Aquaculture 544 (2021) 737093 2could be easily spread through the recirculating fertiliser solution. Particularly, the last two species, formerly considered chromista and currently classified in thePhylum Oomycota, have a superior advantage in liquid media because they present zoospores that facilitate the development of infection of new hosts within minutes (Postma et al., 2008). Phytophthora cactorumis a soil-borne pathogen that affects numerous herbaceous and woody species. In strawberry crops, it causes crown rot, loss of production, and plant death. The incidence of this disease has been observed also in soilless crops, introduced by infected runner plants and cold-stored plants or contaminated irrigation water (Martínez et al., 2010). Fusarium oxysporumis a fungus that is widespread in different types of soil, presenting some pathogenic strains that affect many important crops around the world, causing significant economic loss since infected plants often collapse and die (Borrero et al., 2017; Juber et al., 2014). Some studies have been carried out to identify the plant growth media that are most suppressive against the attacks of pathogenicF. oxysporum isolates (Borrero et al., 2009). However, despite the ease of dispersion described above for some diseases in aqueous media, a lower incidence has been reported in closed hydroponic circuits. This could be related to microbiological activity and modulated by the type of substrate used and the plant species as a driving factor of the microflora and the hydroponic system (Minuto et al., 2007; Postma et al., 2008; Vallance et al., 2009). In the review by Stouvenakers et al. (2019), the antagonistic microorganisms responsible for suppressive effects in hydroponic systems were grouped in the following categories: 1) competition for nutrients and niches; 2) para- sitism; 3) antibiosis and 4) induction of disease resistance in plants. Trying to improve the sustainability of productions and to adjust to the paradigm of the circular economy, aquaponic systems have emerged as an interesting alternative to hydroponic systems. Aquaponic culture consists of a form of agriculture that combines aquaculture and hydro- ponics, where there is a recirculation of water through both subsystems, taking advantage of the metabolic waste of fish that serves as a nutrient for plants (Somerville et al., 2014). In these systems, both circuits can be connected in a single loop, in coupled systems, where water continu- ously flows from one to the other (Palm et al., 2019), or in multiple loops, in decoupled systems, where flow goes just in one direction, from fish tanks to hydroponic beds (Goddek et al., 2019). With this synergistic combination,savingsinfertilisersandwaterareachieved,while reducing potential polluting discharges from both systems. Commercial large-scale aquaponics facilities are usually designed as decoupled systems, which is a great advantage in terms of management, since it is possible to modify the concentrations of nutrients, tempera- ture and the pH of the water to adjust the values required by the plants without affecting the fish. The fact that there is no water flow from hydroponic to aquaculture circuits also allows the applying of phyto- sanitary treatments, facilitating the cure of potential emerging diseases (Goddek et al., 2019). On the contrary, in coupled aquaponic systems, which are commonly utilised in small-scale facilities, the use of pesti- cides to control plant diseases is not appropriate as they may affect fish or biofilter bacteria. Recent articles raise an interesting hypothesis about a natural pro- tectiveactionofaquacultureoraquaponiceffluentsagainstplant pathogens during in vitro tests (Gravel et al., 2015; Sirakov et al., 2016). This phenomenon seems to be related to the presence of antagonistic microorganisms or inhibitory compounds in fish water. The suppressive action has already been observed in hydroponic systems (Postma et al., 2008). In the case of aquaponics, the presence of dissolved or suspended organic matter could also play an important role in the suppressiveness of some diseases, since it can modulate a microbial ecosystem which is less favourable for plant pathogens. This organic matter in the water comes not only from uneaten food debris and fish faeces, but also from organic plant growth media, root exudates and plant residues (Stouve- nakers et al., 2019). Theresultsofinternationalsurveysonaquaponicsproduction developed in the USA (Love et al., 2015) and Europe (Villarroel et al., 2016) have confirmed a lack of knowledge of producers about plant health and the incidence of plant diseases in the studied systems, as was reported by Stouvenakers et al. (2019). Precisely, one of the challenges of aquaponic farming systems is related to disease control since patho- gens can affect both fish and plants (Mori and Smith, 2019). For instance, an outbreak ofFusarium incarnatum, a grass fungus, could cause severe gill damage and even death to black tiger shrimps (Khoa et al., 2004). Therefore, it is crucial to contribute to increasing knowledge in order to achieve the ideal conditions to improve the suppressive effect of aquaponic systems. Until now, there has been just one bibliographic reference comparing the suppressive effects in pure hydroponic systems and in aquaponic systems (Stouvenakers et al., 2020). However, this was carried out using small raft boxes with 4 lettuce plants to test the sup- pressiveness ofPythium aphanidermatum. Therefore, it could be very useful to determine the potential improvements against diseases ach- ieved in the real conditions of aquaponic systems in relation to hydro- ponic production. For this reason, the following study is proposed. Its main goal is to compare the suppressive effects of these two culture systemsfortwopathosystems:P.cactorum–strawberry-and F. oxysporumf. sp.lycopersici(Fol)–tomato. As far as we know, this is the first time that the severities of two diseases in two crops have been compared between a hydroponic and an aquaponic system in real settings using systems under identical envi- ronmental conditions. This is essential to determine what fraction of the suppressive effect that has been referenced in the scientific literature is due to the presence of fish. 2.Material and methods 2.1.Location of the study and environmental conditions The study was conducted inside a greenhouse located at the School of AgriculturalEngineering(UniversityofSeville,Seville,Spain; 37◦21′6.45“N, 5◦56’12.35”W). Two pathosystems were evaluated in independent studies using the same facilities at different times. The test for the strawberry-P. cactorum pathosystem was performed from November 26, 2018 to April 10, 2019, while the second test for the tomato-F. oxysporumf. sp.lycopersici(Fol) pathosystem occurred between February 13 and May 12, 2020. During trial periods, temperatures inside the greenhouse ranged between 2.6 and 38.1◦C for the strawberry test, and from 7.5 to 39.6◦C for the to- mato test (Fig. 1). The relative humidity varied between 15.9 and 94.9% for the strawberry test, and 20.1% and 93.8% for the tomato test. The water temperature ranged between 9.1 and 24.4◦C in the aquaponic systems and between 10.4 and 26.6◦C in the hydroponic ones for the strawberry test; and between 14 and 25.1◦C in the aquaponic systems and between 13.8 and 26.8◦C in the hydroponic ones for the tomato test. 2.2.Description of the hydroponic and aquaponic facilities. Experimental design Four blocks were determined in order to have four replications. Each of them included a hydroponic and an aquaponic system and their location within the block was decided randomly (Figs. 2 and 3). A Nutrient Film Technique (NFT) system was used both for the hy- droponic and aquaponic production of strawberry and tomato. To do so, 3 m long PVC pipes (0.11 m in diameter) were used, each of which had 28 holes (0.06 m in diameter) where the plants were inserted. The pipes were levelled with a 1% slope in order to allow the proper circulation of water. A thin water layer (0.008 m of depth) was maintained inside the pipes, so the roots were in contact with the water but a correct aeration was ensured. In order to study the dynamics of disease transmission G.P. Su ́arez-C ́aceres et al.
Aquaculture 544 (2021) 737093 3along the lines, each NFT channel was divided into four zones: 0, for the inoculated plants, and 1, 2 and 3 for the zones corresponding to increasing distances from the diseased plants (Fig. 2). In the hydroponic systems, the nutrient solution was pumped by means of a 4000 L h1submerged pump (Boyu FP-4000) from a 60 L sump into the NFT pipe, regulating the flow to the hydroponic line with a stopcock and pouring back to the sump. The aquaponic system was composed of a 250 L fish tank (including an air pump to ensure a correct aeration) sequentially connected to two smaller tanks (50 L each) which acted as a clarifier and a biofilter, discharging fish effluents to the sump of the hydroponic subsystem, identical to the one described above. A stopcock on one of the extremes of a“T”fitting connected to the pump was used for sending 80% of the water from the biofilter back to the fish tank and the remaining 20% of the water to the NFT pipe. Again, the water was collected at the end of the pipe and returned to the sump. The water used for the experiment was obtained from the public network and dechlorinated by aerating it for 48 h prior to recharging the tanks. 2.3.Vegetal material and fish species For the first test, young ‘Fortuna’strawberry plants were provided by the Fresas Nuevos Materiales nurseries (Huelva, Spain). The plants were placed in perlite containers inside a growth chamber (photosyntheti- cally active radiation intensity 280μmol s1m2and 12:12 h of light: dark photoperiod, 25/23◦C) during 2 weeks before being transplanted to the NFT systems. Prior to the second test, tomato seeds (Solanum lycopersicumcv. Roma) were placed in a rock wool seedbed in a growth chamber (photosynthetically active radiation intensity 280μmol s1m2and 16:8 h of light:dark photoperiod, 25/23◦C). After 20 days, a nutrient solution was added to the seedbed in order to speed up the growth of the seedlings (0.5 g L1Peter’s foliar feed 27–15-12, Scotts, Heerlen, The Netherlands). When the seedlings had a height of 6 cm and three to four leaves, they were transplanted to the NFT systems (36 days after seed- ing). Due to the large size of tomato plants, a total of 26 seedlings were introduced in each system. The fish species used in the aquaponic systems wasCarassius auratus Fig. 1.Daily maximum, minimum and average temperatures inside the greenhouse during the experiments: (a) Strawberry-P cactorum; (b) Tomato-Fol. G.P. Su ́arez-C ́aceres et al.
Aquaculture 544 (2021) 737093 4(Goldfish). The fish used in this trial came from the university’s aqua- ponic facilities, located in a nearby greenhouse, where they were initially housed in an IBC tank similar to the models proposed by the FAO for small-scale aquaponics. At the beginning of both trials, 14–15 fish (between 133 and 143 g) were selected in order to achieve a total biomass of approximately 2.0 kg. The fish were placed in a container of 70 L provided with an aerator for each of the 4 aquaponic lines. In order to acclimate the animals to the new environment, water from the destination tank was added to the fish container every 5 min, for a total time of 30 min. Once the pH and temperature values were close to those required, the fish were taken out with a net and placed in the new aquaponic tanks. The fish were fed twice a day with 24.4% protein feed by using the pond stick method (Prodac International S.r.l, Cittadella, Italy). The daily amount of food applied in each tank was calculated as 2% of the total fish weight. This amount will result in a contribution of around 1.14 g of ammonia to the water (Somerville et al., 2014). 2.4.Operation and maintenance tasks For the hydroponic culture, a Hoagland solution (Hoagland and Arnon, 1950) was used to weekly refill the collector tanks. In the aquaponic systems, 0.3 L of chelated iron solution (1%) was directly added to the clarifier tank (EDDHA Sequestrene 138 Fe) every fortnight. The plants were sprayed twice a week with 1% potassium sulphate to avoid possible deficiencies. When the plants started showing manganese deficiencies, they were sprayed with 1% manganese sul- phate once a week. The maximum and minimum water temperature was measured twice a week with a Naterial®digital floating thermometer that worked with solar energy. The electrical conductivity was weekly monitored with an EC-Metro Basic 30 conductivity meter and the pH with a Hanna HI5221 pH meter. When the pH exceeded 7.5, citric acid at 1% was added in order to regain values between 6.5 and 7 for both the aquaponic and the hydroponic systems. The nitrate concentration was measured once a week by means of a Merck Millipore RQFlex reflectometer with a Reflectoquant test strip reader. 2.5.Inoculation of the pathogen and monitoring of the disease For the first test, four isolates ofP. cactorum(P35, P100, P113 and P114) obtained from affected plants in Huelva (Spain) were selected for inoculation. These isolates were stored in the culture collection of the Agronomy Department (University of Seville, Spain), where they were kept in water. Inoculation of the strawberry plants was performed after transplantation into the systems on December 5, 2018. Inoculum was obtained by blending 7 days of growing colonies in V8 agar from which came isolates in 50 mL of sterilised water per plate. The roots of the selected plants were submerged in this suspension during 2 h in the first inoculation and 19 h in the second. Only the first six plants of each line were inoculated. Disease severity was monitored from 15 days after the first inocu- lation until the end of the bioassay and was scored with the relative number of affected leaves per plant (number of affected leaves / total number of leaves). The affected plants were wilted, necrotic or dead. At the end of the test (April 10, 2019), all the plants were removed from the hydroponic system. The monosporic isolate (F14) Fol race 2 isolate used for the second experiment was obtained from a culture collection of the Agronomy Fig. 2.Experimental design and schematics of the hydroponic and aquaponic systems. Blue arrows indicate water flow. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) G.P. Su ́arez-C ́aceres et al.
Aquaculture 544 (2021) 737093 5Department (University of Seville, Spain), where it was kept in a 50:50 glycerol:water (v/v) suspension at80◦C. The pathogenicity of this isolate was previously confirmed. The isolate was grown during 7 days at 25◦C in a culture medium composed of agar, malt extract, asparagine andPeter’sfoliarfeed(AMAP)27–15-12(Scotts,Heerlen,The Netherlands) (Borrero et al., 2009). The plates were scraped with water. The fungal suspension was filtered with cheesecloth, and the conidia were counted with a haemocytometer. The inoculum was adjusted at 105conidia per mL. A natural transmission through water under experimental conditions was induced by including infected individuals close to healthy ones (Mehle et al., 2014). Six plants per line were inoculated one week after being transplanted into the aquaponic and hydroponic culture systems by dipping the roots for 2 h in the prepared fungal suspension. At the end of the experiment (May 12, 2020), a longitudinal cut was performed in the stems in order to measure the relative length of stem with brown xylem as an indicator of disease severity (Borrero et al., 2004). 2.6.Statistical analysis The collected data was analysed with Statgraphics Plus (version 5.1; Statistical Graphics Corp., Rockville, MD, USA, 2002). Data normality was determined by the Shapiro-Wilk test and homoscedasticity by the Levene test. An analysis of the variance of the effect of the culture system (aquaponic/hydroponic) and the position of the plants within the NFT pipe (zones 1, 2 and 3), on disease severity was carried out. A pre- liminary factor analysis was performed to check the significance of the effects of the variables: culture system, plant location, block (1, 2, 3, 4) and the interactions between system x location; system x block; system x location x block. 3.Results 3.1.Strawberry–P. cactorum test The existence of significant differences between the culture systems and the disease severity (P=0.0182) was verified, with the aquaponic system having a greater suppressive effect againstPhytophthoracrown rot disease in the strawberry than the hydroponic system (Fig. 4). On the other hand, the location of plants and block factors and their in- teractions with the culture system factor did not show any significant influence. 3.2.Tomato -Fol test In this test, no external symptoms of the disease were observed in the plants, not even in the ones that had been inoculated with Fusarium. This is why the sampling for vascular damage analysis was delayed, pending the appearance of symptoms. As a consequence, the size reached by the plants was much greater than that initially predicted Fig. 3.Experimental configuration for the studied pathosystems: (a) Strawberry-P cactorum; (b) Tomato-Fol. G.P. Su ́arez-C ́aceres et al.
Aquaculture 544 (2021) 737093 6when the experiment was designed. For this reason, the aquaponic systems were not able to supply an adequate level of nutrients for the proper development of the plants. Once the sampling was done, vascular damage was observed even in apparently healthy plants (Fig. 5). Taking all these considerations into account, there were significant differences between the culture systems and the relative length of the stem with brown xylem (P=0.0091). In this case, the hydroponic system showed a greater suppressive effect against Fusarium wilt in tomato than the aquaponic system (Fig. 6). Likewise, significant differences were found between the location of the plants within the NFT pipe and the relative length of the stem with brown xylem (P=0.0228). Plants located furthest from the entrance of the water (locations 2 and 3) were the most affected by the disease (Fig. 7). On the other hand, the non-significance of the effects of the block factor or its interactions with the culture system factor was verified. Regarding the water chemical parameters of each culture system, the NaCl, electrical conductivity (EC) and nitrate (NO3) values in the hy- droponic systems were extremely higher in relation to the aquaponic system as an effect of the Hoagland solution composition (Table 1). 4.Discussion For the strawberry -P. cactorumpathosystem studied- the results obtained in our trial were consistent with previous works that pointed to a higher suppressiveness of water-borne diseases in aquaponic systems (Stouvenakersetal.,2019).Inourcase,despitecrownrot suppressiveness being reported in strawberry hydroponic crops (Martí- nez et al., 2010), a higher and significant rate was confirmed at early stages in aquaponic systems. Given that the NFT lines and environ- mental parameters turned out to be very similar between both types of production systems, it is likely that this difference found in the incidence of the disease was due to microbiological factors. In this sense, the po- tential capacity of microorganisms for inhibiting plant and fish diseases has been reported in aquaponic production for other pathosystems (Sirakov et al., 2016; Stouvenakers et al., 2020). It is probable that, as Fig. 4.Relationship between the aquaponic system (AS) and hydroponic sys- tem (HS) and the severity (%) at 40 days after inoculation ofPhytophthorain strawberry. Bars with different letters are considered significantly different according to the Tukey Test (P<0.05). Fig. 5.Vascular damage in tomato plant without external symptoms of Fusa- rium wilt. Fig. 6.Effect of productive system (aquaponic system [AS] vs. hydroponic system [HS]) on the relative length (%) of the stem with brown xylem (RLSBX) of the tomato. Bars with different letters are considered significantly different according to the Tukey Test (P<0.05). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Fig. 7.Effect of plants location on the relative length (%) of the stem with brown xylem (RLSBX) of the tomato. Bars with different letters are considered significantly different according to the Tukey Test (P<0.05). (For interpreta- tion of the references to colour in this figure legend, the reader is referred to the web version of this article.) Table 1 Water chemical parameters in the four lines of the aquaponic system (AS) and the hydroponic system (HS). pHNaCl (mg L1)EC (μS cm1)NO3 (mg L1) AS17.23±0.25128.29±30.07273.13±62.6658.43±15.37 AS27.23±0.28114.74±33.70246.16±70.2660.14±24.76 AS37.24±0.29135.77±38.79272.25±47.2259.28±12.66 AS47.32±0.26126.74±28.35267.50±57.8245.57±13.49 HS17.08±0.67697.69±296.561412.56±583.64502.44±270.98 HS27.28±0.59583.09±261.841183.06±518.82439.78±259.27 HS37.13±0.72627.44±271.831273.19±538.39447.44±281.41 HS47.11±0.78728.94±348.391474.94±686.23463.55±275.22 G.P. Su ́arez-C ́aceres et al.
Aquaculture 544 (2021) 737093 7indicated by the aforementioned authors, the suppressiveness is due to several factors acting simultaneously, the most important being organic matter in suspension (very low in hydroponic systems) and microbial activity. Although the microbiological population in both production systems was not characterised in our trial, Stouvenakers et al. (2020) concluded that the diversity and composition of the root microbiota were significantly correlated with the suppressive effect of aquaponic water againstPythium aphanidermatumlettuce root rot disease. In the case of the second pathosystem studied (tomato - Fol), the results were totally opposite, resulting in a higher severity of the disease for aquaponic systems. As discussed above, tomato plants did not show any of the characteristic symptoms of Fusarium wilt in the early stages, such as stunting, loss of cotyledons and developing leaves, yellowing, wilting or stem necrosis (McGovern, 2015). Moreover, the measurement used to determine the disease severity in this case (the relative length of the stem with brown xylem) did not allow a constant monitoring and was performed in a later stage of the development of the disease. Therefore, the possible lower incidence in early stages observed for strawberry could not be checked. In fact, the stage of the growing period seems to be an influencing variable. In a study involving the hydroponic growth of tomato (Song et al., 2004), wilt due toFusariumwas reported to be most severe in the intermediate or late growth stage of the growing period (90–120 days). For this reason, the duration of the trial was longer than initially expected, so the size of the plants increased and with it their nutritional requirements. This situation led to an imbalance in the aquaponic sys- tems which were unable to provide adequate levels of nutrients to the plants. As a consequence, these plants suffered a nutritional deficit that made them more sensitive to Fusarium wilt (Borrero et al., 2004). Hence, the hydroponic plants being better nourished, could be more resistant to biotic or abiotic stresses. This effect was also observed by the fact that the disease severity was lower in the plants near the entrance of the water with the nutrients (location 1), despite being closer to the inoculated plants (location 0). The physicochemical conditions intervene in the level of infection and mortality caused by pathogens. As is the case ofPythium aphani- dermatum.This produced 100% mortality in spinach that was grown in water at 30◦C, but 0% of mortality was observed in crops that were in water at 20◦C (Bates and Stanghellini, 1984). As another example, Pythium dissotocumcaused the wilting of 100% of the plants when the water was at 30◦C compared to the 69% that wilted when the water was at 20◦C (Bates and Stanghellini, 1984). These differences in disease prevalence and severity are likely related to optimal growth tempera- tures for these pathogens, with higher infection and mortality rates as a resultofwatertemperaturesbeingmorefavourableforpathogen development (Mori and Smith, 2019). In our study, the maximum values of water temperature reached 25.1◦C in the aquaponic system and 26.8◦C in the hydroponic system, therefore below 30◦C. There are studies that have identified that diseases in aquaponic systems can affect both fish and plants (Khoa et al., 2004; Mori and Smith, 2019). However, neither Fol norP. cactorumwere harmful to goldfishes in our tests since no mortality or disease symptoms were observed. In relation to the water chemical parameters, aquaponic sys- tems remained within the limits recommended by the FAO (Somerville et al., 2014), with a pH between 6 and 7 and a nitrate concentration between 5 and150 mg L1, in order to maintain the wellbeing of the plants, fish and bacteria. The electrical conductivity was kept close to 1500μS cm1in the hydroponic systems, not exceeding 1700μS cm1. Though the recommended pH in which the plants have a greater availability of nutrients is between 5.5 and 6.5 (Domingues et al., 2012), it was kept slightly over those values in order to maintain conditions similar to aquaponic systems. Further studies are required to confirm higher suppressiveness in aquaponic systems compared to hydroponic systems, trying to maintain an adequate balance in the contribution of nutrients in each system. The study of several pathosystems could help to confirm the potential suppressiveness in aquaponic systems. Likewise, it would be interesting to take into account different types of fish, such as tilapia, which is fequently employed in aquaponic systems. 5.Conclusions In view of the present findings, the hypothesis of greater suppres- siveness against water-borne diseases in the specific conditions of our tests is consolidated. Still, additional trials must be designed in such a way as to guarantee an adequate supply of nutrients in both systems. This fact seems to be in line with the low concern of aquaponic pro- ducers concerning plant diseases, compared with other issues such as plant nutrition or pest control. The identification of the microorganisms responsible for this suppressiveness could play a key role in integrated control, incorporating them as biological control agents (BCA) without negative effects on any of the populations that make up these systems or for the consumers of their products. The reduction in the use of pesti- cides, replacing them with BCAs, would represent a considerable benefit for the environment, as has already been demonstrated with the pro- hibition of the use of some soil fumigants with notable environmental risks such as methyl bromide. 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