutrition B.V. (Helmond, AG (Bützberg, NL) CH) 51.19 13.40 51.92 13.4051.96 13.40 Water 2016, 8, 533 17 of 21 Primo floatTilapico 37/12 TEMPO 4.5 4.5 AllerCoppens Aqua International A/S (Christiansfeld, B.V. (Helmond, DK) NL) 13.40 20.95 13.40 20.9313.40 20.93 Primo float 37/12 4.5 Aller Aqua A/S (Christiansfeld, DK) 20.95 20.93 20.93 EFICO Alpha 838F Table A2. Fish feed (in kilograms) fed to tilapia during the experiment. EFICO Alpha BioMarBioMar Group Group (Aarhus (Aarhus C, C, DK) DK) 10.00 10.00 10.00 10.0010.00 10.00 Tilapia838F 3.0 TilapiaFish Feed3.0 Producer System A System B System C Tilapia Vegi 3.0 Hokovit, Hofmann Nutrition AG (Bützberg, CH) 3.83 3.83 3.83 Tilapia Vegi 4.5 Hokovit, Hofmann Nutrition AG (Bützberg, CH) 51.19 51.92 51.96 TableTable A3.Tilapico LeafA3. LeafTEMPO and and fruit 4.5 fruit mineral Coppensmineral nutrient International nutrient concentrations concentrations B.V. (Helmond, NL) of of the the commercially commercially13.40 13.40 produced produced13.40 tomato. tomato. Primo float 37/12 4.5 Aller Aqua A/S (Christiansfeld, DK) 20.95 20.93 20.93 EFICO Alpha Leaf Analysis Fruit Analysis Mineral Nutrient LeafBioMar Analysis Group (Aarhus C, DK) 10.00 Fruit10.00 Analysis 10.00 Mineral Nutrient838F Tilapia 3.0 1st Harvest 2nd Harvest 1st Harvest 2nd Harvest 3rd Harvest C (mg∙g−1) 1st Harvest325.0 2nd Harvest359.0 1st403.6 Harvest 2nd393.2 Harvest 391.7 3rd Harvest Table A3. Leaf and fruit mineral nutrient concentrations of the commercially produced tomato. C (mgN·g −(mg1) ∙g−1) 325.040.0 359.040.0 19.8 403.6 14.3 393.2 18.8 391.7 − N (mgP·g (mg1) ∙g−1) 40.02.0 Leaf Analysis 40.05.0 1.6 19.8 Fruit Analysis4.6 14.3 6.3 18.8 Mineral−1 Nutrient P (mg·Kg (mg) ∙g−1) 2.01st24.0 Harvest 2nd 5.058.0Harvest 1st Harvest12.9 1.6 2nd Harvest38.1 4.6 3rd Harvest47.2 6.3 −1 −1 K (mg·g )C (mg−1 ∙g ) 24.0325.0 58.0359.0 403.6 12.9 393.2 38.1391.7 47.2 S −(mg∙g ) 8.0 25.0 0.5 1.2 1.7 · 1 −1 S (mg g )N (mg−1∙g ) 8.040.0 25.040.0 19.8 0.5 14.3 1.218.8 1.7 Mg −(mg∙g ) 2.0 4.0 0.4 1.1 1.2 Mg (mg·g 1P) (mg∙g−1) 2.02.0 4.05.0 1.6 0.44.6 1.16.3 1.2 Fe− (μg∙g−1) 36.0 175.0 20.7 40.4 60.4 Fe (µg·g 1)K (mg∙g−1) 36.024.0 175.058.0 12.9 20.7 38.1 40.447.2 60.4 − −1 Ca (mgCa·g (mg1S) (mg∙g ∙)g −1) 14.014.08.0 41.041.025.0 0.50.3 0.3 1.2 0.8 0.8 1.7 1.4 1.4 − −1 Cu (mgCu·g (mgMg1) ∙(mgg )∙ g−1) 2.02.02.0 8.08.04.0 0.42.0 2.0 1.1 4.4 4.4 1.2 13.2 13.2 − Mn (µMng·g (1μFe)g ∙(gμ−g1∙)g −1) 336.0336.036.0 1564.01564.0175.0 20.79.0 9.0 40.439.1 39.1 60.4 35.5 35.5 − Zn (µgZn·g (1μCa)g ∙(mgg−1)∙ g−1) 7.07.014.0 58.058.041.0 0.35.7 5.7 0.816.4 16.4 1.4 22.4 22.4 Cu (mg∙g−1) 2.0 8.0 2.0 4.4 13.2 Mn (μg∙g−1) 336.0 1564.0 9.0 39.1 35.5 Zn (μg∙g−1) 7.0 58.0 5.7 16.4 22.4

Figure A1. Tomato plants in raft culture subunit (C9) affected by spider mites at the end of June 2014. Figure A1. Tomato plants in raft culture subunit (C9) affected by spider mites at the end of June 2014. Figure A1. Tomato plants in raft culture subunit (C9) affected by spider mites at the end of June 2014.

Figure A2. Tomatoes in all hydroponic units affected by blossom‐end rot disease at the end of FigureFigure A2.September A2.Tomatoes Tomatoes 2014. in in all all hydroponic hydroponic unitsunits affected by by blossom blossom-end‐end rot rot disease disease at the at end the endof of SeptemberSeptember 2014. 2014.

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Figure A3. Cutting of the roots on both sides of the NFT channel over a period of a few days. Figure A3. Cutting of the roots on both sides of the NFT channel over a period of a few days. Figure A3. Cutting of the roots on both sides of the NFT channel over a period of a few days.

Figure A4. Difference between healthy roots in the middle and rotten roots in the corners of the raft Figure A4. Difference between healthy roots in the middle and rotten roots in the corners of the raft Figureculture A4. basin.Difference between healthy roots in the middle and rotten roots in the corners of the raft cultureFigure A4.basin. Difference between healthy roots in the middle and rotten roots in the corners of the raft culture basin. culture basin.

Figure A5. Rotten roots on the bottom of the NFT channels (bottom); and healthy roots in drip Figureirrigation A5. (top Rotten). roots on the bottom of the NFT channels (bottom); and healthy roots in drip Figure A5. Rotten roots on the bottom of the NFT channels (bottom); and healthy roots in drip irrigationFigure A5. (topRotten). roots on the bottom of the NFT channels (bottom); and healthy roots in drip irrigation (top). irrigation (top).

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Figure A6. Tomato plants (Solanum lycopersicum L. cv. ‘Gardenberry F1’ (Hild)) in summer 2014 in the Figure A6. Tomato plants (Solanum lycopersicum L. cv. ‘Gardenberry F1’ (Hild)) in summer 2014 in the WädenswilFigure A6. aquaponic Tomato plants system. (Solanum lycopersicum L. cv. ‘Gardenberry F1’ (Hild)) in summer 2014 in the Wädenswil aquaponic system. Wädenswil aquaponic system. 160 [kg]

160

140[kg]

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120 100 100 80 hydroponic

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60per

60 yield

yield 40 40

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Cumulative 0 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45

Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week Week RAFT CULTURE DRIP IRRIGATION NFT CHANNEL RAFT CULTURE DRIP IRRIGATION NFT CHANNEL

Figure A7. Average cumulative yield (n = 3) per hydroponic subunit of all three quality categories FigureFigure A7. A7.Average Average cumulative cumulative yield yield ( n(n= = 3)3) perper hydroponic subunit subunit of ofall allthree three quality quality categories categories from the “Wädenswil aquaponic system”, 2014. fromfrom the “Wädenswil the “Wädenswil aquaponic aquaponic system”, system”, 2014. 2014. References ReferencesReferences 1. Food and Agriculture Organization of the United Nations (FAO). Economic Valuation of Water Resources in 1. Food1. Food andAgriculture: and Agriculture Agriculture From the Organization Sectoral Organization to a Functional ofof the Perspective United United Nations of Nations Natural (FAO). Resource (FAO). Economic ManagementEconomic Valuation; FAO Valuation Water of Water Reports of Resources Water 27; Resources in in Agriculture:Agriculture:FAO: Rome, From From Italy, the the 2004. Sectoral Sectoral Available to a Functional to online: a Functional ftp://ftp.fao.org/agl/aglw/docs/wr27e.pdf Perspective Perspective of Natural ofResource Natural Management Resource (accessed; FAO Management on 13 Water June 2016).Reports; FAO 27; Water 2. FAO:European Rome, Italy,Commission. 2004. Available Environmental online: ftp://ftp.fao.org/agl/aglw/docs/wr27e.pdf Impact of Products (EIPRO). Analysis (accessed of the on Life 13 JuneCycle 2016). Reports 27; FAO: Rome, Italy, 2004. Available online: ftp://ftp.fao.org/agl/aglw/docs/wr27e.pdf (accessed 2. EuropeanEnvironmental Commission. Impacts RelatedEnvironmental to the Final Impact Consumption of Products of the EU (EIPRO).‐25. Technical Analysis Report. of2006. the Available Life Cycle on 13 June 2016). Environmentalonline: http://ec.europa.eu/environm Impacts Related to theent/ipp/pdf/eipro_report.pdf Final Consumption of the (accessed EU‐25. Technical on 5 September Report. 2016). 2006. Available

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