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Article

Residue from Açai Palm, Euterpe oleracea, as Substrate for Cilantro, Coriandrum sativum, Seedling Production in an Aquaponic System with Tambaqui, Colossoma macropomum

by
José Alexandre Santos da Costa
1,
Fabio Carneiro Sterzelecki
1,*,
Joane Natividade
1,
Rafael José Furtado Souza
1,
Thayanne Cristine Caetano de Carvalho
1,
Nuno Filipe Alves Correia de Melo
1,
Ronald Kennedy Luz
2 and
Glauber David Almeida Palheta
1
1
Programa de Pós-Graduação em Aquicultura e Recursos Aquáticos Tropicais, Instituto Socioambiental e dos Recursos Hídricos, Universidade Federal Rural da Amazônia, Belém 66077-830, Brazil
2
Laboratório de Aquacultura, Departamento de Zootecnia, Escola de Veterinária, Universidade Federal de Minas Gerais—UFMG, Avenida Antônio Carlos 6627, Belo Horizonte 31270-901, Brazil
*
Author to whom correspondence should be addressed.
Agriculture 2022, 12(10), 1555; https://doi.org/10.3390/agriculture12101555
Submission received: 19 August 2022 / Revised: 12 September 2022 / Accepted: 22 September 2022 / Published: 27 September 2022
(This article belongs to the Special Issue Sustainable Aquaculture: Current Perspectives and Future Challenges)
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Abstract

:
The production of high-quality seedlings is important to achieve better productivity in horticulture. Despite being well developed in conventional agriculture, there are few studies on aquaponic systems. The substrate choice in this integrated culture affects plant and economic feasibility. This study verified the effects of using Euterpe oleracea residue as a substrate for Coriandrum sativum seedling production in an aquaponic system with tambaqui, Colossoma macropomum. Five mixtures of Euterpe oleracea offal (0%, 25%, 50%, 75% and 100%) with coconut fiber, nourished by aquaponic wastewater, were evaluated. Water quality, fish and plant performance were analyzed during an 18-day experiment. Although total ammonia decreased from 5.17 mg L−1 to 0.64 mg L−1, nitrite and nitrate did not exceed 1 mg L−1 and 3 mg L−1, respectively. C. macropomum mean weight gain was 118.79 g and achieved high food assimilation, with a 0.86 feed conversion rate. Mean blood hematocrit (30.20 ± 5.99%) and glucose (59.5 ± 10.06 mg dL−1) indicates good physiological status of the C. macropomum. The use of the Euterpe oleracea offal mixture at 50% decreased by half the total fresh mass of Coriandrum sativum, down to 1.12 ± 0.30 g, but did not decrease dry mass (p > 0.05). When the mixture was above 25%, plant and leaf length were 8 cm and 3 cm smaller, respectively, and the number of leaves and stem base diameter were reduced by 34% and 40%, respectively. We do not recommend using more than 25% of Euterpe oleracea offal with coconut fiber for Coriandrum sativum seedling production in an aquaponic system.

1. Introduction

Integrated food production has been increasing in recent decades as an alternative to traditional farming that often threatens the environment. Aquaponics is a soilless culture that combines aquatic animal and vegetable farming, reducing the demand for space and water. It also reduces pollution since the wastewater from aquaculture is used to nourish plants [1]. However, this is a relatively new concept of food production and there is insufficient information about its application for many plant and fish species, mainly at early stages of development.
Seedling growth comprises the stage from emergence of the radicle until the appearance of a sufficient number of green leaves to allow plants to survive independently from stored energy. It is a transition phase, from heterotrophism to autotrophism, influenced by the environment and management practices, and can be carried out directly in soil, or in trays sheltered by greenhouse [2,3]. In soilless culture, alternative organic substrates (e.g., peat, composts, bark and wood residues) or inorganic ones (e.g., gravel, sand, perlite) can be used to produce plant seedlings. The specific composition establishes a physical, chemical and biological environment that can be more or less favorable to seedling vigor and development [4]. The media choice should also consider productivity and cost-effectiveness, since there is no room for excess expenses in aquaponic systems [1].
In this context, regional and low-cost substrates should be evaluated, searching for sources of local sustainability. The Amazon forest is inhabited by a palm species denominated açai, Euterpe oleracea Mart., whose fruit pulp is highly consumed in Brazil and exported to America, Europe and Asia [5,6]. In 2018, 221,000 t were produced, nevertheless the process to extract Euterpe oleracea pulp discards approximately 85% of the fruit, composed of seed and offal ([7,8]. This residue has a significant impact on the Amazon environment, which has recently led to many studies to test the use of discarded seed and offal in civil construction [9,10], animal farming [11] and for use as food for humans [7]. Moreover, previous studies have shown the potential use of Euterpe oleracea residue as substrate in conventional agriculture. The nutrient (5.97 g kg−1 of N, 2.15 g kg−1 of P, 8.13 g kg−1 of K, 1.69 g kg−1 of Ca and 3.02 g kg−1 of Mg) and physical profile showed important nutrients available for vegetable nutrition and support. More than 90% of particles were between 0.5 and 4 mm, pH 5.26, conductivity 3.6 mScm−1 and total porosity of 88.89% [12]. However, no studies have been carried out in an aquaponic system possible use.
In this study, we tested the effects of the use of Euterpe oleracea offal substrate on cilantro, Coriandrum sativum, seedling production in an integrated aquaponic system with tambaqui Colossoma macropomum, an important commercial species to Amazon basin and the second most produced in Brazil [13].

2. Materials and Methods

The experiment was carried out at the Universidade Federal Rural da Amazônia, Belém, Pará, Brazil (Lat. 1°27′30″ S and Long. 48°28′12″ W), in a greenhouse environment of 96 m2 and 3 m high covered by low-density polyethylene (150 µm). All procedures were approved by the Committee for Ethical Animal Use of the Universidade Federal Rural da Amazônia (CEUA/UFRA), protocol number CEUA 1457260820.

2.1. Experimental Design

The experimental unit (Figure 1) used a deep-water technique composed of a 3000 L fish tank, a 250 L settling tank and a 100 L sump filled with substrate for nitrifying bacteria (600 plastic cups, 50 mL, 64.68 cm2, and 76 commercial bioball biofilters) and a water pump with a capacity of 3000 L h−1. Dechlorinated tap freshwater was pumped equally (45 L h−1) to five plant bed each 0.72 m wide, 1.62 m long and 0.10 m tall. To maintain high levels of dissolved oxygen, air was supplied in fish tank by 0.38 cv Blower (ASTEN, SP, Brazil).
Commercial Coriandrum sativum seeds var. Verdão (Feltrim® Farroupilha, RS, Brazil) were sown in polystyrene trays with 128 cells, ten seeds per cell. Two polystyrene trays were used per treatment, filled with five different substrates, composed of increasing concentrations of Euterpe oleracea offal (0%, 25%, 50%, 75% and 100%) combined with coconut fiber substrate (GOLDEN MIX, Artur Nogueira, SP, Brazil). The seeds were irrigated with tap water for 3 days until germination, when they were transferred to vegetable bed, one treatment per bed, and the experiment started.
Experimental fish were cultivated in an intensive aquaponic system with 3000 L, when all fish were measured and weighed, 34 fish with 113.14 ± 67.74 g and 17.95 ± 3.29 cm, to initiate the experiment. They were fed with the commercial feed NUTRIPISCIS STARTER® (45% protein and 9% lipid) at a feeding rate of 5%, three times per day (9:00, 12:00 and 17:00).

2.2. Water and Air Analysis

The air temperature and humidity were measured daily using a digital thermometer and hydrometer (WLXY, HF-2a, São Paulo, SP, Brazil). The water temperature and dissolved oxygen (YSI ProODO, OH, EUA, ±0.01 mg L −1), conductivity (electrical conductivity meter TDS& EC, São Paulo, São Paulo, SP, Brazil, ±2% FS) and pH (pHmeter AKSO®, São Leopoldo, RS, Brazil, ±0.01) were also monitored daily.
Nitrogen compounds were analyzed by collecting water samples from the fish tank, 10 to 30 cm below the surface. They were then filtered through a GF/F 0.7 μm membrane and stored frozen at −20 °C until use w [14]. Water analysis included total ammonia (Bolleter et al. (1961), ±0.03 mg L−1), nitrite (Griess reaction, using APHA [14] methodology, RSD 4%), and nitrate [14] (RSD 1.14%), read at 220 nm/270 nm in spectrophotometry Ionlab, Araucária, PR, Brazil.

2.3. Fish Growth Performance

For growth and survival analysis, the C. macropomum juveniles were counted, measured, and weighed after 18 days, when the study was concluded. A precision balance BEL ± 1 mg (São Paulo, SP, Brazil) was used. Weight gain was obtained by subtracting the final from the initial weight. Feed conversion ratio (FCR) was calculated by: FCR = feed consumption/fish weight gain after 18 days.

2.4. Vegetable Performance

To evaluate Coriandrum sativum performance, fresh mass, dry mass and length of the whole vegetable, leaf and root (n = 20 per treatment) were verified 18 days after transplanting. Weights were acquired using a precision balance BEL ± 0.1 mg (São Paulo, SP, Brazil). In addition, the number of leaves was observed 18 days after being sown. For dry mass analysis, plant, root and leaves were oven dried for 72 h at 65 °C.
Before sown, chemical analyses were carried out at Embrapa Amazônia Oriental using Embrapa methods ([15]; CV < 20%) on the five substrate mixtures, verifying nitrogen (N), phosphorus (P), potassium (K), sodium (Na), aluminum (Al), calcium (Ca) and ion calcium (Ca+), pH (Table 1).

2.5. Blood Analysis

After 18 days, blood samples were collected from 10 fish. Before sampling, fish were starved for 24 h, anaesthetized (with 50 mg L−1 of eugenol Asfer, São Caetano do Sul, SP, Brazil) and 0.5 mL of blood was drawn from the caudal vein. To prevent blood clotting, one drop of EDTA 10% (Hemstab®, Lagoa Santa, MG, Brazil) was added into a syringe. Although one aliquot of blood was used to determine the hematocrit percentage by the microhematocrit method (de Paiva et al., 2013, 0.66% SE), glucose was measured with a digital glucometer Accu-Chek (Sao Paulo, SP, Brazil, accuracy of 74% and precision of 2.7).

2.6. Statistical Analysis

The data were submitted to the homoscedasticity and normality. For parametric variables, one-way ANOVA and Tukey post hoc tests were used to verify significant differences (p < 0.05). To non-parametric results, Kruskal–Wallis and Dunn’s post hoc test were used to explore significant differences (p < 0.05). GraphPad prism 6, San Diego, USA was used for statistical analysis.

3. Results

3.1. Water and Air Analysis

After 18 experimental days, mean air temperature and humidity in greenhouse (mean ± SD, 34.96 ± 2.09 °C and 77.42 ± 2.18%, respectively) was higher than in the outdoor environment (28.72 ± 1.58 and 54.03 ± 7.14%, respectively). Water temperature was 28.01 ± 0.54 °C. The dissolved oxygen, pH and electrical conductivity of water were 7.25 ± 0.96 mg L−1, 7.10 ± 0.23 and 60.78 ± 10.19 µS cm−1, respectively.
Considering nitrogen compounds, while total ammonia showed a slight reduction during the experimental period, from 5.17 mg L−1 to 0.64 mg L−1 after 18 days, nitrite and nitrate did not exceed 1 mg L−1 and 3 mg L−1, respectively (Figure 2).

3.2. Vegetal Performance

The mixture of an increasing amount of Euterpe oleracea offal with coconut fiber affected Coriandrum sativum growth (Table 2). The total fresh mass and fresh leaf mass decreased at all levels of Euterpe oleracea offal mixture and root fresh mass declined when more than 25% (p < 0.05) was used. Nevertheless, the dry mass parameters were not different (p > 0.05), except for the roots, which decreased by 100%.
In a broad sense, Coriandrum sativum root and leaf length, as well as leaf number and stem base diameter (p < 0.05) decreased when more than 25% of Euterpe oleracea offal was included.

3.3. Fish Growth Performance

No fish mortality or diseases were observed during the experiment. After 18 days, C. macropomum weight was 231.44 ± 93.09 g, a weight gain of 118.29 g, which resulted in a final biomass of 7.87 kg. Mean blood glucose was 59.5 ± 10.06 mg dL−1 and hematocrit 30.20 ± 5.99%.

4. Discussion

The ideal nursery growth media depends on the culture system adopted and this choice can affect seedling growth and quality [16,17,18], since some substrates do not provide a suitable environment with enough water, oxygen, nutrients and physical support for early plant development [3]. In this study, the mixture of Euterpe oleracea offal affected Coriandrum sativum seedling development cultivated in an aquaponic system.

4.1. Water and Air Quality

Coriandrum sativum is a vegetable that requires elevated temperature to achieve optimum growth, above 24 °C [19]. The air and water temperature in this study were maintained high throughout the experiment. The other water parameters were also in an acceptable range, normally found in aquaponic systems. Neutral to slightly acidic water, close to 7, and dissolved oxygen above 5 mg L−1 are normally used to increase plant and fish performance [20,21].
Nitrogen nutrients in aquaponic water are mainly available in organic form, and therefore are not detected by an electric conductivity meter. In the first 3 days, total ammonia was higher than recommended for recirculating aquaculture system, 3 mg L−1 [22], but the non-ionized ammonia (0.045 mg L−1) was lower than the mean lethal concentration [23] determined for tambaqui hybrid species (Colossoma macropomum x Piaractus mesopotamicus) and for juveniles of Colossoma macropomum with LC 50–96 h of 7.76 mg L−1 of NH3 [24]. Therefore, the ammonia and nitrate absorbed by the roots [25] were detected in the water tank at a relative low level that would not affect fish health [22,23], but were sufficient for plants nutritional requirements [20,26].

4.2. Vegetal Performance

Seedlings most often fail due to lack of adequate water for enough time for the seedlings to become established. In a deep-water aquaponic technique water flows continuously to the plants, carrying nutrients from the fish tank. In the nursery phase, it is possible to use a range of growth substrates to establish the first environment. Coconut fiber is increasingly used for seedling production in soilless culture [3], but Euterpe oleracea offal has never been tested in an aquaponic system. In this study, most Coriandrum sativum growth parameters decreased when more than 25% Euterpe oleracea offal was mixed with the coconut fiber. Previous studies on conventional production also showed negative effects with the inclusion of Euterpe oleracea residues in the substrate used for Brassica oleracea seedling production [27]. However, if processed [12] or mixed with other composites [28], Euterpe oleracea residue can be added at higher ratios without compromising seedling growth, an issue that should be tested in aquaponic systems.
The growing media compose the first environment of seedling production, and the quality must be appropriated for seed germination and early plant growth. Coconut fiber is increasingly used as substrate, mainly because its physical properties that increases air space [28]. Coriandrum sativum growth may have been affected by the high Euterpe oleracea offal content in the substrate mixture because of its influence on physical and chemical properties. Previous study showed that Euterpe oleracea substrate has a different particle-size distribution from commercial substrate [27], which may affect pore size, hydraulic conductivity and capillarity [29]. The substrate tension, gas diffusivity and unsaturated hydraulic conductivity has a direct effect on the availability of water, oxygen and nutrients to plant roots. For sub irrigated crops, as adopted in this experiment, the suitability of the substrate for allowing capillary rise is very important for an appropriate distribution of the nutrient solution in the growth media. In addition, substrate pH plays a key role in vegetable nutrition, since it determines the nutrient availability [4,30,31].
Moreover, the use of fresh Euterpe oleracea offal in conventional agriculture resulted in negative seedling performance, probably due to the toxins released by substrate decomposition [27]. However, when Euterpe oleracea offal was previously fermented [32], it was possible to add higher concentration into substrate, up to 75%, without deleterious development of tomato, Lycopersicon esculentum, seedling. Further studies should be carried out on the chemical, physical and biological properties of Euterpe oleracea offal to define the best strategy in aquaponic systems.

4.3. Fish Performance

After 18 days, no mortality and high growth of Colossoma macropomum were observed, which corroborates other studies of recirculating aquaculture systems [33,34], confirming the potential for their cultivation in an aquaponic system [35]. In this study, the daily weight gain (6.57 g day−1) was similar to the yield achieved in recirculating aquaculture system (6.42 g day−1) [36], but lower than Colossoma macropomum performance developed at same stage in pond, when reached 7.50 g day−1 [37] and 9.34 g day−1 [38]. The low feed conversion ratio of 0.86 indicates good assimilation in closed culture as shown in previous study [39].
Fish blood parameters are broadly used as health biomarkers in aquaculture production and are important for monitoring physiological status [15,40]. In this study, glucose and hematocrit were at similar levels as those found in previous studies of recirculating aquaculture systems, 57.03 ± 10.17 mg dL−1 and 24.00 ± 1.41% [36], which indicates “normal” captivity conditions.

5. Conclusions

To conclude, the Coriandrum sativum seedling performance indicates that Euterpe oleracea offal mixture over 25% should be avoided. More studies are needed to verify the effects of substrate processing (such as fermented, heated, microwaved and soaked) on the chemical and physical properties of the growth media mixture and on the seedling performance in aquaponic systems.

Author Contributions

All authors contributed to the study conception and design, being part of master study of J.A.S.d.C., carried out by J.N., R.J.F.S. and T.C.C.d.C. The manuscript was written by F.C.S. and reviewed by N.F.A.C.d.M., R.K.L. and G.D.A.P. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by CAPES, the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Project no. 88887.200588/2018-00, PROCAD Amazônia. LUZ, R.K received research fellowships from CNPq (308547/2018-7) and from Conselho Nacional de Desenvolvimento Científico e Tecnológico (Project no. 402952/2021-9).

Institutional Review Board Statement

All procedures were approved by the Committee for Ethical Animal Use of the Universidade Federal Rural da Amazônia (CEUA/UFRA), protocol number CEUA 1457260820.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

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Agriculture 12 01555 g001 550
Figure 1. Schematic aquaponic system used in this study composed of (A) 1—fish tank, 2—settling tank, 3—sump filled with plastic media and 4—plant bed. (B) Water is pumped from sump to five plant bed through 1—tube and drained by gravity by 2—tubes flowing back to the fish tanks.
Figure 1. Schematic aquaponic system used in this study composed of (A) 1—fish tank, 2—settling tank, 3—sump filled with plastic media and 4—plant bed. (B) Water is pumped from sump to five plant bed through 1—tube and drained by gravity by 2—tubes flowing back to the fish tanks.
Agriculture 12 01555 g001
Agriculture 12 01555 g002 550
Figure 2. Nitrogen compound levels during the experimental period of 18 days. Total ammonia (NH3), nitrite (NO2) and nitrate (NO3).
Figure 2. Nitrogen compound levels during the experimental period of 18 days. Total ammonia (NH3), nitrite (NO2) and nitrate (NO3).
Agriculture 12 01555 g002
Table
Table 1. Chemical analysis of substrate mixture of Euterpe oleracea offal with coconut fiber substrate (dry matter). (N) Nitrogen, (P) phosphorus, (K) potassium, (Na) sodium, (Al) aluminum, (Ca) calcium and (Ca+) ion calcium and pH.
Table 1. Chemical analysis of substrate mixture of Euterpe oleracea offal with coconut fiber substrate (dry matter). (N) Nitrogen, (P) phosphorus, (K) potassium, (Na) sodium, (Al) aluminum, (Ca) calcium and (Ca+) ion calcium and pH.
Parameter0%25%50%75%100%
N (%)0.030.020.020.020.08
(mg dm−3)
P10787455114
K336336336337337
Na10785644128
(cmolc dm−3)
Al0.390.320.190.240.22
Ca2.921.811.71.151.23
Ca+3.963.263.152.542.48
pH5.455.7565.956.11
Table
Table 2. Coriandrum sativum growth parameters using an increasing concentration of Euterpe oleracea offal substrate with coconut fiber in an aquaponic system after 18 days-experiment.
Table 2. Coriandrum sativum growth parameters using an increasing concentration of Euterpe oleracea offal substrate with coconut fiber in an aquaponic system after 18 days-experiment.
Parameters0%25%50%75%100%
(g)
FLM2.22 ± 0.71 a1.48 ±0.54 b0.69 ± 0.24 d1.01 ± 0.28 c0.98 ± 0.30 cd
FRM1.06 ± 0.28 a0.96 ± 0.40 a0.43 ± 0.21 c0.63 ± 0.20 bc0.69 ± 0.29 b
TFM3.29 ± 0.95 a2.44 ± 0.87 b1.12 ± 0.39 c1.64 ± 0.45 d1.67 ± 0.57 d
DLM0.10 ± 0.02 0.19 ± 0.11 0.21 ± 0.12 0.21 ± 0.12 0.16 ± 0.09
DRM0.07 ± 0.04 ab0.08 ± 0.04 ab0.09 ± 0.05 a0.10 ± 0.05 a0.05 ± 0.03 b
TDM0.17 ± 0.04 0.26 ± 0.16 0.30 ± 0.18 0.31 ± 0.18 0.21 ± 0.12
NL3.10 ± 0.31 a3.0 ± 0.0 a2.07 ± 0.37 b2.03 ± 0.18 b2.0 ± 0.0 b
(cm)
TL26.07 ± 2.96 ab27.13 ± 2.60 a19.13 ± 2.90 d20.63 ± 3.67 cd23.45 ± 3.01 bc
LL12.81 ± 1.21 a11.60 ± 1.70 a8.28 ± 1.01 b8.40 ± 1.84 b9.07 ± 1.03 b
RL13.25 ± 0.82 b15.53 ± 0.03 a10.86 ± 0.74 c12.23 ± 1.51 c14.38 ± 0.35 ab
SBD0.10 ± 0.01 a0.10 ± 0.0 a0.08 ± 0.0 b0.07 ± 0.01 c0.06 ± 0.01 c
Results are shown as mean ± SD (n = 30). Different letters indicate significant difference (p < 0.05); FLM = Fresh leaf mass; FRM = fresh root mass; TFM = Total fresh mass; DLM = Dry leaf mass; DRM = Dry root mass; MST = Total dry mass; NL = Number of leaves; LL = Leaf length; TL = Total length; RL = Root length; SBD = Stem base diameter; % shows the percentage of Euterpe oleracea offal share in the substrate.
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MDPI and ACS Style

da Costa, J.A.S.; Sterzelecki, F.C.; Natividade, J.; Souza, R.J.F.; de Carvalho, T.C.C.; de Melo, N.F.A.C.; Luz, R.K.; Palheta, G.D.A. Residue from Açai Palm, Euterpe oleracea, as Substrate for Cilantro, Coriandrum sativum, Seedling Production in an Aquaponic System with Tambaqui, Colossoma macropomum. Agriculture 2022, 12, 1555. https://doi.org/10.3390/agriculture12101555

AMA Style

da Costa JAS, Sterzelecki FC, Natividade J, Souza RJF, de Carvalho TCC, de Melo NFAC, Luz RK, Palheta GDA. Residue from Açai Palm, Euterpe oleracea, as Substrate for Cilantro, Coriandrum sativum, Seedling Production in an Aquaponic System with Tambaqui, Colossoma macropomum. Agriculture. 2022; 12(10):1555. https://doi.org/10.3390/agriculture12101555

Chicago/Turabian Style

da Costa, José Alexandre Santos, Fabio Carneiro Sterzelecki, Joane Natividade, Rafael José Furtado Souza, Thayanne Cristine Caetano de Carvalho, Nuno Filipe Alves Correia de Melo, Ronald Kennedy Luz, and Glauber David Almeida Palheta. 2022. "Residue from Açai Palm, Euterpe oleracea, as Substrate for Cilantro, Coriandrum sativum, Seedling Production in an Aquaponic System with Tambaqui, Colossoma macropomum" Agriculture 12, no. 10: 1555. https://doi.org/10.3390/agriculture12101555

APA Style

da Costa, J. A. S., Sterzelecki, F. C., Natividade, J., Souza, R. J. F., de Carvalho, T. C. C., de Melo, N. F. A. C., Luz, R. K., & Palheta, G. D. A. (2022). Residue from Açai Palm, Euterpe oleracea, as Substrate for Cilantro, Coriandrum sativum, Seedling Production in an Aquaponic System with Tambaqui, Colossoma macropomum. Agriculture, 12(10), 1555. https://doi.org/10.3390/agriculture12101555

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