Waterborne diseases pose a significant risk in hydroponic crops, especially those caused by some species such as Fusarium, Pythium, and Phytophthora. However, there is evidence of an increase in suppressiveness when using aquaculture effluents, as is the case with aquaponics systems.
Introduction
One of the main problems that appear in intensive monocropping systems, where the same cultivation is repeated continuously over time in the same plot, is the rise of soil-borne diseases (De Cal et al., 2005). In crops such as strawberries, the high incidence of these diseases has led to widespread use of soil disinfection practices. In this sense, fumigation of the soil with methyl bromide has been relied on to avoid the attack of pathogens in these crops. However, this practice has been prohibited due to its environmental risks (European Commission, 2009).
Until now, dazomet, metam sodium and metam potassium (methyl isocyanate generators) were soil fumigants authorized in the Andalusian Integrated Production Regulations for strawberry, raspberry, and blackberry. However, they did not pass the uniform principles established by Regulation (EC) No. 1107/2009 in a recent revision. Hence, the authorisation for its use was canceled by the General Directorate of Health of Agricultural Production.
Also, 1,3 dichloropropene and chloropicrin, or their mixtures, are subject to the concession of exceptional uses by crop, area, and problem. Furthermore, this concession is currently subject to various appeals. Therefore, with the current regulatory situation, and except for temporary authorizations, farmers lack chemical alternatives for soil disinfestation, which can compromise the productivity of these crops and their economic viability, in cases of high infestations by soil pathogens (Greco et al., 2020).
In order to reduce the negative effects of soil-borne diseases for certain crops, a significant increase in production has been observed in soilless and hydroponic systems, which allow greater control of plant health regardless of soil quality, while required nutrients are provided to plants with fertigation (Martínez et al., 2017).
By using a hydroponic system, a controlled amount of water and nutrients lead to high growth rates (Mattson and Heinrich, 2019), reducing at the same time the chemical inputs (Askari-Khorasgani and Pessarakli, 2020).
However, the change from soil-based production to hydroponic systems could lead to a significant risk of the occurrence of other pathogens especially adapted to aquatic environments, among which the Fusarium, Pythium, and Phytophthora species stand out since they could be easily spread through the recirculating fertilizer solution.
Particularly, the last two species, formerly considered chromista and currently classified in the Phylum 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 cactorum is 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 oxysporum is 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 pathogenic F. 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:
- competition for nutrients and niches
- parasitism
- antibiosis
- 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 hydroponics, 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 continuously flows from one to the other (Palm et al., 2019), or in multiple loops, in decoupled systems, where the flow goes just in one direction, from fish tanks to hydroponic beds (Goddek et al., 2019). With this synergistic combination, savings in fertilizers and water are achieved, 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, temperature, 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 phytosanitary treatments, facilitating the cure of potential emerging diseases (Goddek et al., 2019). On the contrary, in coupled aquaponic systems, which are commonly utilized in small-scale facilities, the use of pesticides to control plant diseases is not appropriate as they may affect fish or biofilter bacteria.
Recent articles raise an interesting hypothesis about a natural protective action of aquaculture or aquaponic effluents against plant 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 that is less favorable 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 (Stouvenakers et al., 2019).
The results of international surveys on aquaponics production 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 pathogens can affect both fish and plants (Mori and Smith, 2019). For instance, an outbreak of Fusarium 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 suppressiveness of Pythium aphanidermatum. Therefore, it could be very useful to determine the potential improvements against diseases achieved in the real conditions of aquaponic systems in relation to hydroponic production.
For this reason, the following study is proposed. Its main goal is to compare the suppressive effects of these two culture systems for two pathosystems: P. cactorum –strawberry- and F. oxysporum f. 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 environmental 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.
Discussion
For the strawberry – P. cactorum pathosystem 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 (Stouvenakers et al., 2019). In our case, despite crown rot suppressiveness being reported in strawberry hydroponic crops (Martínez et al., 2010), a higher and significant rate was confirmed at early stages in aquaponic systems.
Given that the NFT lines and environmental 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 potential 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 indicated 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 characterized 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 against Pythium aphanidermatum lettuce 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 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 strawberries 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 tomatoes (Song et al., 2004), wilt due to Fusarium was 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 systems 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 of Pythium aphanidermatum. 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 the water at 20 °C (Bates and Stanghellini, 1984). As another example, Pythium dissotocum caused 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 temperatures for these pathogens, with higher infection and mortality rates as a result of water temperatures being more favorable for pathogen 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 nor P. cactorum was harmful to goldfishes in our tests since no mortality or disease symptoms were observed. In relation to the water chemical parameters, aquaponic systems 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 L−1, in order to maintain the wellbeing of the plants, fish, and bacteria.
The electrical conductivity was kept close to 1500 μS cm−1 in the hydroponic systems, not exceeding 1700 μS cm−1. 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 frequently employed in aquaponic systems.
Conclusions
In view of the present findings, the hypothesis of greater suppressiveness 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 producers 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 pesticides, replacing them with BCAs, would represent a considerable benefit for the environment, as has already been demonstrated with the prohibition of the use of some soil fumigants with notable environmental risks such as methyl bromide. These new findings could strengthen the positioning of aquaponics as a sustainable production technique within the circular economy framework.
Source: Suárez-Cáceres, G. P., Pérez-Urrestarazu, L., Avilés, M., Borrero, C., Eguíbar, J. R. L., & Fernández-Cabanás, V. M. (2021). Susceptibility to water-borne plant diseases of hydroponic vs. aquaponics systems. Aquaculture, 737093.
Useful Article: Aquaponic Plants And Their Phytochemical Content And Quality
