Received: 20 January 2018 | Revised: 30 August 2018 | Accepted: 1 September 2018

DOI: 10.1111/are.13840

ORIGINAL ARTICLE

Stochastic modelling of aquaponic production of tilapia

(Oreochromis niloticus) with lettuce (Lactuca sativa) and
cucumber (Cucumis sativus)

Nallely Estrada‐Perez1 | Alfredo Hernandez‐Llamas2 | Javier M. J. Ruiz‐Velazco1,3 |

Iram Zavala‐Leal1,3 | Carlos A. Romero‐Bañuelos3 | Elia Cruz‐Crespo4 |
Cecilia Juárez‐Rossete4 | Delia Domínguez‐Ojeda3 | Antonio Campos‐Mendoza5

1
Programa de Posgrado en Ciencias
Biológico Agropecuarias (CBAP), Abstract
Universidad Autónoma de Nayarit, Nayarit, We propose stochastic models for predicting and analysing the production of tilapia
Mexico
2 (Oreochromis niloticus), lettuce (Lactuca sativa), and cucumber (Cucumis sativus) culti-
Centro de Investigaciones Biológicas del
Noroeste (CIBNOR), La Paz, Mexico vated in an aquaponic system. Fish and plants were cultivated in a shade house
3
Escuela Nacional de Ingeniería Pesquera, using 30, 60, and 90 fish/m3 employing an NFT system. Results from Monte Carlo
Universidad Autónoma de Nayarit, Nayarit,
Mexico simulation showed that higher yields of tilapia and cucumber, as well as larger plant
4
Unidad Académica de Agricultura, sizes, were obtained by stocking at the highest density (90 fish/m3). At this density,
Universidad Autónoma de Nayarit, Xalisco,
with 95% confidence, yields of tilapia varied from 39.60 to 59.26 kg/m3, the final
Nayarit, Mexico
5
Facultad de Biología, Universidad
length of lettuce leaves varied from 13.53 to 28.5 cm, the final length of cucumber
Michoacana de San Nicolás de Hidalgo, plant varied from 119 to 235.3 cm, and biomass of cucumber varied from 0.98 to
Morelia, Michoacán, México
0.99 kg/m2. Regression and sensitivity analyses showed that dissolved oxygen, den-
Correspondence sity, temperature, and electrical conductivity significantly affected the production of
Javier M. J. Ruiz‐Velazco, Escuela Nacional
de Ingeniería Pesquera, Universidad
tilapia; density, nitrites, pH, and temperature influenced lettuce production; ammo-
Autónoma de Nayarit, Nayarit, México. nium, pH, and density affected the production of cucumber plants; and ammonium
Email: marcialj@uan.edu.mx
and density influenced yields of cucumber. The greatest certainty to achieve higher
Funding information yields of large tilapia was found at low densities. For plants, there was more cer-
SEP‐PROMEP (Project Exbecarios), Grant/
Award Number: N/A; CONACYT (F0lNS)/
tainty of harvesting larger products when cultivated with tilapia stocked at the high-
PROYECTOS DE REDES, Grant/Award est density. A preliminary economic analysis of tilapia production showed that net
Number: 194652
revenues ranged from USD$ 18.50 to 81.76 per system, and that the best results
were obtained when using the highest stocking density. We conclude that the mod-
els are useful for predicting and analysing the production of an aquaponic system.

KEYWORDS
aquaponics, cucumber, lettuce, modelling, stochastic, tilapia

1 | INTRODUCTION
Aquaponics has received considerable attention due to its capability
to sustain water quality, minimize freshwater consumption, and pro-
vide a marketable vegetable crop (Adler, Harper, Wade, Takeda, &
Summerfelt, 2000; Danaher, Shultz, Rakocy, & Bailey, 2011, 2013;
Espinosa‐Moya et al., 2016; Graber & Junge, 2009; Lennard, & Leo-
nard, 2005; McMurtry, Sanders, Cure, & Hodson, 1997; McMurtry,
Sanders, Cure, Hodson, Haning et al., 1997; Pantanella, Cardarelli,
Danieli, MacNiven, & Colla, 2011; Pantanella, Cardarelli, Di Mattia, &
Colla, 2015; Shete et al., 2016). The medium‐based hydroponics is

Aquaculture Research. 2018;49:3723–3734. wileyonlinelibrary.com/journal/are © 2018 John Wiley & Sons Ltd | 3723
3724 | ESTRADA‐PEREZ
also the system where the highest number of plant species has been
tested, followed by floating rafts and NFT; lettuce (Lactuca sativa),
water spinach (Ipomoea aquatica), tomato (Lycopersicum esculentum),
basil (Ocimum basilicum), and cucumber (Cucumis sativus) were the
most frequently used species, among others (Maucieri et al., 2018).
The most commonly raised fish were tilapia (Tilapia spp.), orna-
mental fish, catfish (order Siluriformes), perch (Perca spp.), bluegill
(Lepomis macrochirus), trout (Oncorhynchus spp., Salmo spp., Salvenlius
spp.), and bass (Micropterus spp., Morone spp.). Other animals such as
shrimp and prawns (Suborder Dendrobranchiata), crayfish (Astacoidea
and Parastacoidea Families), and carp (Cyprinidae Family) have been
cultivated (Love et al., 2015). Some of the studies in Acuaponia with
NFT, lettuce (L. sativa), and tilapia (Oreochromis niloticus) are those of
Cani et al. (2013); da Silva Cerozi and Fitzsimmons (2016); Delaide,
Goddek, Gott, Soyeurt, and Jijakli (2016), and Goddek et al. (2016).
Kloas et al. (2015) used tomato (L. esculentum) instead of lettuce,
and Sayara et al. (2016) managed Cyprinus carpio with O. niloticus.
Lennard and Leonard (2006) found the NFT system to be less effi-
cient regarding nutrient removal and lettuce yield than the medium‐
based or floating raft system. Schmautz et al. (2016) obtained signifi-
cantly lower tomato production in NFT than in a floating raft system
but not than medium‐based system (Maucieri et al., 2018). Neverthe-
less, NFT appears to be an appropriate technology for aquaponics,
based on capital cost and ease of use (Goda, Essa, Hassaan, & Shar-
awy, 2015; Lennard & Leonard, 2006; Nicoletto et al., 2018).
The bioeconomic analysis is an interdisciplinary approach aimed
at, among other things, optimizing management of control variables,
such as harvesting time, stocking densities, aeration, water flow
rates, and tank size. Allen, Botsford, Schuur, and Johnston (1984)
propose the use of bioeconomics for aquaculture management, and
its principles can be extended to aquaponics. To accomplish this,
modelling production of fish and plants from a specific aquaponic
system is essential.
In this study, we propose stochastic production models for an
aquaponic system containing tilapia, lettuce, and cucumber, taking
into account water quality, nutrient concentrations, and management
of stocking density of tilapia and we provide a preliminary economic
analysis. Primary data from an experiment cultivating tilapia and
plants with the aquaponic system were used to calibrate the models.
Despite its importance, risk management is the least developed
approach in bioeconomics of aquaculture (Llorente & Luna, 2016).
The models derived from this study are intended to be a part of a
bioeconomic model for managing economic risk in future research.
There are no antecedents in the literature of studies modelling pro-
duction of an aquaponic system, using a stochastic approach.
2 | MATERIALS AND METHODS
2.1 | Experimental setting
Tilapia (O. niloticus), lettuce (L. sativa, var. Parris Island), and cucum-
ber (C. sativus var. Carolina) were cultivated in a shade house located
in Nayarit state, Mexico (21°29′56″N, 105°12′00″W) from
ET AL.
September 2014 to January 2015. Masculinized tilapia
(69.72 ± 12.67 g) were obtained from a commercial hatchery and
stocked at 30, 60, and 90 juveniles/m3 in 1 m3 cylindrical plastic
tanks (three tanks per density).
Cultivation was carried‐out in recirculation systems in combina-
tion with an NFT system. Each system covered 9.25 m2 and con-
sisted of 1 m3 polyethylene tank (for tilapia cultivation), one 100 L
solids sedimentation tank, and one‐100L nitrification tank. The NFT
system consisted of six PVC pipes (3 m in length, 10.16 cm in diam-
eter). The dissolved oxygen was controlled using a 1‐Hp blower (Pio-
neer PRB40–510 CE, China). (see Castillo‐Castellanos et al., 2016,
for further details). Each trough contained six lettuce plants and four
cucumber plants. The tilapia growth trial lasted 22 weeks, during
which two cycles of plant production were carried out, 6 weeks for
lettuce and 7 weeks for cucumbers. Pelleted feed (35% and 30%
protein) were daily offered to tilapia in three rations, adjusting the
ration according to tilapia biomass every week (starting with 3.5%
and ending with 1.8% of the fish biomass).
2.2 | Data collection
Tilapia was weighed each week on a digital balance. Survival was cal-
culated by counting dead fish at the end of each week. After
4 weeks, the length of lettuce leaves and length of cucumber stalk
were measured weekly. Harvest weight of cucumbers was measured
with a precision digital balance.
A multiparameter sonde (Pro2030; YSI, Yellow Springs Instru-
ments, OH, USA) was used for monitoring, on a daily basis, water
quality (dissolved oxygen, temperature, and electrical conductivity) in
the tanks and troughs; pH was measured with a potentiometer. Also,
ammonium, nitrites, nitrates, and phosphates were weekly measured
with a spectrophotometer (BioTek, Winooski, VT, USA). Analysis of
variance was conducted with Statistica 6.0 to detect differences in
mean values of fish growth, FCA, final lengths of cucumber plants
and lettuce, nutrient concentrations, dissolved oxygen, temperature,
electrical conductivity, and pH among stocking densities, with signifi-
cance set at p < 0.05.
2.3 | Tilapia production model
Biomass production of tilapia (bt) was calculated, as a function of
time:
bt ¼ wt nt (1)
where wt is mean individual weight and nt is surviving fish at
time t.
Individual weight, in turn, was calculated modifying the model of
Naranjo‐Páramo, Hernandez‐Llamas, and Villarreal (2004), using the
model:
wt ¼ wi þ mt þ Csenð2πt=L þ SÞ (2)
where wi is initial weight, m estimates the absolute growth rate,
C estimates the amplitude of weight variation (deviation) around the
ESTRADA‐PEREZ ET AL.
linear trend, L is the length of the period between minima or maxima
deviations, and S is a parameter for time adjustment.
Surviving individuals (nt) were calculated using the exponential
equation (Gulland, 1969):
nt ¼ n0 ezt (3)
where n0 is the initial fish population and z is the instantaneous
mortality rate.
2.4 | Plant production model
Growth in length of lettuce leaves and cucumber plant was mod-
elled, using the following equation (Serna‐Gallo et al., 2014):
1  kt
Lt ¼ Li þ ðLf  Li Þð Þ (4)
1  kc
where Lt is the length predicted after t time units (e.g., 4, if Lt is
predicted after 4 weeks of cultivation), Li and Lf are initial and final
lengths, k is the rate at which Lt changes from its initial to its final
values, and c is the number of time units at harvest time. The num-
ber of surviving plants as a function of time was calculated using
Equation (3).
2.5 | Cucumber production model
Cucumber weight was only available at the end of each production
cycle, precluding the use of a model to calculate production as a
function of time. Instead, multiple linear regression was used to
establish a relationship between final fruit weight and water quality
variables, concentrations of nutrients, and tilapia stocking density.
2.6 | Parameter estimation
Nonlinear regression in Statistica 6.0 was used to fit Equations (2)
and (4). The following equation was used to estimate mortality rate
(z) of Equation (3):
z ¼ ½Lnðnf =n0 Þ=tc (5)
where nf is the population at harvest time (tc). Simple linear
regression was used to estimate parameters in equation calculating
cucumber fruit biomass.
2.7 | Multiple regression and correlation analyses
Multiple regression analyses were conducted to predict growth
parameters and the instantaneous mortality rate as a function of
water quality, concentrations of nutrients, and tilapia stocking den-
sity (stocking density, hereafter). Accordingly:

tion (6) were modified as follows:
Q ¼a0 þ a1 ðT Þ þ a2 ðDOÞ þ a3 ðpHÞ þ a4 ðCEÞ þ a5 NHþ
4 þ



(6)
a6 NO  
2 þ a7 NO3 þ a8 PO4 þ a9 ðDÞ
where Q is any of the growth parameters (with the exception of
wi, n0 y S) or the instantaneous mortality rate, or final cucumber
| 3725
weight, a0, a1 … a9 are regression coefficients, T is temperature, DO
is dissolved oxygen, EC is electrical conductivity, and D is stocking
density.
The mean values of the predictor variables recorded during the
trials were used for regression analyses. Predictor variables consid-
ered for analysis were those previously resulting significantly corre-
lated with growth parameters and the instantaneous mortality rate.
The backward stepwise regression procedure in Stata 10 software
(StataCorp, College Station, TX, USA) was used for analysis, setting
significance for acceptance or rejection of predictors at p < 0.1. This
procedure uses the method described in Rencher (2002) for auto-
matic analysis of collinearity.
2.8 | Performance of production models
This was assessed by determining whether biomass (tilapia and
cucumbers) or plants’ length calculated in the models was reasonably
comparable to the biomass and lengths recorded at the end of the
cultivation trials. For every case (replicate) in the database, the mean
value of water quality variables, concentrations of nutrients, and
stocking density were used to calculate the corresponding growth
parameter, mortality rate, and cucumber weight, which in turn were
used to estimate biomass at the end of the trial. The calculated bio-
mass was compared with the actual biomass. After analysing all
cases, sets of observed–calculated pairs of biomass values were
obtained for tilapia and plants.
Following Poole (1974), the sets of observed–calculated biomass
were analysed using simple linear regression, fixing the intercept at
zero. A Student's t test was then used to determine whether the
slope of the resulting straight line was significantly different from 1.
When no significant differences were detected, we concluded that
the calculated biomass was comparable to observed biomass and that
model performance was acceptable. The linear regression routine in
Stata 10.0 was used for analysis, setting significance at p < 0.05.
2.9 | Stochastic elements
Randomness in production models was incorporated by using proba-
bility distributions of water quality variables and concentrations of
nutrients that resulted significant in the multiple regression analyses
(Equation (6). When no significant relationships were established
using Equation (6), a probability distribution was directly used for
the corresponding production parameter. Values of water quality
variables, concentrations of nutrients, and production parameters
were used for distribution fitting, using @Risk 5.0 software (Palisade,
Ithaca, NY, USA).
Further randomness was incorporated using the “envelope”
method (Vose, 2001). For this, the deterministic values of Q in Equa-
Qe ¼ Q þ r (7)
where Qe is the stochastic value of parameter, Q and r are the
residual values (residual variability, hereafter) of the parameter
3726 | ESTRADA‐PEREZ ET AL.

calculated from a normal distribution fitted to the residual values T A B L E 1 Water quality variables in tanks used for cultivation of
resulting from the corresponding multiple linear regression. tilapia
Variable Minimum Maximum Mean ± SD
T (°C) 24.22 31.07 27.85 ± 2.64
2.10 | Monte Carlo simulation
DO (mg/L) 3.75 5.54 4.57 ± 0.5
Output probability distributions of tilapia and plants were inferred, pH 7.90 8.46 8.19 ± 0.20
using Monte Carlo simulation. In a first step, values of water quality
EC (mS/cm) 0.57 1.02 0.75 ± 0.12
variables and concentrations of nutrients were sampled from the
NH4+ (mg/L) 0.47 4.62 1.92 ± 1.16
corresponding input probability distributions to calculate Q values in
NO2− (mg/L) 0.95 8.59 4.46 ± 2.6
Equation (6). In a second step, r values in Equation (7) were sampled
NO3− (mg/L) 63.26 289.90 122.29 ± 64.34
from the corresponding residual values distributions and added to Q
PO4− (mg/L) 1.90 10.47 4.01 ± 2.16
values to finally obtain Qe. Correlations between water quality vari-
ables and concentrations of nutrients were taken into account for Note. DO, dissolved oxygen; EC, electrical conductivity.

simulation. Procedures in @Risk 5.0 were used for simulations.

The coefficient of variation (CV = SD/mean) was used as an index T A B L E 2 Water quality variables in troughs used for cultivation
of uncertainty regarding production (Ayyub, 2014). Output probabil- of lettuce and cucumbers
ity distributions of tilapia and plants production were generated cor-
Variable Minimum Maximum Mean ± SD
responding to alternative management schemes of stocking density,
T (°C) 24.23 31.97 27.89 ± 2.77
including experimental and intermediate densities (30, 45, 60, 75,
DO (mg/L) 4.04 5.54 4.66 ± 0.47
and 90 fish/m3).
pH 7.93 9.09 8.26 ± 0.3
EC (mS/cm) 0.58 0.99 0.74 ± 0.12
2.11 | Sensitivity analysis NH4+ (mg/L) 0.46 3.56 1.82 ± 1.05

The relative importance of water quality variables, concentrations of NO2−.(mg/L) 0.81 8.87 4.25 ± 2.48

nutrients, and production parameters in determining the variability in NO3− (mg/L) 36.60 281.90 123.26 ± 65.2

tilapia and plants production was studied using sensitivity analysis.
The multiple regression analysis in @Risk 5.0 served to analyse sen-
sitivity. Accordingly, a high absolute value of a standardized regres-
sion coefficient indicates high sensitivity.
2.12 | Preliminary economic analysis of aquaponics
system
Net revenue and the benefit–cost ratio were used for evaluation of
tilapia production. Income was calculated according to the harvested
biomass and tilapia price and the operating costs: preparation and
maintenance, fertilizer, fry, labour, energy, fuel, feed, and miscella-
neous.
3 | RESULTS
The minimum, maximum, and mean values of water quality variables
and concentrations of nutrients in the tanks and troughs containing
tilapia and plants are shown in Tables 1 and 2.
Results from ANOVA indicate significant differences at the con-
centrations of nutrients (Table 3). The nutrients increased as stocking
density rose, except phosphates, where no significant difference was
detected. The EC significantly decreased as the stocking density of
tilapia increased (Table 3). There were significant differences in the
final weight and FCR among stocking densities of tilapia (Table 4).
Lower stocking rates of tilapia resulted in higher final weight and
FCR (Table 4).
PO4− (mg/L) 1.78 9.60 4.11 ± 2.06
Note. DO, dissolved oxygen; EC, electrical conductivity.
Significant differences were found in Lf of cucumber plants
among stocking densities of tilapia (Table 5). The larger sizes of
cucumber were obtained when using the highest stocking density of
tilapia (Table 5). The results showed high survival of tilapia (>95%),
while the plants of lettuce showed the lowest survival (Table 6).
The curve proposed to describe the growth of tilapia (Equation
(2) yielded significant results, regarding regression ANOVA, and ade-
quately fitted growth data from the three stocking densities (Fig-
ure 1). After week 8, the growth rate declined until weeks 15 and
16 and then increased. At the end of the trial, progressively higher
weight of fish was obtained as stocking density decreased, from
578.5 to 770.5 g per fish. The period of slow growth coincided with
the one when water temperature tended to diminish systematically
(Figure 2).
Significant results and good fits were obtained with Equation (4)
for modelling growth of lettuce and cucumber plants (Figures 3 and
4). Both plants grew larger when receiving water from tanks with
tilapia stocked at the highest density (lettuce, 22.3 cm; cucumber
plants, 238. 1 cm), while plants receiving water from tanks stocked
at the lowest density were smaller (lettuce, 13.0 cm; cucumber
plants, 83. 6 cm).
There were some significant relationships between parameters of
the production models and water quality variables, concentrations of
nutrients, and stocking density. Absolute growth rate of tilapia was
ESTRADA‐PEREZ ET AL. | 3727

T A B L E 3 Results from analysis of variance for water quality variables at different stocking densities of tilapia
Density (fish/m3) Ammonium Nitrites Nitrates Phosphates
30 1.15 ± 0.42a 2.05 ± 0.48a 82.84 ± 6.72a 3.02 ± 0.63a
60 1.70 ± 0.25ab 4.04 ± 0.94a 107.99 ± 27.17ab 4.02 ± 0.52a
90 2.60 ± 0.41b 6.66 ± 0.49b 178.96 ± 25.14b 5.28 ± 1.11a
3
Density (fish/m ) Dissolved oxygen Electrical conductivity Temperature pH
a a a
30 4.96 ± 0.12 0.63 ± 0.03 28.13 ± 1.08 8.27 ± 0.20a
a b a
60 4.49 ± 0.26 0.80 ± 0.04 28.11 ± 1.14 8.23 ± 0.29a
90 4.39 ± 0.08a 0.81 ± 0.04b 27.37 ± 1.25a 8.17 ± 0.23a

T A B L E 4 Results from analysis of variance of final weights and
FCR of Oreochromis niloticus
Density (fish/m3) Weight (g) FCR
a a
30 733.40 ± 24.96 1.36 ± 0.04
60 563.20 ± 23.74 b
1.07 ± 0.05
90 553.96 ± 11.58 b
0.84 ± 0.03
Note. Means ± SE sharing at least one superscript are not significantly
different.
positively influenced by low stocking density and high concentration
of dissolved oxygen, while the amplitude of weight variation around
the linear trend was inversely related to temperature and electrical
conductivity, and the length of the period occurring between minima
or maxima deviations increased when electrical conductivity was
high (Table 7). Mortality rate was not significantly related to any of
the factors analysed.
Larger final length of lettuce was produced as the stocking den-
sity of tilapia increased, and the electrical conductivity and nitrites
decreased. On the other hand, pH, temperature and stocking density
influenced the growth coefficient (Table 8). No significant relation-
ship was detected between the mortality rate and the factors anal-
ysed.
The final length of cucumber plant was positively influenced by
stocking density, while an inverse relationship was found between
the growth coefficient and temperature and ammonium (Table 9).
Mortality increased at high pH (Table 9). Fruit production was posi-
tively influenced by ammonium concentration which, in turn, signifi-
cantly increased as stocking density rose (Table 10).
Performance of production models was found satisfactory after
Student's t test showed that there were no significant differences
between 1 and the slope of a linear model relating observed and cal-
culated biomass (tilapia and fruit) and the final length of the plants
(Figure 5).
Output probability distributions of the final biomass of tilapia,
b length of plants, and biomass of cucumber are shown in Figure 6 for
c the stocking density of 90 fish/m3. With 95% confidence, yields of
tilapia were with a mean of 49.62 kg/m3; final length of lettuce
leaves was 13.53–28.5 cm, and the final length of cucumber plants
was 119–235.3 cm. Biomass of cucumbers was with a mean of
0.989 kg/m2.
Analysis of production variability related to stocking density indi-
cates that uncertainty in tilapia production increased as stocking
density increased, as seen in higher coefficients of variation (Fig-
ure 7a). For the plants, increasing stocking density of tilapia leads to
longer lengths and lower uncertainty (Figure 7b‐d).
Sensitivity analysis indicated that fish production at 90 fish/m3
was mainly affected by dissolved oxygen and absolute growth rate,
while mortality had intermediate importance. The other parameters
and variables had lower relevance (Table 11). The final length of let-
tuce leaves was mainly dependent on its residual variability, nitrites,
and electrical conductivity, while the growth coefficient and temper-
ature had intermediate importance, and the influence of pH was
negligible (Table 11). For cucumber plants, the main factor influenc-
ing final length was its residual variability, and the other parameters
and variables had a negligible influence (Table 11). Variability in
cucumber production was mainly influenced by ammonium and its
residual variability.
The result of the economic analysis showed that net revenues
ranged from USD$ 18.50 (30 fish/m3) to 81.76 (90 fish/m3) per sys-
tem, and the benefit–cost ratio from 1.35 (35.0% gain) (30 fish/m3)
to 1.88 (88.0% gain) (90 fish/m3) (Table 12).

T A B L E 5 Results from analysis of variance of final lengths of cucumber plants and lettuce between densities
Cycle 1 Cycle 2

Density (fish/m3) Cucumber plants (cm) Lettuce (cm) Cucumber plants (cm) Lettuce (cm)
a a a
30 92.00 ± 13.25 16.19 ± 0.93 93.90 ± 7.06 12.66 ± 1.15a
60 118.53 ± 15.40ab 14.76 ± 3.85a 96.07 ± 7.54a 12.67 ± 0.21a
b a b
90 181.70 ± 33.21 18.92 ± 4.04 183.52 ± 36.27 15.44 ± 1.33a

Note. Means ± SE sharing at least one superscript are not significantly different.
3728 | ESTRADA‐PEREZ ET AL.

T A B L E 6 Survival percentage (%) of fish, cucumber plants, and nutrients, and stocking density concurred with what is generally
lettuce known of tilapia cultivation and aquaponic systems, which indicate
3 consistency and reliability of the predictive capacity of the models.
Density (fish/m ) Fish Cucumber plants Lettuce
30 96.67 ± 3.33 77.78 ± 33.92 74.07 ± 26.10 In multiple regression, it is often recommended using significance

60 96.11 ± 1.92 95.14 ± 6.13 55.56 ± 34.83 levels of p > 0.05 to retain relevant predictor variables (Quinn &

90 95.19 ± 1.70 91.67 ± 7.91 70.37 ± 30.46

4 | DISCUSSION
Performance of our production models was satisfactory for predict-
ing biomass of tilapia and cucumbers and length of lettuce and
cucumber plants. This result from the reliability of the growth and
mortality curves and equations derived from multiple linear regres-
sion analysis. We did not find antecedents in the literature on the
use of the growth curves for modelling growth of tilapia and crops.
The curve we propose for modelling the growth of tilapia
accounts for periodic variations in growth rate associated with a
trend in water temperature and adequately fitted growth data corre-
sponding to the three stocking densities. The curve used for mod-
elling plant growth (Equation (2), originally proposed by Serna‐Gallo
et al. (2014) for modelling growth of the Pacific winged oyster (Pte-
ria sterna), was useful for describing the growth of lettuce and
cucumber plants. This model incorporates the so‐called “expected‐
value” parameters (i.e., initial and final length), which directly esti-
mate length values registered in the database rather than asymptotic
or theoretical parameters that lack biological meaning (Ratkowsky,
1986).
In our study, the relationships between parameters of the pro-
duction model and water quality variables, concentrations of
Keough, 2002). We set the significance level at p < 0.10 to lower
the risk of omitting important independent variables. The equations
were considered adequate after determining that working with the
production models satisfactorily calculated biomass of tilapia and
cucumber and length of lettuce and cucumber plants.
Meeting the requirements of fish and plants in aquaponic sys-
tems is not easy, and some products do not receive optimal cultiva-
tion conditions (Somerville, Cohen, Pantanella, Stankus, & Lovatelli,
2014). We decided to test tilapia because it has a wide tolerance to
temperature, pH, and dissolved oxygen and solids (Cantor‐Atlatenco,
2007). Lettuce and cucumber were selected because the trial would
be conducted during the cooler season when temperate tempera-
tures are expected. In general, water quality parameters were ade-
quate for tilapia, but near the tolerance limits for lettuce and
cucumber.
Regression analysis showed that the growth of tilapia was posi-
tively affected by the concentration of dissolved oxygen and nega-
tively affected by stocking density. A minimum of 3 mg/L of
dissolved oxygen is necessary for growth and reproduction of tilapia
(Wheaton, 1982). Dissolved oxygen should be within 3 and 10 mg/L
(CONAPESCA, 2012; ISA, 2007), with an optimum approximating
4 mg/L (Asiain, Fernández, Reta, & Suárez, 2011). Low oxygen con-
centration normally results in diminished feed consumption and fish
growth (Saavedra‐Martínez, 2006). In our study, the concentration
was acceptable, ranging from 3.75 to 5.54 mg/L, which promoted

900
D30
800 D60
D90
700

600
Weight (g)

500

400

300

200

100

F I G U R E 1 Examples of growth curves

0 of tilapia fitted to data sets corresponding
0 5 10 15 20 25
to stocking densities of 30, 60, and 90
Time (weeks) fish/m3
ESTRADA‐PEREZ ET AL. | 3729

32 300
D90
D60
30 250
D30

200
Temperatura (°C)

28

Length (cm)
150
26

100
24

50
22
0
0 1 2 3 4 5 6 7 8
20
0 5 10 15 20 25 Time (weeks)
Tiempo (semanas)
F I G U R E 4 Examples of growth curves of cucumber plant fitted
FIGURE 2 Water temperature in tanks used to rear tilapia to data sets corresponding to stocking densities of 30, 60, and 90
fish/m3 for both production cycles

30
D90
T A B L E 7 Relationships between parameters of the production
D60 model of tilapia and water quality variables and stocking density
25 D30
Model P
m = −2.402333 + 7.51914 DO − 0.1068669 D 0.0015
20
C = 542.1632 − 17.70886 T − 93.24482 EC 0.0031
Length (cm)

L = −8.998705 + 31.3453 EC 0.0397

15 Note. DO, dissolved oxygen; D, density; T, temperature; EC, electrical
conductivity.

10
T A B L E 8 Relationships between parameters of the production
model of lettuce and water quality variables and stocking density
5 Model P
Lf = 23.87876 − 19.90656 EC + 0.1923708 D − 1.165875 0.0134
NO2−
0
0 1 2 3 4 5 6 7 k = −10.32138 + 0.9678007 pH + 0.1125991 T + 0.003914 0.0224
Time (weeks) D

Note. EC, electrical conductivity; D, density; T, temperature.

F I G U R E 3 Examples of growth curves of lettuce fitted to data
sets corresponding to the stocking densities of 30, 60, and 90 fish/
m3 for both production cycles T A B L E 9 Relationships between parameters of the production
model of cucumber plants and water quality variables and stocking
density
growth rate at higher concentrations. This result agrees with the Model P
results of sensitivity analysis, where dissolved oxygen was the most
Lf = 37.96499 + 1.494879 D 0.0007
influential factor in tilapia production.
k = 5.60614 − 0.1376642 T − 0.197745 NH4+ 0.0025
Increasing stocking density affects the growth of cultivated fish
z = −0.5896874 + 0.0741485 pH 0.0086
species adversely (Canario, Condeca, Power, & Ingleton, 1998; Hay-
Note. D, density; T, temperature.
lor, 1991; Jorgensen, Christiansen, & Jobling, 1993; Martin &
Wertheimer, 1989). Tadesse (2007), working with Nile tilapia, found
smaller fish when stocking density increased from 50 to 200 fish/m3. tropical fish with a good growth response at 25°C–32°C (Meyer,
Our results confirm the negative effect of higher density on growth 1998). Below 24°C, physical activity and feed consumption are sig-
rate (Table 5). nificantly lower (Abdelghany, 1996). Abrupt changes in temperature,
Temperature is an important factor influencing the production of such as five °C, negatively affect tilapia, eventually causing mortality
tilapia (Green, Teichert‐coddington, & Hanson, 2000). Tilapia is a (CONAPESCA, 2012). In our study, the temperature in tanks
3730 | ESTRADA‐PEREZ ET AL.

T A B L E 1 0 Relationships between the biomass of cucumbers (B) Electrical conductivity is an indirect indicator of total salt concen-
and ammonium and between ammonium and stocking density (D) tration in water (Gilsanz, 2007). We detected a significant relation-
Model P ship between parameters C and L in the growth equation of tilapia
B = 81.48 × − 310.8* (NH4+)3 0.0007 and electrical conductivity, although we did not find information in
(NH4+)2 + 381.97 × NH4+ − 110.58 the literature on the possible physiological influences of electrical
NH4+ = −0.1304182 + 0.0236274 × D 0.0018 conductivity on tilapia.
Note. B, biomass; D, density. Fish produce considerable waste products, particularly nitrates,
which are readily accessible for plants (FAO, 2014). We found that,
containing tilapia was within the range recommended for cultivation. except for phosphates, nutrients from waste were highest at a stock-
The fish tolerated a gradual change from 31°C to 24°C, although a ing density of 90 fish/m3, giving a positive relationship between
decrease in growth rate accompanied the decline of temperature. stocking density and the final length of lettuce and cucumber plants,
The growth rate was high as long as temperature, regardless of low and cucumber biomass.
or high, remained stable. At the beginning of the experiment, when The final length of lettuce leaves was negatively affected by
the temperature was high and stable, the growth rate was high. nitrites and electrical conductivity. Nitrites concentration in this
After 8 weeks, temperature systematically declined, causing lower study was 4.25 ± 2.48 mg/L, higher than 1 mg/L recommended for
growth rate. After 15 and 16 weeks, when temperature stabilized at aquaponic systems (FAO, 2014), likely impairing plant growth. In our
low values, growth rate recovered. study, the volume of the biofilter, included the clarifier or sedimenta-
We also observed that the values of parameter C in Equation (2), tion tank, was approximately 20% of the cultivation tanks, coinciding
which estimates the decreases and increases in growth rate over with the volumes reported by Valenti, Mallasen, and Silva (1998)
time, were lower when the mean values of temperature (estimated (i.e., 4%–20%). High concentration of nitrites may be a consequence
for the whole cultivation period) in tanks were higher, thus indicating of biofilters not working completely at the maturation stage that is
an overall positive effect of temperature by attenuating growth rate when microbial populations do not readily oxidize all contributions
decay. These results evidence the extreme sensitivity of tilapia of ammonium to nitrites, intervening with the appearance of nitrite
growth response to temperature. We did not find in the literature (Wortman & Wheaton, 1991).
studies reporting the type of growth responses of tilapia we In this study, electrical conductivity was 0.74 ± 0.12 mS/cm,
observed. within ranges recommended for aquaponic systems: 0.3–0.8

(a) 20 (b)
50
Regression y = 1.002x (p = 0.00001) Regression y = 1.063x (p = 0.00001)
45 t-test (p = 0.09) t-test (p = 0.23)
18
Observed biomass (kg/m3)

Observed length (cm)

40
16
35

30 14
25
12
20

15 10
15 20 25 30 35 40 45 50 10 12 14 16 18 20
Calculated biomass (kg/m3) Expected length (cm)

(c)
200 (d)
Regression y = 1.096x (p = 0.00001)
1.8
180 Regression y = 0.983x (p = 0.00001)
t-test (p = 0.27) 1.6 t-test (p = 0.76)
160
Observed biomass (kg/m2)
Observed length (cm)

1.4
140
1.2
120
1
100
0.8
80
60 0.6
40 0.4
20 0.2
F I G U R E 5 Relationships between
0 0
observed and calculated tilapia biomass (a),
0 20 40 60 80 100 120 140 160 180 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8
length of lettuce leaves (b), cucumber
Calculated length (cm) Expected biomass (kg/m2) plants (c), and cucumber biomass (d)
ESTRADA‐PEREZ ET AL. | 3731

(a) (b)
2.5% 95.0% 2.5% 2.5% 95.0% 2.5%
0.08 0.12
39.95 59.25 13.53 28.50
0.07 0.1
0.06
Mean = 49.7
0.08 Mean = 21.36

Frecuency (%)
Frequency (%)

0.05 SD = 5.10 SD = 3.79

CV = 0.10
0.04 0.06 CV = 0.18
0.03
0.04
0.02
0.02
0.01
0 0
30

35

40

45

50

55

60

65

10

15

20

25

30

35
Biomass (kg/m3) Length (cm)

(c) (d)
2.5% 95.0% 2.5% 95.0% 2.5%
0.016 2.5%
119.0 235.3 2,000
0.989278 0.990243
0.014 1,800

0.012 1,600
Mean = 183.73 1,400 Mean = 0.99
Frecuency (%)

Frequency (%)

0.01 SD = 30.66
1,200 SD = 0.0003
CV = 0.18
0.008 CV = 0.0003
1,000
0.006 800
600
0.004
400
0.002 200
0 0
0.9892

0.9894

0.9896

0.9898

0.99

0.9902

0.9904
100

120

140

160

180

200

220

240

260

Length (cm) Biomass (kg/m2)

F I G U R E 6 Probability distributions of final tilapia biomass (a), final lengths of lettuce leaves (b), cucumber plant (c), and cucumber biomass
(d) obtained at 90 fish/m3. Confidence intervals (95%) are indicated

(Nelson & Pade, 2008). Despite this, our results indicate that let-
tuce is very sensitive to total salt concentration, where small
decreases in salt content resulted in a positive effect on plant
growth. Results from the sensitivity analysis confirm this, where
nitrites and electrical conductivity strongly influenced the final
length of lettuce.
A high value of the growth coefficient indicates that the
growth of plants is slow at the start of cultivation, but increases
until the end of the trials. Higher temperatures and pH caused
the slow initial growth of lettuce. The optimum temperature for
lettuce is 15°C–22°C (FAO, 2014) and pH 6.0–6.5 (Aubert, 1997).
In our study, this was 27.89 ± 2.77°C and pH 8.26 ± 0.3, causing
delays in growth response. Although lettuce was not cultivated
under optimal conditions, at the highest density trial of tilapia,
final length was similar to those reported by Somerville et al.
(2014).
The opposite situation was observed for the cucumber plants,
where high temperature and ammonium levels were associated with
low values of the growth coefficient, indicating fast growth at the
start of cultivation. Recommended temperature for cucumber plant
in an aquaponic system is 22–28°C and ammonium <1.0 mg/L (FAO,
2014). Water temperature in our study was within the recommenda-
tions, which resulted in good early growth response. The mean con-
centration of ammonium was 1.82 mg/L, similar to 1.87 mg/L
reported by Kotzen and Appelbaum (2010) at the start of aquaponic
cultivation of tilapia. We did not find reports on specific tolerance of
cucumber to ammonium. According to our results, it appears that
ammonium had no impact on the growth of cucumber while kept at
0.46–3.56 mg/L.
Length of cucumber plants varied from 20 to 200 cm after 55
and 65 days cultivation in aquaponic systems (Somerville et al.,
2014). Our results (82.8–172.5 cm) were achieved in 49 days. There
3732 | ESTRADA‐PEREZ ET AL.

60 (a) 1.2 (b)

Average Average
50 0.104 1
SD SD 0.00030
0.098
Production (kg/m3)

Production (kg/m2)
40 0.8
0.093 0.00038

30 0.088 0.6
0.00053

20 0.084 0.4
0.00088
10 0.2
0.0025
0 0
0 10 20 30 40 50 60 70 80 90 100 0 10 20 30 40 50 60 70 80 90 100
Density (org/m3) Density (org/m3)

30 (c) 250 (d)

Average Average
25 SD
SD 200
0.177
20 0.182
Length (cm)
Length (cm)

0.204 150 0.210

15 0.244 0.248
0.302 100 0.302
10 0.391 0.388
F I G U R E 7 Final production of tilapia
(a), cucumber (b), lengths of lettuce leaves
50
5 (c), and cucumber plant (d) as a function of
tilapia stocking density. Values of the
0 0 coefficient of variation are indicated.
0 10 20 30 40 50 60 70 80 90 100 10 20 30 40 50 60 70 80 90 100
Values of the standard deviation of
Density (org/m3) Density (org/m3)
cucumber biomass are negligible

T A B L E 1 1 Results from the sensitivity analysis of the production was higher mortality of cucumber plants associated with high pH,
of tilapia, lettuce, cucumber plant, and cucumbers to parameters and most likely as a consequence of, as explained previously; pH was
variables (P–V) of the corresponding production models. Regression higher than recommended for aquaponics.
coefficients (RC) are ranked according to absolute values from the
The stochastic production model of tilapia indicated that variabil-
most‐to‐the‐least sensitive
ity in final yields was higher at higher stocking density. Absolute
Tilapia Lettuce
variability (SD) of production increased as a function of density, but
P–V RC P–V RC P–V RC P–V RC the increase in mean yields was not enough to compensate for that
DO 0.81 L −0.06 Lf 0.62 T 0.28 variability, resulting in higher coefficient of variation as density
m 0.48 EC 0.04 NO2− −0.55 pH −0.01 increased. Increase in mean yields was limited because, although
z −0.17 T 0.02 EC −0.49 increasing density resulted in a larger population of tilapia, it also
S 0.07 C −0.01 k 0.34 produced fish of smaller size. This means that there is higher cer-

Cucumber plant Cucumbers tainty in obtaining yields predicted for large tilapia cultivated at low
densities. In contrast, certainty in producing plants and cucumbers
P–V RC P–V RC P–V RC
increased as density increased because the higher concentrations of
Lf 1.0 k 0.01 NH4+ 0.97
nutrients resulted in larger length and weight (i.e., lower values of
NH4+ 0.01 T 0.01 B −0.01
coefficient of variation) of plants and cucumbers. This means that
Note. DO, dissolved oxygen; m, absolute growth rate; z, instantaneous there is more certainty in obtaining the predicted production by
mortality rate; S, L, C are parameters of the growth curve; EC, electrical
managing high densities.
conductivity.

T A B L E 1 2 Operating costs,
Density (fish/m3)
income, net revenue (USD$/
30 60 90 System), and benefit–cost ratio (B/
Costs 53.58 64.82 92.59 C) per cultivation system of tilapia
Income 72.08 95.59 174.35
Net revenue 18.50 30.77 81.76
B/C 1.35 (35.0% gain) 1.47 (47.0% gain) 1.88 (88.0% gain)
ESTRADA‐PEREZ ET AL.
5 | CONCLUSIONS
The proposed models are useful for predicting and analysing experi-
mental results from an aquaponic trial, using a stochastic approach,
which is different than conventional approaches. The models can be
used as part of a bioeconomic model to determine optimal harvest-
ing times and to manage economic risk.
ACKNOWLEDGEMENTS
Ira Fogel of CIBNOR provided valuable editorial services. N.E.P. is a
recipient of a student fellowship from Consejo Nacional de Ciencia y
Tecnología of Mexico (CONACYT). This study was supported by
SEP‐PROMEP (Project Exbecarios) and CONACYT (F0lNS)/PROYEC-
TOS DE REDES (Project Num. 194652).
ORCID
Alfredo Hernandez‐Llamas http://orcid.org/0000-0001-6369-6963
Javier M. J. Ruiz‐Velazco http://orcid.org/0000-0003-1193-2164
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