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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; fish@urbanfarmers.com (A.G.); alex.mathis@zhaw.ch (A.M.)
2 Institute of Agricultural Sciences, ETH Zurich, Universitätsstrasse 2, 8092 Zurich, Switzerland;
fi.loeu@gmail.com (F.L.); frank.liebisch@usys.ethz.ch (F.L.)
3 Faculty of Health Sciences, University of Ljubljana, Zdravstvena pot 5, 1000 Ljubljana, Slovenia;
tjasa.bulc@zf.uni-lj.si
* Correspondence: zala.schmautz@zhaw.ch (Z.S.); ranka.junge@zhaw.ch (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 (Figure 1). 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
and the system started to work as a quasi-closed loop AP.
Water 2016, 8, 533  3 of 21 

 
Figure  1. Plan
Figure 1. Plan ofof 
thethe  experimental 
experimental subunits 
subunits in thein aquaponic
the  aquaponic  laboratory, 
laboratory, from 31 from 
March31 
to 5March  to  5 
November
November 2014, with three replicates (A, B, and C) at the Zurich University of Applied Sciences in 
2014, with three replicates (A, B, and C) at the Zurich University of Applied Sciences in Wädenswil,
Wädenswil, 
Switzerland. Switzerland.  Framing 
Framing line style line which
indicates style  subunit
indicates  which  subunit 
is connected is  component.
to which connected  to  which 
While the
component. While the elements are drawn to scale, the distances between them are not to scale. 
elements are drawn to scale, the distances between them are not to scale.

2.1. The Aquaponic System 
2.1. The Aquaponic System
Three  identical 
Three identical experimental 
experimental recirculating 
recirculating AP  systems 
AP systems (A, B, (A,  B,  were
and C) and  installed
C)  were ininstalled  in  a 
a greenhouse,
greenhouse, covering 270 m
2 2 in total (Figure 1). Each AP system (Figure 2) was composed of a fish 
covering 270 m in total (Figure 1). Each AP system (Figure 2) was composed of a fish holding tank
holding 
(2700 L),tank  (2700 
a solids L),  a  solids 
removal removal 
unit (drum unit 
filter) (drum 
with water filter) 
levelwith 
sensorwater 
(230level  sensor thickening
L), solids (230  L),  solids 
unit,
thickening unit, i.e., radial flow settler (45 L), a moving bed biofilter (580 L), an oxygenation zone (30 
i.e., radial flow settler (45 L), a moving bed biofilter (580 L), an oxygenation zone (30 L), a collection
L), a collection sump with water level sensor (470 L), piping (65 L) and a HP unit (730 L). The HP unit 
sump with water level sensor (470 L), piping (65 L) and a HP unit (730 L). The HP unit in each of three
in each of three AP replicate systems consisted of three subunits: (i) NFT channel (4 m × 0.2 m) with 
AP replicate systems consisted of three subunits: (i) NFT channel (4 m × 0.2 m) with four coconut
four coconut fiber slabs for plant support; (ii) floating raft culture basin (650 L; 4 m × 1 m × 0.2 m) 
fiber slabs for plant support; (ii) floating raft culture basin (650 L; 4 m × 1 m × 0.2 m) with an aeration
with 
pipe to an provide
aeration additional
pipe  to  provide 
oxygenadditional 
to the roots oxygen 
(25 L·to minthe 
−1 )roots  (25  L∙min
and floating
−1)  and  floating  rafts 
rafts (Dryhydroponics,
(Dryhydroponics, BV’s‐Gravenhage, The Netherlands); and (iii) a drip irrigation system (4 m × 2 m) 
BV’s-Gravenhage, The Netherlands); and (iii) a drip irrigation system (4 m × 2 m) with four coconut
with four coconut fiber slabs for plant support and 20 narrow tubes delivering water directly to the 
fiber slabs for plant support and 20 narrow tubes delivering water directly to the plants. Each replicate
plants. Each replicate AP system had a water volume of 4.85 m
AP system had a water volume of 4.85 m3 and a surface of 35 m2 and a surface of 35 m
3
.
2. 

The climate in the greenhouse was controlled and recorded by a greenhouse climate computer 
The climate in the greenhouse was controlled and recorded by a greenhouse climate computer
(MasterClim 4 Zones, Anjou Automation, Mortagne‐sur‐Sèvre, France). During the day (start 1 h after 
(MasterClim 4 Zones, Anjou Automation, Mortagne-sur-Sèvre, France). During the day (start 1 h
astronomical  sunrise), 
after astronomical the  heating 
sunrise), was was
the heating activated  if  the 
activated inside 
if the inside temperature 
temperaturewas  wasbelow 
below18  18 °C 
◦ C and 
and
aeration (openings in the greenhouse roof and additional ventilation) started if the temperature was 
aeration (openings in the greenhouse roof and additional ventilation) started if the temperature was
above 20 °C. During the night (start 1 h after astronomical sunset), the heating was activated if the 
above 20 ◦ C. During the night (start 1 h after astronomical sunset), the heating was activated if the
temperature was below 16 °C and aeration started if the temperature was above 20 °C. The sprinkling 
temperature was below 16 ◦ C and aeration started if the temperature was above 20 ◦ C. The sprinkling
system (CoolNet, Netafim Ltd., Tel viv, Israel) came into operation if the temperature was above 27 
system (CoolNet, Netafim Ltd., Tel Aviv, Israel) came into operation if the temperature was above
°C or the humidity below 40% (Figure 3). 
27 ◦ C or the humidity below 40% (Figure 3).
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“Wädenswil aquaponic
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in2014:
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removed
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from from
from
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sludge was manually removed from the system three times a week and collected in an outdoor unit.  timestimes
times times
times aweek
aaweek aweek
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outdoor unit.unit.
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Solids-free water
water
water water
water
was
waswas was
was returned
returned
returnedreturned
returned to
to to
the
Solids‐free water was returned to the solids removal unit.  to
the the
to thesolids
the
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solids solids
solids removal
removal
removal removal
removal unit.
unit.
unit. unit.
unit.

InIn
order
In order
order to make
to
to make
make a acomparison
acomparison
comparison to to commercial
to
to commercial production,
production, fourfourtomato
tomato plants
plantsof the
of same
the samecultivar
cultivar
In
Inorder totomake
make a comparison
a comparison tocommercial
commercial
commercial production,
production, four
production, four tomato
tomato
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Water 2016, 8, 533 5 of 21
Water 2016, 8, 533  5 of 21 

Figure 3. Figure 3. Weekly mean values for temperature (T), and relative humidity (RH) in the greenhouse, and 
Weekly mean values for temperature (T), and relative humidity (RH) in the greenhouse, 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 ofIn the System
spring  2014,  the  AP  system  was  stocked  with  tomato  plants  (Solanum  lycopersicum  L.  cv. 
“Gardenberry F1” (Hild)) and Nile tilapia (Oreochromis niloticus). Tomato seedlings were obtained on 
In spring 2014, the AP system was stocked with tomato plants (Solanum lycopersicum 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 February from Tozer Seeds Ltd. (Pyports, UK) and were supplied by Max Schwarz AG (Villigen,
HP units on 31 March. Initially, each HP unit hosted seven tomato plants with 24 shoots (31 March–
Switzerland) before
12  June).  On being cultivated
12  June,  further
one  random  in the
healthy  greenhouse.
shoot  per  HP  unit Seedlings wereto transplanted
was  removed  into the HP
assess  total  green 
biomass in each HP unit, leaving 23 shoots per unit. To ensure equality between HP units, on 25 July, 
units on 31 March. Initially, each HP unit hosted seven tomato plants with 24 shoots (31 March–12 June).
one shoot per channel was removed, leaving 22 healthy shoots, with each tomato plant occupying an 
On 12 June, one random healthy shoot per HP unit was removed to assess total green biomass 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 was removed, leaving 22 healthy shoots, with each tomato plant occupying an average area of
tomato plant tips were cut nine weeks before the end of the experiment to prevent further elongation. 
1.1 m2 . The tomato plants were cultivated using a high wire system [25], with the supporting wire at a
Plant protection with beneficial organisms (Encarsia formosa, Ichneumons, and Phytoseiulus persimilis) 
height ofand pesticides (Natural, Pegasus, and Envidor) was performed dependent on the needs (Table A1) 
4.20 m. The growth period after transplanting was 31 weeks. The tomato plant tips were
and according to integrated pest management principles using beneficial organisms and products 
cut nine weeks before the end of the experiment to prevent further elongation. Plant protection with
registered for organic production as standard pest control measures. Other chemical pesticides were 
organisms (Encarsia formosa, Ichneumons, and Phytoseiulus persimilis) and pesticides (Natural,
beneficialonly applied to control high pest pressure situations. Bumblebees provided by Andermatt Biocontrol 
Pegasus, and Envidor) was performed dependent on the needs (Table A1) and according to integrated
AG (Grossdietwil, Switzerland) were used to support pollination. In June, a high occurrence of spider 
pest management principles using beneficial organisms and products registered for organic production
mites was observed in the greenhouse, with one of the raft culture HP subunits (C9) being the most 
affected 
as standard pest channel 
control(Figure  1  and Other
measures. Figure chemical
A1).  However,  a  rating 
pesticides of  spider 
were only mite  damage 
applied on  leaves 
to control high pest
sampled  for  nutrient  analysis  did  not  show  severe  damage  or  significant  differences  between  the 
pressure situations. Bumblebees provided by Andermatt Biocontrol AG (Grossdietwil, Switzerland)
treatments. Towards the end of September blossom‐end rot was observed on some fruits in all of the 
were used to support pollination. In June, a high occurrence of spider mites was observed in the
HP  units  (Figure  A2).  From  July  onwards  regular  cutting  of  the  roots  in  the  NFT  channels  was 
greenhouse, with one
necessary.  of the
Inside  the raft culture
channels,  HP subunits
increasing  (C9) being
root  biomass  was the most affected
blocking  channel
the  water  (Figure 1 and
flow,  causing 
Figure A1). However, a rating of spider mite damage on leaves sampled for nutrient analysis did not
leakages, and clogging the pipes. The roots were cut on both sides of the channel over a period of a 
few days to cause less stress to the plants, as shown in Figure A3. Rotten roots were observed after 
show severe damage or significant differences between the treatments. Towards the end of September
removing roots from the raft culture and NFT channels in November. The most damaged roots were 
blossom-end rot was observed on some fruits in all of the HP units (Figure A2). From July onwards
found in the corners of the raft culture (Figure A4), probably resulting from insufficient aeration, and 
regular cutting of the roots in the NFT channels was necessary. Inside the channels, increasing root
in the NFT channels under the coconut fiber slabs (Figure A5). 
biomass was Nile tilapia larvae were obtained from Til‐Aqua International (Velden, The Netherlands). On 12 
blocking the water flow, causing leakages, and clogging the pipes. The roots were cut on
both sides of the channel over a period of a few days to cause less stress to the plants, as shown in
June, each fish tank was stocked with 300 tilapias (approximate 67.8 g per fish). The fish were fed ad 
Figure A3.libitum (i.e., to apparent satiation) three times a day (8:00, 13:00, and 17:00) with a swimming pelleted 
Rotten roots were observed after removing roots from the raft culture and NFT channels in
feed (Table A2). While nutrient uptake by the tomato plants remained more or less stable after 12 
November. The most damaged roots were found in the corners of the raft culture (Figure A4), 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 (Table 1) 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 (Table 2) [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 H2 O2 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 H2 O 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 × A503 × V
Lycopene mg·kg−1 = (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:H2 O, 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 µL H2 O and 50 µL of FCR (Folin-Ciocalteau, 10%). After 1 min, 80 µL
Na2 CO3 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 (Table 3). 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 (Table 2) 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 Fruit Quality Parameters 
Internal Fruit Quality Parameters
The fruit sugar content was at its lowest in June, and significantly highest in the August harvest
The fruit sugar content was at its lowest in June, and significantly highest in the August harvest 
(Figure 4A). The significantly highest sugar content was measured in the NFT system, and the lowest
(Figure 4A). The significantly highest sugar content was measured in the NFT system, and the lowest 
in in the drip irrigation system (Figure 4A). The sugar content of the fruits from commercial HP control 
the drip irrigation system (Figure 4A). The sugar content of the fruits from commercial HP control
was in the same range as for the drip irrigation. The fruit sugar content of the October harvest was not
was in the same range as for the drip irrigation. The fruit sugar content of the October harvest was 
measured because of low number of fruits and other fruit analyses were prioritized. Fruit pH (acidity)
not measured because of low number of fruits and other fruit analyses were prioritized. Fruit pH 
was significantly
(acidity)  lowest in thelowest 
was  significantly  October harvest.
in  the  Pronounced
October  differences between
harvest.  Pronounced  the HP
differences  systems
between  the were
HP 
only observed in the first harvest, when the raft culture showed significantly higher fruit pH values
systems were only observed in the first harvest, when the raft culture showed significantly higher 
than NFT (Figure 4B).
fruit pH values than NFT (Figure 4B). 

 
Figure 
Figure 4.  Fruit 
4. Fruit internal 
internal quality 
quality parameters 
parameters sugarsugar  content 
content (A); pH
(A); fruit fruit 
(B);pH  (B);  sugar–acid 
sugar–acid ratio (C);ratio  (C); 
lycopene
lycopene  content  (D);  total  phenolic  compounds  (E);  and  oxygen  radical  absorbance 
content (D); total phenolic compounds (E); and oxygen radical absorbance capacity (F) compared for raft capacity  (F) 
compared 
culture, for  raft  culture, 
drip irrigation, nutrientdrip 
film irrigation,  nutrient 
technique (NFT) andfilm  technique 
a control group(NFT)  and  in
cultivated a  acontrol  group 
commercially
cultivated in a commercially operated hydroponic system at three sampling points in summer. Error 
operated hydroponic system at three sampling points in summer. Error bars represent standard
bars  represent 
deviation. Differentstandard 
uppercasedeviation.  Different 
and lowercase uppercase 
letters indicateand  lowercase 
significant letters  (Tukey’s
differences indicate  significant 
HSD, n = 3,
differences  (Tukey’s  HSD,  n  =  3,  p  <  0.05)  for  harvests  and  hydroponic 
p < 0.05) for harvests and hydroponic systems, respectively. The factors, harvest (H) and systems,  respectively. 
treatmentThe 
(T),
andfactors, harvest (H) and treatment (T), and their interaction (H*T) were reported by “***” for p < 0.001, 
their interaction (H*T) were reported by “***” for p < 0.001, “*” for p < 0.05 and “.” for p < 0.1.
“*” for p < 0.05 and “.” for p < 0.1. 
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 (Figure 4C) 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 (Figure 4D), 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 (Figure 4E). 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 (Figure 4F). 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 (Figure 5). 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 (Table 4).
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 (Table 5).

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 
market tomatoes produced in Switzerland (CH) and in The Netherlands (NL) compared to the average
harvest in the aquaponic system. Error bars represent standard deviation; n = 4. 
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 Productivity and Vitality Parameters
No significant differences were observed in dry matter fraction between the HP systems. Whole 
green biomass results showed no significant differences in the fresh weight between the HP systems. 
No significant differences were observed in dry matter fraction between the HP systems.
There was a difference between the fraction of dry matter of the whole tomato plant at the beginning 
Whole green biomass results showed no significant differences in the fresh weight 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%. There were no significant differences in green cut between the HP systems. Plant height
experiment (data not shown). The average plant length of the aquaponically grown tomatoes was 6.7 
constantly increased during the season with no significant differences between the HP subunits at
m. The weekly growth rate decreased slightly over time and the average growth rate was 22 cm per 
the end of the experiment (data not shown). The average plant length of the aquaponically grown
week. 
tomatoes was 6.7 m. The weekly growth rate decreased slightly over time and the average growth rate
The fractional distribution of nutrient content (C, N, P, K, Ca, Cu, Mg, Mn, Zn, and Fe) of the 
tomato 
was 22 cm per fruits 
week.and  green  biomass  in  the  total  output  of  the  HP  subunits  is  presented  in  Figure  6. 
Statistical 
The analysis 
fractional only  showed 
distribution significant 
of nutrient differences 
content (C, N,in 
P, the  amount 
K, Ca, of  Mn 
Cu, Mg, between 
Mn, Zn, and the Fe)
drip 
of the
irrigation  and  the  floating  raft  systems.  Overall,  there  was  an  obvious  difference  between  the  raft 
tomato fruits and green biomass in the total output of the HP subunits is presented in Figure 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.
Water 2016, 8, 533
Water 2016, 8, 533  12 of 21
12 of 21 

100%

90%

80%

70%

60%

50%

40%

30%

20%

10%

0%
NFT channel

NFT channel

NFT channel

NFT channel

NFT channel

NFT channel

NFT channel

NFT channel

NFT channel

NFT channel
Drip irrigation

Drip irrigation

Drip irrigation
Raft culture

Drip irrigation
Raft culture

Drip irrigation
Raft culture

Raft culture

Drip irrigation
Raft culture

Drip irrigation
Raft culture

Raft culture

Drip irrigation
Raft culture

Drip irrigation
Raft culture

Drip irrigation
Raft culture
C N P K Ca Cu Mg Mn Zn Fe
Green biomass Tomato fruits
 
Figure 6. Distribution of total nutrient uptake in the plant in terms of tomato fruits and green biomass
Figure 6. Distribution of total nutrient uptake in the plant in terms of tomato fruits and green biomass 
in the aquaponic system compared between drip irrigation, raft culture, and nutrient film technique
in the aquaponic system compared between drip irrigation, raft culture, and nutrient film technique 
(NFT) system; n = 3.
(NFT) system; n = 3. 

The significantly highest leaf chlorophyll contents (SPAD) were observed in August (Figure 7). 
The significantly highest leaf chlorophyll contents (SPAD) were observed in August (Figure 7).
However, 
However, onlyonly inin  June, 
June, diddid  measurements 
measurements show 
show significant 
significant differences 
differences between 
between the systems,
the AP AP  systems, 
when
when  the  NFT  system  had  significantly  higher  values  than  the  raft  culture  grown  tomatoes. 
the NFT system had significantly higher values than the raft culture grown tomatoes. The commercially The 
commercially  grown  tomatoes  were  similar  to  the  raft  culture  in  June  and  lower  in  August.  In 
grown tomatoes were similar to the raft culture in June and lower in August. In October, the relevant
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 
uppercase and lowercase letters indicate significant differences (Tukey’s HSD, n = 3, p < 0.05)
Different= 3, p < 0.05) for harvests and HP systems, respectively. The factors, harvest (H) and treatment (T), 
for harvests and HP systems, respectively. The factors, harvest (H) and treatment (T), and their
and their interaction (H*T) were reported by “***” for p < 0.001 and “**” for p < 0.01. 
interaction (H*T) were reported by “***” for p < 0.001 and “**” for p < 0.01.
3.4. Plant Nutritional Status (Leaf Mineral Analysis) 
In terms of leaf mineral concentrations, significant differences were found between the harvests 
3.4. Plant Nutritional Status (Leaf Mineral Analysis)
for all nutrients (Table 6). Significant differences between the HP subunits were only observed for C 
In terms of leaf mineral concentrations, significant differences were found between the harvests
and Mn. The NFT system had significantly higher C concentrations throughout the entire growing 
for all nutrients (Table 6). Significant differences between the HP subunits were only observed for C
period, while the raft culture system had significantly lower C concentrations in the leaves. The drip 
irrigation system did not differ from the NFT and raft culture systems. Significant differences in Mn 
and Mn. The NFT system had significantly higher C concentrations throughout the entire growing
concentrations were observed between the HP systems. The raft culture had the highest and the drip 
period, while the raft culture system had significantly lower C concentrations in the leaves. 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 irrigation the 6. 
Table  lowest mineral
Average  nutrient
leaf  mineral  concentrations
concentrations  in the for 
(±SD)  shown  leaves. The harvests 
the  three  NFT system values were
and  the 
corresponding ANOVA results. Different letters indicate significant differences (Tukey’s HSD, n = 3, 
between the other two (Table 7).
p < 0.05) for harvests. The effect of 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. 
Table 6. Average leaf mineral concentrations (±SD) shown for the three harvests and the corresponding
ANOVAMineral Nutrient 
results. Different letters indicate significant
1st Harvest  2nd Harvest differences (Tukey’s HSD,
3rd Harvest n = 3, p < 0.05) for
ANOVA Result 
harvests. TheC (mg∙g−1) 
effect of 322.3 ± 12.1 
factors (harvest (H)A  and368.7 ± 6.7  B  and
treatment (T)) 365.0 ± 8.2  B 
their interaction H: *** 
(H*T) 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 Nutrient S (mg∙g−1)  1st Harvest
8.3 ± 1.2  A  2nd Harvest AB 
22.0 ± 1.7  3rd Harvest
23.3 ± 5.1  B  ANOVA Result
H: **, HxT: . 

C (mg·g ) 1 Mg (mg∙g −1) 
322.3 ± 12.1 2.7 ± 0.6 
A B  5.7 ± 0.6 
368.7 ± 6.7 B A  6.0 ± 1.0 
365.0 ± 8.2 A  B H: ***  H: ***
N (mg·g−1 ) Fe (μg∙g
−1) 
30.3 ± 0.6 22.7 ± 5.5 
A C 37.0 99.3 ± 17.8 
± 1.0 BB  191.0 ± 116.5 
36.0 ± 1.0 A  B H: ***, T: .  H: ***
P (mg·g−1 ) Ca (mg∙g 1.8−1) ± 0.4 20.7 ± 3.2 
A AB 3.7 ±45.0 ± 6.9 
0.6 BA  58.3 ± 13.3 
3.3 ± 0.6 B  B H: ***  H: ***
K (mg·g−1 ) Cu (mg∙g 14.7−1) 
± 0.6 2.3 ± 0.6 
B B 39.3 ±15.3 ± 1.5 
0.6 BA  23.3 ± 4.9 
77.0 ± 10.5 A  A H: **  H: ***
S (mg·g−1 ) Mn (μg∙g 8.3−1) ± 1.2 107.3 ± 56.2 
A B 22.0905.3 ± 402.1 
± 1.7 AB A  1308 ± 493.2 
23.3 ± 5.1 A  H: ***, T: ***, HxT: * 
B H: **, HxT: .
Mg (mg·g−1 ) Zn (μg∙g 2.7 ± 0.6 9.7 ± 1.5 
−1) 
B B  5.7 ±
60.7 ± 15.5 
0.6 6.0 ± 1.0 A 
AA  156.7 ± 10.3  A H: ***  H: ***
Fe (µg·g−1 ) 22.7 ± 5.5 C 99.3 ± 17.8 B 191.0 ± 116.5 A H: ***, T: .
Ca (mg·g−Table 7. Average manganese leaf mineral concentrations (±SD) in μg∙g
1) 20.7 ± 3.2 AB 45.0 ± 6.9 A 58.3 ±−113.3 B
 shown for the three harvests H: ***
Cu (mg·g−comparing 
1)
all ±three 
2.3 0.6 hydroponic 
B 15.3 ±Different 
systems.  1.5 A indicate 
letters  ± 4.9
23.3significant  A
differences  H: **
(Tukey’s 
Mn (µg·g−HSD, n = 3, p < 0.05) between HP systems. 
1) 107.3 ± 56.2 B 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  −1 a  94 ± 10.7  ab 
Table 7. Average manganese leaf mineral
2nd (7August 2014) 
concentrations
1302 ± 359  b 
(±SD) in µg·g shown
498 ± 241 
for the three harvests
a  916 ± 404  ab 
comparing all 3rd (16 October 2014) 
three hydroponic systems. Different letters
1870 ± 679  b  indicate significant
1107 ± 592  a  differences
947 ± 533  (Tukey’s
ab  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 TEMPO 4.5
Tilapia Vegi 4.5  Coppens International B.V. (Helmond, NL)
Hokovit, Hofmann Nutrition AG (Bützberg, CH)  13.40
51.19  51.92 13.40 51.96  13.40
Water 2016, 8, 533  17 of 21 
Primo floatTilapico TEMPO 4.5 
37/12 4.5 Coppens International B.V. (Helmond, NL) 
Aller Aqua A/S (Christiansfeld, DK) 13.40 
20.95 13.40 20.93 13.40  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    BioMar Group (Aarhus C, DK) 10.00 10.00 10.00  10.00
Tilapia838F Tilapia 3.0 
3.0 Fish Feed 
BioMar Group (Aarhus C, DK) 
Producer
10.00  10.00 
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 
Leaf and fruit mineral nutrient concentrations of the commercially 13.40  produced
13.40  tomato.
TableTable A3. Leaf and fruit mineral nutrient concentrations of the commercially produced tomato. 
A3.
Tilapico TEMPO 4.5  Coppens International B.V. (Helmond, NL)  13.40 
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 Group (Aarhus C, DK) 
Analysis 10.00  Fruit Analysis10.00 
10.00 
838F Tilapia 3.0  1st Harvest  2nd Harvest 1st Harvest 2nd Harvest  3rd Harvest
Mineral Nutrient
C (mg∙g−1)  1st Harvest 325.0  2nd Harvest
359.0  1st Harvest
403.6  2nd
393.2 Harvest 3rd Harvest
391.7 
Table A3. Leaf and fruit mineral nutrient concentrations of the commercially produced tomato. 
·g−1 ) −1) 
C (mgN (mg∙g 40.0 
325.0 40.0 
359.0 19.8 
403.6 14.3 
393.2 18.8 391.7
·g−1 ) −1) 
N (mgP (mg∙g 40.02.0  Leaf Analysis
40.0
5.0  19.8 Fruit Analysis 
1.6  14.3
4.6  6.3  18.8
Mineral Nutrient 
g−1 )
P (mg·K (mg∙g −1)  2.0
1st Harvest 
24.0  2nd5.0
Harvest 1st Harvest
58.0  1.6
12.9  2nd Harvest 
38.1  4.6 3rd Harvest47.2  6.3
g−1 )C (mg∙g
K (mg·S (mg∙g −1) 
−1)  24.0 325.0 
8.0  58.0
359.0 
25.0  12.9
403.6 
0.5  393.2  1.2 38.1 391.7  1.7  47.2
S (mg·g−1 )N (mg∙g −1)  8.0 40.0  25.0
40.0  19.8 0.5 14.3  1.2 18.8  1.7
Mg (mg∙g−1) −1 2.0  4.0  0.4  1.1  1.2 
Mg (mg·g−1P (mg∙g
) )  2.0 2.0  4.0
5.0  1.6 0.4 4.6  1.1 6.3  1.2
Fe (µgFe (μg∙g
−1) 
·g−1 )K (mg∙g −1)  36.036.0 
24.0 
175.0 
175.0
58.0 
20.7 
20.7
12.9 
40.4 
38.1  40.4 47.2 
60.4  60.4
Ca (mgCa (mg∙g)
−1) 
·g−1S (mg∙g −1)  14.014.0 8.0  41.0 
41.0
25.0  0.3 
0.5 0.3 1.2 0.8 0.8 1.7  1.4  1.4

Cu (mg∙g) −1)  −1)  2.0 2.0  8.0  2.0 
Cu (mg 1
·g Mg (mg∙g 2.0  8.0
4.0  0.4 2.0 1.1 4.4 4.4 1.2  13.2  13.2
Mn (µg ·g−1Fe (μg∙g
Mn (μg∙g) −1)  −1)  336.0 336.0 
36.0  1564.0 
1564.0
175.0  9.0 
20.7 9.0 39.1 
40.4  39.1 60.4  35.5  35.5
·g−1Ca (mg∙g
) −1)  −1)  7.0 7.0 
Zn (µgZn (μg∙g 14.0  58.0
41.0 
58.0  0.3 5.7
5.7  16.4
0.8 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 
Figure 
Figure A2.  Tomatoes 
Tomatoes
A2.September 2014. in in 
allall  hydroponic units
hydroponic units  affected
affected  by 
byblossom‐end 
blossom-end rot rot
disease 
disease at  the 
at end  of 
the end of
September 2014. 
September 2014.
Water 2016, 8, 533 18 of 21
Water 2016, 8, 533  18 of 21 
Water 2016, 8, 533  18 of 21 
Water 2016, 8, 533  18 of 21 

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

 
 
Figure  A5.  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 
irrigation (top). 
Figure  A5.  Rotten  roots  on  the  bottom  of  the  NFT  channels  (bottom);  and  healthy  roots  in  drip 
irrigation (top). 
Figure A5. Rotten roots on the bottom of the NFT channels (bottom); and healthy roots in drip
irrigation (top). 
irrigation (top).
Water 2016, 8, 533 19 of 21
Water 2016, 8, 533  19 of 21 

Water 2016, 8, 533  19 of 21 

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

160
Cumulative yield per hydroponic subunit [kg]

140
140
120
120
100
100
80
80

60 60

40 40

20 20

0 0
Week 20
Week 21
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Week 45
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Week 44
Week 45

RAFT CULTURE DRIP IRRIGATION NFT CHANNEL


RAFT CULTURE DRIP IRRIGATION NFT CHANNEL  
 
Figure Figure A7. Average cumulative yield (n = 3) per hydroponic subunit of all three quality categories 
A7. Average cumulative yield (n = 3) per hydroponic subunit of all three quality categories
Figure A7. Average cumulative yield (n = 3) per hydroponic subunit of all three quality categories 
from the “Wädenswil aquaponic system”, 2014. 
from from the “Wädenswil aquaponic system”, 2014. 
the “Wädenswil aquaponic system”, 2014.
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