Aquaponics has the potential to produce sustainable, high-quality food through the integration of hydroponics and aquaculture, but its commercialization is stalled by bottlenecks in pest and disease management. We reviewed integrated pest and disease management steps and techniques in hydroponics to qualify as suitable techniques for different aquaponic designs. Non-chemical prophylactic measures are highly proficient for pest and disease prevention in all designs. Still, the use of chemical control methods remains highly complicated for all systems.
Introduction
The world growing human population will need a further 50% increase in the current food production by 2050 (FAO, 2017). The intensification in food production has resulted in heavy pollution, destruction of habitats, loss of species, and erosion of biodiversity (Tilman et al. 2002; FAO 2017).
There is an eminent interest in shifting the current production model to a more balanced ‘eco-economy’ that recycles nutrients, prevents or reduces waste, and supports dietary changes (Conijn et al. 2018). In this context, sustainable aquaculture methods, which also include practices such as aquaponics, are viewed as an important tool (Tacon et al. 2009).
Aquaponics is considered a sustainable system that integrates intensive fish culture with hydroponic plant cultivation (Rakocy et al. 2004). It allows wastewater from fish to be purified by plants, and then, the purified wastewater may be reused, leading up to >90% water reuse (Tyson et al. 2011; Dalsgaard et al. 2013; Zou et al. 2016).
It produces little or no pollution compared with conventional fish culture systems (Goddek et al. 2015). This further lowers the demand for industrial fertilizers (Rakocy 2007) as compared to agriculture or hydroponic plant cultivation. Despite these benefits, aquaponics still largely remains a ’backyard activity’ rather than the desired commercialization (Monsees et al. 2017a; Mchunu et al. 2018).
This is mainly because substantial doubts still exist, as many key questions about the overall feasibility of aquaponic production remain unanswered (Goddek et al. 2015; Short et al. 2017; Monsees et al. 2017a, b; Lunda et al. 2019). With only a few published surveys available on ground-level realities (Love et al. 2014, 2015; Short et al. 2017; Mchunu et al. 2018), it is often difficult to assess the adoption or success of aquaponics in the commercial context (Monsees et al. 2017b).
One of the core bottlenecks hindering the commercialization of aquaponics is pest and disease management (Pilinszky et al. 2015; Junge et al. 2017; Goddek et al. 2019). Pests such as aphids, spider mites, whiteflies, and fungus gnats and plant pathogens such as bacteria, fungi, and viruses have been reported to cause severe damages to hydroponic plants and reduce yields (Rakocy et al. 2012; Goddek et al. 2019), simultaneously increasing the investments for pest management control.
Depending on the design of aquaponics (coupled, decoupled, with/without mineralization unit; see supplementary material for more details), the use of existing approaches of pest and diseases management often faces restrictions in fear of the possible effects of pesticide, repellent, or biological control agent on the non-targeted system components.
There is an urgent need to establish pest and disease management that is accommodative for different aquaponic designs. To the best of our knowledge, despite having ample practical or theoretical literature on various aspects of aquaponics, technicalities on integrated pest and disease management (IPDM) ‘tailor-made’ for aquaponics have been somewhat overlooked for long.
In the last decade, IPDM has evolved to replace excessive use of pesticides for control of pests and pathogens in both field and indoor agriculture (Greenberg et al. 2012; Schnelle & Rebek 2013). As a sustainable approach, it combines or synergizes preventive, cultural, mechanical, physical, biological, and chemical control methods in established steps to keep pest activities below economic losses (Soloneski & Larramendy 2012; Somerville et al. 2014).
Like in field agriculture, IPDM principles in hydroponics are carried out in chronological steps that stretch from activities before an outbreak of pest/disease to an assessment of the control method applied. These steps include
- Prevention
- Identification of pests
- Monitoring of pest activity
- Determining and selecting control method(s)
- Assessment of the method (Stein 2006).
Hydroponics, being one of the major components of aquaponics, interacts with the rest of the aquaponic system, depending on the design of such a system (Monsees et al. 2016; Monsees et al. 2017a). This interaction would expose other components of the system to any IPDM selected in step 4 above. Hence, for effective IPDM implementation, IPDM steps and decisions taken would have to consider the components of aquaponics design. This aspect of aquaponics remains completely unaddressed.
To address this knowledge gap, we made an exhaustive review of the existing tools of IPDM in aquaponics and discussed them in the context of different aquaponic designs (background information on aquaponic designs has been provided in the supplementary text). To the best of our knowledge, the present review is the first of its kind.
Hence, we investigated the common preventive IPDM techniques and their possible adoption in aquaponics, suitable chronological IPDM steps and methods for different aquaponic designs, and further suggested alternatives for IPDM techniques that are found to be detrimental to aquaponic systems. We further provided an organized strategy inventory that provides technical information on the alternatives and relevant conclusive assessment of the control methods.
System-Specific Dilemmas
We encountered some system-specific dilemmas (i.e. incompatibilities) in the type of pest and disease control methods that can be used.
Coupled aquaponics
The pesticides, repellents, and biological control used during pest and disease infestation of plants in hydroponic units may affect the biofilter bacteria and fish (Rakocy 2007; Rakocy et al. 2012; Stouvenaker et al. 2019). The nutrient recovery in the mineralization unit carried out either by aerobic or by anaerobic microbial digestion of fish sludge can be sensitive to pesticides (Goddek et al. 2015; Stouvenaker et al. 2019), thus affecting the overall nutrient mobilization of the aquaponic system.
On the other hand, fish antibiotic/therapeutic residues used in the rearing unit can be taken up by the plants which can further be transferred to humans (Rakocy et al. 2012). All these can culminate in the end impact, which majorly is the effects on the safety of the final harvests meant for human consumption.
Decoupled aquaponics
In elementary DAPs, the plant water is not reused for fish production. Therefore, the water (if laden with pesticides, repellents, or biological controls) cannot enter the fish culture and mineralization unit either. This design could accommodate more approaches to pest and disease management without much interference with other compartments.
Recent designs of DAPs, however, allow to reuse of the evapotranspiration water from plants via condensation in cooling traps (Kloas et al. 2015; Monsees et al. 2017a) or to treat the hydroponic solution in desalination units (Goddek et al. 2018) before passing on to the fish unit.
However, the transfer of pesticide/repellent via these ‘water recovery’ options is presumably minimized or nullified (Reinhardt et al. 2019). Future research should focus on the residual chemicals (from pesticides/repellents) in the condensate (for cooling traps) or filtrate (for desalinization units) to reinforce the safety claims of DAPs over coupled aquaponics.
Prevention
The rationale behind ‘prevention in aquaponics’ is clarified in the supplementary text. Below, using peer-reviewed articles, we highlighted the potential effects of various prophylactic measures on different aquaponic components.
Replicability issues of general prophylactics in aquaponics
Various prophylactic measures are carried out separately in hydroponics and RAS systems to avoid the infestation of pests, pathogens, or the occurrence of diseases (Stouvenakers et al. 2019). Most of these measures are usually put in place before the emergence of diseases and pests. Their replicability (from hydroponics to RAS or vice versa) in aquaponic systems could be determined by the administration procedure, the nature of the measure, and the type of aquaponics.
Plant compartment And Fish compartment
Hydroponic farmers have developed practices that are regularly taken to prevent pests and disease outbreaks in the system (Goddek et al. 2016). These include:
- General sanitation routine
- Direct treatments
- Environmental manipulation
General sanitation routine includes the use of disinfection mats, specific protective clothes, room sanitization, barrier netting or planting measures such as seasonal fallow period, and use of disease-resistant plant cultivars (Jarvis 1989; Stanghellini 1993; Albajes et al. 1999).
Direct treatments include treatment towards the standing population, for example, water treatments with ultraviolet radiation (UV), heating, slow filtration techniques, or use of chemical sanitary such as cyromazine, chloramines, humic acid, and prochloraz, which are not recommended in coupled aquaponics (Song et al. 2004; Date et al. 2005; Jones 2016).
In environmental manipulation, farmers usually manipulate environmental variables, temperature, pH, humidity, water vapor density, and their interaction. Disease prevalence is generally dependent on these factors (Jarvis 1989). A case example is provided in the supplementary text. This implies that solutions would have to be selected based on the aquaponic design at hand. Those measures which do not involve direct application into the common nutrient water are usually replicable across all aquaponic systems.
In contrast, prophylactic measures needing direct application into process water pose risk, especially in coupled aquaponics. The measures involving environmental manipulation to eliminate target pest or pathogen pose can be overcomplicated at times. The manipulated environmental conditions might be antagonistic to optimum conditions required by fish, biofilter bacteria, or the plants themselves.
Fish compartment and Plant compartment
Similarly, prophylactic measures in recirculating aquaculture system (RAS) include general culture measures (e.g. use of pathogen-free water, tools disinfection, quarantining, use of pathogen-resistant strains and stocking at low density) and substance-based measures (e.g. probiotics, bioremediation, anti-parasitic substances) (reviewed in Assefa & Abunna 2018; Dawood et al. 2019; Lieke et al. 2019).
The substance-based measures might be detrimental in conventional aquaponics due to the residual effects (residues) they could pose a threat to plants, rhizosphere microbiota, final uptake into fruits or leafy vegetables, or mineralization units themselves (Rakocy 2007; Rakocy et al. 2012). Research on this aspect has been meager, and existing knowledge is mostly presumptive or qualitative.
Pest monitoring
Despite several preventive measures underlying, pest and pathogen outbreaks might still be inevitable. Hence, farmers would have to be prepared to carry out further steps of IPM. Pest and disease monitoring are the first steps in IPM. In general, pest location and identification require frequent plant inspection (mainly leaves) (Boissard et al. 2008). One of the most common methods for pest monitoring in the greenhouse is conventional sticky traps (Pinto-Zevallos & V€anninen 2013).
The traditional pest scouting, identification, and counting on sticky cards might be exhausting for large-scale aquaponics (Xia et al. 2015). There are ample studies carried out on the use of automated systems for this exercise (see Cho et al. 2007; Lopez-Morales et al. 2008; Xia et al. 2015).
On the other hand, the aquatic medium of aquaponics creates more room for pathogens such as Pythium, Fusarium, and Phytophthora species (Jarvis et al. 1993; Goddek et al. 2018). Hence, more extensive and frequent plant inspection would be required to early detect potential pests and pathogens in the system.
Farmers should frequently observe for bloom disease symptoms and monitor flies (e.g. fungus gnats, mosquitoes), which might be vectors of plant pathogens (virus, fungi, and bacteria). Besides, seedlings and portions of nutrient solution exposed to light also develop algae, which not only competes for nutrients but also serves as food for shore flies and fungus gnats.
On sighting ‘actual’ pests, correct identification of such pests is the most important step to controlling them (Norris et al. 2003). The correct ’current’ pest identification technique is the most important step in pest control (Norris et al. 2003). Ease of identification of pests might be associated with farmer’s experience or access to the consultation (internet or experts). There are numerous photographic guides on the identification of different pests (Jepson 1987; Blackman & Eastop 2000; Zhang 2003).
Disease monitoring in rearing unit
Furthermore, to establish the health status of an entire aquaponic system, pathogen detection and identification would have to be further extended to the RAS unit of the system. In this respect, the measurement of ammonia and nitrite of water should be carried out at least once a week to establish the efficiency of the biofilter at converting ammonia to nitrate.
Also, fish behaviors such as swimming and response to feeding should be observed daily for unusual behavior. Common places of infections such as eyes, gill filaments, caudal peduncle, and distal ends of caudal and dorsal fins should be frequently observed for signs of diseases.
Besides, key water quality parameters such as dissolved oxygen, pH, and temperature should be tested daily. All these practices are necessary for all designs of aquaponics, and they are of utmost importance to the early detection of pathogens and pests and are not perceived to create any possible negative feedback.
Monitoring pest activity (population level of pest)
After detection and proper identification of the pest, a farmer would need to establish surveillance to determine the level of the detected pest population, and further assess the potential for economic loss (Norris et al. 2003; Abrol & Shankar 2012). This is usually carried out with the use of sticky card traps, light traps, sex pheromone traps, etc. All these methods have been severally reviewed and discussed in Abrol and Shankar (2012) and Miller et al. (2015).
The results from the monitoring activities would inform the farmers on when to initiate a control strategy (if needed), at a point (action/economic threshold), where the cost of yield loss exceeds the cost of given management (Hallett et al. 2014). It is usually expressed as a ratio of ‘cost of control’ to the product of ‘price of produce, loss per yield and reduction in pest attack (Yencho et al. 1986).
Several studies have established an action threshold for pests and different plants (Nault & Shelton, 2010; Ramsden et al. 2017). Hence, the monitoring of pests in aquaponics using the above method(s) is not perceived to pose any further negative effects on other components of the system and would fit in into the IPDM of any design.
Reviewing and selecting a control strategy
The rationale behind reviewing and selecting a control strategy is clarified in the supplementary text.
Cultural control
This is a common, proven approach for agriculture–horticulture yet overlooked in aquaponics so far. Cultural control is practices that are employed before, during, or after planting to prevent pests and diseases (Rodrıguez-kabana & Canullo 1992). These practices range from the selection of disease-resistant crop variety or less succulent plants to crop rotation (Somerville et al. 2014).
Other practices include spacing, companion planting, trap cropping, and fertilization (Somerville et al. 2014; Jones 2016). Furthermore, stunted growth of plants or yellowing of leaves in conventional aquaponics might be attributed to the imbalances in the fish density: plant area ratio.
Thus, the numbers of fish in the rearing unit are usually increased to obtain an improved result in the system or vice versa (Somerville et al. 2014). All these practices are directly non-detrimental to any units of aquaponics, and their clinical adoption would reduce the cost for other control methods.
Some key bottlenecks or disadvantages of cultural controls that can indirectly affect aquaponics are summarized in Cultural and pest monitoring methods are the best first approach to contain pest infestation or disease after they have been detected, because they can be used to keep the pest population below the action threshold (economy injury level), with little or no cost.
Risks of economic loss can be reduced when they are effectively combined with preventive measures. However, since these methods are manipulative strategies, farmers require a good understanding of the system and culture of organisms/plants to plan an effective cultural control method. Otherwise, farmers might have to seek other control methods.
Physical and mechanical control measures
Jet streaming with water (for plant pests). Being the most basic one, it involves actively removing the pests away from the plants by using a high-pressurized ‘jet stream’ of water to wash off the pests on leaves or plants, to minimize their infestation or kill them (Somerville et al. 2014). But the limited penetration of water jets deeper into the canopy to eradicate most of the insect pests is questionable.
Besides, fetching a bulk quantity of water for jetting might be cumbersome for the time taken and expensive especially for large-scale aquaponics (Sakthivel et al. 2011). However, this method is generally adaptable in all aquaponic designs with no foreseeable threat.
Ultraviolet (UV) irradiation (for water-borne pathogens)
UV irradiation which is commonly effective at a wavelength of 200 to 280 nm (Van Os 2009) produces detrimental effects on microorganisms by damaging their DNA and consequently reducing microbial loads by up to 99% (Elumalai et al. 2017; Xu et al. 2018).
Mori and Smith (2019) study found that there is a wide variation in the sensitivity of fish and plant pathogens to UV doses. An example is furnished in the supplementary text. To optimize UV treatment, the recommended turbidity is < 2 NTU (Zheng et al. 2014).
Hence, the prefiltration of nutrient water is usually carried out before the use of UV irradiation to remove the suspended solids. In aquaponics, however, turbidity can be manually reduced by pre-treating the water in gravel or sand-bed unit, where protozoa and algae can also be removed (Bennet 2008).
However, any beneficial bacteria or microbe in the process water will most likely be neutralized as well (Mori & Smith 2019), indicating the overall effects this could have in coupled systems. Results of some specific studies using UV on aquaponic water are compiled in the supplementary text. The technical use of UV sterilizers in aquaponics can be restricted to treating incoming freshwater (water source) to avoid immeasurable effects on the beneficial bacteria and rhizosphere community.
However, the use of UV in aquaponics has not been largely reported to creating a significant problem in the system designs of aquaponics, but their use might be restricted to only large-scale aquaponics which could also be increasing cost at large. Alternatively, an influx of pathogenic organisms in irrigation water sources is sources of pathogens in RAS systems; hence, it would be more cost-effective for farmers (especially small-scale farmers) to use disease-free water sources.
Groundwater sources such as borehole and well water or rainwater have been reported to be more pathogen-free than surface waters such as river or lake water which contain more pathogenic organisms (Steele & Odumeru 2004; Bregnballe 2015).
Ozonation (for water-borne pathogens)
Ozone application is highly effective for the control of microbial and chemical contamination in hydroponics and highly efficient at inactivating pathogens such as Fusarium sp., Phytophthora sp. and Pythium sp. in nutrient solutions (Igura et al. 2004; Schnitzler 2004).
However, it produces oxidative by-products (e.g. reactive oxygen species, free radicals) and a significant amount of residual oxidants (e.g. brominated compound and haloxy anions, OH ) that are toxic to fish (Igura et al. 2004; Goncalves & Gagnon 2011; Graham et al. 2011).
Ozone decomposition which is initiated by pH and temperature leads to the formation of OH and reactions of compounds such as sulfite, nitrite, olefinic aliphatic hydrocarbons, phenols, polyaromatic hydrocarbons, organic amines, and sulfides (Hoigne 1988).
The oxidative property and the resulting reactions or effects of the abovelisted compounds on the standard water quality in aquaponics make the use of ozone in aquaponics dangerous as it poses risk to fish and beneficial bacteria and even humans (Pattillo 2017). Farmers might be compelled to work with experts to develop an ozonation process that fits specifically for a certain design to ensure a high level of safety.
Filtration (for water-borne pathogens)
Filtration in hydroponics involves filtering incoming water or effluent water from particulates such as microorganisms through a granulated or fibrous material (Berkelmann et al. 1995; Boller & Kavanaugh 1995). Filtration techniques majorly used in hydroponics are membrane and slow sand filtration (Ehret et al. 2001). Water flow rate, sand/grain size and genus of pathogen determine the effectiveness of slow sand filtration at removing pathogens (van Os et al. 1999; Deniel et al. 2006).
Fine sand and common grain size of 0.15–0.3 mm might be perceived to be impractical with large capacity aquaponics, but farmers could rather substitute with larger media such as gravel or less fine sand to increase flow rate, but the better result is reportedly obtained with finer sand size. The peculiarity of slow sand filtration is that it is highly cost-effective for the removal of pathogens (Bennett 2008), making it affordable for use in small-scale aquaponic systems.
Filtration techniques are non-selective; hence, coupled aquaponic farmers should preferably install them at the inlet of the biofilter to treat freshwater from the water source. Though slow sand filtration does not eliminate all pathogens (van Os et al. 2001), it can easily ‘fit-in’ into any aquaponic design, when it is aimed for removing pathogens from water source right at the inlet of the biofilter. Besides, since this technique automatically removes particles from water, reducing turbidity, its combination with UV improves the overall quality of water.
Biological control measures
Entomopathogenic microorganisms (for plant pests)
Entomopathogenic microorganisms are considered the most important group of microorganisms for controlling greenhouse pests (Osborne et al. 2004). The common among these is entomopathogenic bacteria, Bacillus thuringiensis, entomopathogenic fungi, and entomopathogenic nematodes (Osborne et al. 2004; Khan et al. 2012). Entomopathogenic nematodes are commonly used against soildwelling insect pests; hence, their use in the soilless system is limited (Osborne et al. 2004).
However, many entomopathogenic nematodes used in greenhouses are commercially available (e.g. NemaShield, Nemasys, Scanmask, Nemaflor, Nemycel, and Entonem) (Kaya & Koppenh€ofer 1996; Koppenh€ofer et al. 2000). Entomopathogenic bacteria attack the host via ingestion (per os), making them effective against pest larvae. Bacillus thuringiensis subs. kurstaki have been found effective against Tuta absoluta which causes serious damages in tomatoes (Giustolin et al. 2001; Gonzalez-Cabrera et al. 2011).
On the other hand, entomopathogenic fungi parasites directly breach the cuticle to enter the insect hemocoel, causing infections in many insect species (Khan et al. 2012). They have been found effective against many insect species belonging to the orders Hemiptera, Orthoptera, Thysanoptera, Homoptera, Coleoptera, Diptera, and Lepidoptera.
Also, their acaripathogenic characteristics make them a potential biocontrol for a broad range of mites and ticks (Zimmermann 2007; De Faria & Wraight 2007). Some bioinsecticides are based on entomopathogenic fungi (Ascomycota: Hypocreales) commonly used in protected cultures against sucking pests such as whiteflies, thrips, aphids, mealybugs, and scales (Inglis et al. 2001; Osborne et al. 2004).
Microorganisms as biocontrol agents (for fish)
Inactivated and attenuated microorganisms or their derivatives commonly referred to as vaccines have been used against bacterial, fungal, or viral fish diseases in intensive aquaculture systems (reviewed in Assefa & Abunna 2018). They are usually administered orally, through bath or injection (Sommerset et al. 2005). Some options are much more ‘applied’ than vaccination in intensive fish culture units, owing to their broad-spectrum effect and flexibility in the application (through feed or in water directly).
Beneficial live microorganisms called probiotics, their growth substrates called prebiotics (in a combination called ‘symbiotic’) or simply immunostimulants, and herbal extracts through feed have much wider application in fish disease management (reviewed in Dawood et al. 2019; Soltani et al. 2019). Most biological controls designated for fish pest and disease management are usually advocated as ‘fish-friendly choices, albeit their slow mode of action than chemical therapeutics (some of which might sooner or later face ban in Europe; Lieke et al. 2019).
Non-targeted effects of microorganisms as biocontrol agents (BCAs) in aquaponic set-ups
Studies analyzing the non-targeted effects of biological control agents in the aquaponic system are limited and often contradictory. At least the ones having direct application in water (or systems) might have some effect, positive or negative, which requires further clarification (Stouvenakers et al. 2019). There are few reasonable risks associated with the inoculation of foreign microbial BCA in coupled aquaponics.
For plant compartment
Pseudomonas fluorescens and related species are known to colonize the rhizosphere aggressively and establish competition with root pathogens for nutrients (Couillerot et al. 2009). Such competition may concern the acquisition of organic substrates released by seeds and roots (Kamilova et al. 2005), as well as micronutrients such as soluble iron, which is often in limited amounts in aquaponics (Eck et al. 2019; Robaina et al. 2019).
Also, microbial communities can produce multiple modulatory effects on plant physiology (Joyce et al. 2019). Microbacterium oxydans, Pseudomonas thivervalensis and Burkholderia cepacia tested as plant growth-promoting bacteria affected the cultivation-dependent and cultivation-independent bacterial communities in the root endosphere and rhizosphere of Brassica napus (Ren et al. 2019), which can further reduce plant immunity to diseases.
For fish compartment
Only a few studies have investigated the effects of entomopathogenic microorganisms on fish, which might be due to their low adoption in pest and disease management or safety perception of the public on the products. The results from such studies are compiled and provided in the supplementary text. On the other hand, there are also reported effects of microbial biocontrol agent (probiotic) use in RAS systems.
Phaeobacter probiotics grown primarily against pathogens of the family Vibrioniaonaceae in RAS biofilter limit the colonization of the pathogen, but further competes with nitrifying bacteria for oxygen, nutrients, and space in the biofilm which would have led to reduced nitrification recorded (Prol-Garcıa & Pintado 2013). These studies showed probiotics added to an established bio filter can endanger the beneficial biofilter population or reduce the efficiency of the unit.
Potential of the aquaponic microbial community as biological control
As discussed above, the use of external microbial biocontrol in aquaponics is limited by their potential effects on fish and beneficial bacteria. Hence, it is important to explore the potential of the indigenous microbial community for disease management. Recent studies have explored the potential of the aquaponic microbial community at disease control (Schreier et al. 2010; Schmautz et al. 2017; Wongkiew et al. 2018; Bartelme et al. 2018; Eck et al. 2019).
About 13 to 15 phyla have been reported in different compartments of the system, but the dominant genera are usually 6–7. Approximately, proteobacteria (42%), bacteroides (15%), and actinomycetes (13%) form the dominant bacterial consortium in most aquaponic systems. The average CFU in the biological filter is about 7.3 9 106 per gram of media, and the total concentration of bacteria on biofilter media ranges between 5.1 9 106 and 1.1 9 108 9 107 (Munguia-Fragozo et al. 2015).
Proteobacteria (e.g. Pseudomonas) and Bacteroidetes (e.g. Bacillus) species have been used successfully as biological agents in hydroponics and aquaculture (probiotics). Additional information shows that microbial inoculants majorly tested in hydroponics are dominated by heterotrophic bacteria (e.g. Pseudomonas and Bacillus) (68%), due to their broad-spectrum efficiency over several pathogens.
Though they seem to hold good potential for disease control and prevention in aquaponics (Montagne et al. 2017; Stouvenakers et al. 2019), but there is currently limited information on the specific taxonomic identification of the microbial phyla and the possible usage characteristics.
Moreover, study shows that Bacillus sp. (38%), Trichoderma sp. (19%), and Burkholderia sp. (14.3%) are relatively more available in commercial biopesticides than Pseudomonas sp. (4.8%).
Macro-organisms as biocontrol agents (for plants only)
The use of natural enemies against pests, as an option, is available for greenhouse pests (Paulitz & Belanger 2001). A prerequisite for the release of natural enemies is that natural enemies immediately suppress the pest populations and due to their reproduction can manage several pest generations (van Driesche & Heinz 2004; Hajek & Eilenberg 2018).
These natural enemies are either predators or parasitoids. Predatory mites (Acari) such as Amblyseius swirskii and Phytoseiulus persimilis are highly efficient due to the wide range of pests such as whiteflies, thrips, phytophagous mites, and dipterans they can attack (Navarro-Campos et al. 2020). However, despite their reported success in many crops, the sticky hairs on tomato plants have reduced their performances on tomato pests (Gullino et al. 2020).
Common predatory ladybirds (Coleoptera) such as Adalia bipunctata, Cryptolaemus montrouzieri, and Dephalstus catalinae are used on greenhouse aphids, mealybugs, scales, and whiteflies (Gullino et al., 2020). Other predatory biocontrol agents include Hemipterans (e.g. Macrolophus pygmaeus), Nematodes (e.g. Heterorhabditis bacteriophora), and Neuropterans (Chrysoperla carnea), which primarily predate on thrips, shore flies, and aphids, respectively (McEwen et al. 2007).
In contrast, parasitoids such as Aphidius colemani (for aphids) and Encarsia formosa (for whiteflies) are more specific in the pest they attack, making them more sustainably compatible with other biocontrol agents. However, they are highly prone to attacks from hyperparasitoids such as Alloxysta victrix and Asaphes lucens, rendering them less effective at controlling large pest infestations (Sullivan 2009).
Non-targeted effects of macroscopic biocontrol agents (BCAs) in aquaponic set-ups.
In terms of non-targeted impacts, the common presumption is that the parasitoids and predators would eventually be consumed by fish if they accidentally drop in water (Somerville et al. 2014). Lee and Welander (1994) investigated the influence of predators (e.g. rotifers and nematodes) on nitrification in aerobic biofilm processes and found biofilm predators reduced nitrate production rate (from 4 mg N L 1 hour 1 to 3 mg N L 1 hour 1) in 2 weeks – indicating a strong negative effect on nitrification.
However, these are not common macro-organisms as BCAs for aquaponics. Most likely, the macro-organisms as BCAs pose negligible interferences or risk than the microbial BCAs in aquaponic system functioning (e.g. negative interferences with a biofilter, mineralization unit, plant microbiota). Their influences on the overall microbial community structure or parasitism on fish are still unknown (Schmautz et al. 2017).
To avoid a backflow effect of the macro-organisms (as BCA) on the crop in absence of enough prey (i.e. after successful elimination of target pests), provisions of alternative food or hosts would have to be provided (Bennison 1992; Frank 2010). Further information on this aspect is provided in the supplementary text.
Chemical control
The use of pesticides (insecticides, fungicides, herbicides, acaricides, nematicides) is considered ‘last resort’ in IPDM, owing to their detrimental effects on non-target organisms and persistence (Fournier & Brodeur 2000; Stouvenaker et al. 2019).
They, however, comparatively facilitate mass production of high-quality crops and are inexpensive (van Lenteren 2000; Ikeura et al. 2011). This makes them quite inevitable. The system-specific dilemmas associated with chemical control have already been discussed above. Additional clarity on the precautious approach to be used for chemical control in aquaponics is elaborated in the supplementary text.
Insecticides
Insecticides are highly effective emergency action chemicals that control macro-insect vectors and insect pest populations when it exceeds economic thresholds (Ascough et al. 2008; Morand & Lajaunie 2018). Insecticides can be divided into organochlorine, organophosphorus, and carbamate compounds, where pesticides in each group have similar characteristics (Gerba 2019).
Aside from the persistence issues associated with these chemicals, their use in aquaponics can be directly deleterious to fish and beneficial bacteria in coupled aquaponics or make reuse of water difficult for decoupled aquaponic farmers. Hence, aquaponic reliance on insecticides has continued to raise questions on its products (Reinhardt et al. 2019). However, there are available alternatives that are highly adaptable to completely replace the use of insecticide in hydroponics and aquaponics.
Algaecides
Although the problem of weeds and the related use of herbicides in aquaponic set-ups seem mostly irrelevant, there can be concerns with algae. Since optimum growth conditions for hydroponic crops and algae are the same, the latter is always an integral part of hydroponic culture media if left unmanaged (Coosemans 1995). They compete with hydroponic crops for nutrients; hence, their control is eminent for optimal growth of the desired crops (Masser et al. 2013).
Algaecides are chemicals used to keep algae from interfering with the growth of hydroponic crops (Sene et al. 2010). Algaecides might not be toxic to fish when applied according to the manufacturer’s instruction (Masser et al. 2013), but they can disrupt the overall behavioral response of fish coupled with their phytotoxic characteristics (Hostovsky et al. 2014).
However, algae presence in aquaponics can be associated with ‘sub-par’ management. The use of herbicide in aquaponics might be avoided if adequate measures are taken. Algae growth in aquaponics is initiated by access to light; hence, if nutrient solutions and fish tanks are either shaded or covered with a dark material, the growth of algae would be completely controlled (Schwarz & Gross 2004; Somerville et al. 2014). Hence, the use of algicides could be avoided in most aquaponic production.
Fungicides
The warm, high relative humidity and wind-free condition in the greenhouse support fungal growth on leaves and dispersal in the air (Hala si et al. 2008). Hence, farmers need to prevent an outbreak of fungal diseases. There are existing measures that are taken to prevent a fungal outbreak, including the planting of fungi-resistant seeds, frequent sanitization of tools, environmental condition manipulations such as increased temperature (they barely survive at 30°C), reduced relative humidity (below 85%) through the diffused fresh warm air and adjusted moisture level.
When a fungi disease is identified, farmers should immediately remove affected plants and discard all debris in the greenhouse to reduce its spread. Microbial biological agents from Bacillus, Trichoderma, and Pseudomonas species have all been identified to significantly reduce fungal growth. However, their unimpressive results due to variable performances under different environmental conditions have reduced their use (Weltzien 1991; Heydari & Pessarakli 2010).
Repeated foliar application of fungicides is usually adopted to control a fungal outbreak in both field and indoor agriculture. Chemicals such as phosphate, potassium bicarbonate, surfactants and foliar nutrients have also been reported as good remedies against fungal attacks (Crisp et al. 2006). Fungicides are destructive to fish and beneficial bacteria in coupled systems, but their use could be adopted in decoupled systems where nutrient solutions are not reused in the RAS unit.
Sulphur, which is either applied as a spray or via vaporization under high temperature, is considered an effective organic substance against powdery mildew (Crisp et al. 2006). However, side effects such as toxicity to beneficial mites and insects (Calvert & Huffaker 1974), transmission of off-flavours to crops (Martin & Salmon 1931; Gubler et al. 1996), contribution to environmental pollution (Hofstein et al. 1996) and health concerns for human (Mehler 2003) have reduced their use. Alternatives to synthetic pesticides are discussed in the following chapter.
Nematicides
Plant-parasitic nematodes feed on plants or seeds and rapidly spread in the circulation of nutrient solution in hydroponics. The common nematode species associated with the greenhouse include root-knot (Meloidogyne), lesion (Pratylenchus), burrowing (Radapholus) and leaf stem, or foliar nematodes (Aphelenchoides or Ditylenchus) (Moens & Hendrick 1992; Giannakou & Anastasiadis 2005; Hugo & Malan 2010).
Some alternatives (weak) to potential nematicide applications are presented in the supplementary text. Nematode infestation and outbreak are not so common in the greenhouse (especially when there are good hygiene routines), but on their outbreak, farmers might have to trust chemical control to curtail the outbreak. Hence, this group of pesticides is also still relevant to the outbreak of nematodes in soilless systems.
Non-targeted effects of pesticides in aquaponic set-ups
Effects on fish: The rationale and introductory background are presented in the supplementary text. The amount of active ingredients in sprayed pesticide solution that escapes or drifts into nutrient solution is generally unknown.
We investigated ten common pesticides by simulating runoff of 10% and 20% of active ingredient (AI) from the commercial application rate diluting into the nutrient solution of a standard UVI aquaponic system with 506.4L of available water per m2 of plant sprayed. The resulting concentrations were compared with the corresponding NOEC (fish) and LC50 (Oreochromis niloticus) values of the pesticides.
At 10% runoff concentration, endosulfan is the most toxic with a value (20.7 lg L 1) highly greater than the corresponding NOEC (0.05 lg L 1) and LC50 (10.2 lg L 1) concentrations. Carbofuran, cypermethrin, and deltamethrin also show potential toxicity with values greater than NOEC (40 lg L 1, 2 lg L 1, and 0.3 lg L 1, respectively).
Expectedly, all pesticides become more toxic at 20% runoff concentrations compared with 10% runoff. Based on the results, we urge the system managers to adopt precautions to keep runoff thresholds below 10-15% – the lower the safer. The pesticides such as actara, glyphosate, mancozeb, and methomyl appear comparatively less risky.
However, their application should not overlook effects on microbe-mediated nutrient solubilization processes in aquaponic systems. Their biodegradation over time can alter overall water quality in aquaponic systems. As an example, the effects on nitrification and phosphorus solubility can be considered (Figs 2, 3).
In general, the result from this study indicates that higher runoff of pesticides would pose more threat to aquaponics (especially coupled aquaponics). In other studies, high residues of endosulfan, cypermethrin, and deltamethrin were reported in hydroponically grown vegetables, with effects increasing by dosage concentration (Hatzilazarou et al. 2004).
In a recent study (Hong et al. 2020), imidacloprid (IMI) caused significant alterations in microbial communities and induced sub-lethal acute stress in cultured animals. Beneficial bacteria were decreased, while pathogenic forms increased after exposure to IMI. Some additional studies in this regard have been compiled in the supplementary text. These results have shown that apart from the pesticide chemical components (which a farmer cannot alter), the volume of application dosage and application technique might increase the amount of pesticide solution drifting into the water.
We further generated ‘trigger’ percentage runoff from corresponding pesticides’ LC50 and calculated runoff concentrations. These values will help farmers to have an idea of the runoff percentage that will trigger havoc in the system, and further help them in selecting safer pesticides, which are pesticides with higher ‘trigger’ percentage runoff.
However, reducing pesticide solution runoff is a prominent exercise to minimize pesticide active ingredients ending up in the water. A prior covering of openings leading to the nutrient solution would minimize the quantity of the pesticide solution and subsequently the active ingredient drifting into the nutrient solution.
It might be difficult to completely ‘shut out’ drifting of pesticide solution into the nutrient solution, but a dilution of the nutrient solution through the addition of freshwater would dilute the active ingredient into more folds, reducing their effects on fish, rhizosphere community, and beneficial bacteria. Pesticides are quite prone to evaporation (Sanusi et al. 1999).
Using cooling traps to rapidly capture pesticide-laden water as condensate and discarding it is worth exploring for smaller systems. Caution should be exercised in not returning the untreated condensate. In this perspective, the flexibility of the decoupled aquaponics allows the manager to reuse or discard such condensate. Few advanced, practical techniques to reduce influx/drifting away from pesticides to system water are discussed in the supplementary text.
Effects on Nitrification – N mineralization
Nitrification, as one of the key processes in aquaponics, converts ammonia and provides nitrate through metabolic activities of chemoautotrophic bacteria (e.g. Nitrosomonas, Nitrobacter, and Nitrospira) (Monsees et al. 2017b). This process requires among other factors, oxygen for ammonia and nitrite oxidation (3.43 mg for the oxidation of 1 mg NH3–N and 1.14 mg for the oxidation of 1 mg NO2–N) (Chen et al. 2006; Suhr & Pedersen 2010).
Pesticide biodegradation in water is associated with carbon dioxide evolution and oxygen uptake; hence, standard water quality parameters can be altered (Teater et al. 1958; Wainwright & Pugh 1973; Parr 1974). We surveyed existing literature to investigate the positive and negative effects of selected pesticides on nitrification. The effect on nitrification was measured by the percentage change towards or against the nitrification processes.
The interquartile range of change is between 7% and + 33.6%. Aldicarb, carbofuran, chlorsulphuron, DDT, mancozeb, and neem showed negative changes (below 0%) on nitrification. Aldrin, benomyl, BHC, cycloate, fenvalerate, glyphosate, lenacil, oxadiazon, oxyfluorfen, PCA, and phorate produced positive change ranging between 0 and 100%, while phenmedipham produced positive change> 100%.
These varying effects would have originated from the disruption or stimulation of the growth of nitrifying bacteria or the processes involved in nitrification. Reduction in nitrifying bacteria biomass (Widenfalk et al. 2009), phototrophic carbon assimilation (Downing et al. 2004), oxygen depletion (Downing et al. 2008), and reduced diversity of microbial structure (Muturi et al. 2017) are some of common specific effects of pesticides on nitrification.
Effects on Phosphorus solubility activities
In modern aquaponics, pH in the mineralization unit is lowered (<6) to improve phosphorus solubility (along with other nutrients), for plant optimal requirement (Goddek et al. 2018). With pesticide biodegradation reactions strongly connected with pH (and temperature) changes (Siddique et al. 2002; Al-shaalan et al. 2019), they are presumed to have effects on phosphorus solubility in aquaponics.
The interquartile range of change is between 34.3% and + 17.8%. BHC, monocrotophos, oxadiazon, profenophos and quinalphos have positive changes on P solubility from 0 to 75%. Actara, carbofuran, chlorpyrifos, cypermethrin, deltamethrin, endosulfan, fenvalerate, glyphosate and profenophos show negative changes (below 0%) to phosphate solubility. Possible effects of pesticides on condensate and desalination units in decoupled aquaponics are summarized in the supplementary text.
Alternatives to synthetic pesticides – natural pesticides: Organic pesticides are mostly essential plant oils and extracts such as extracts of neem oil, pyrethrum oil, soya bean lecithin, clove oil, thyme oil, cinnamon oil, rosemary oil, tea tree, garlic oil, and peppermint oil.
They are considered an alternative to synthetic pesticides because they are less or non-persistent in the environment, less toxic, and produce little or no residual effects (Schmutterer 1990; Mfarrej & Rara 2019). Coupled with their antimicrobial effects, they have been reported in many studies as effective against many plant pathogens and pests. There is also growing interested in the use of plant extracts and oils to replacing fish antibiotics.
There is, however, little or no knowledge of how the mechanisms of actions would affect non-target organisms (including fish and beneficial bacteria) or disrupt biological or chemical processes. There are no NOEC values established for essential oils; thus, we compared a simulated 10% and 20% runoff concentration of 7 natural pesticides (clove, garlic, cottonseed, pyrethrum, rosemary, neem, and thyme oils) with their corresponding lethal concentrations (LC50) to fish.
Comparatively, concentrations of natural pesticides are lower than the corresponding LC50 at both runoff concentrations, with pyrethrum having the lowest value (0.67 lg L 1), making natural pesticides expectedly safer than synthetic pesticides. Expectedly, all pesticides reach towards their corresponding lethal concentrations, when runoff increases from 10% to 20%.
However, the unavailability of NOEC values indicates that the effects of pesticides on fish behavior, biology, water chemistry, and beneficial bacteria may still be unknown. Moreover, some studies have identified significant effects of essential oils on fish, water chemistry, and microorganisms.
Hence, coupled aquaponic farmers should rather rely on prophylactic measures, cultural control, and biological control methods. Decoupled aquaponic farmers should invariably adopt natural pesticides as a’last resort’ ahead of synthetic pesticides.
Other chemicals
In hydroponics, pathogen contamination arises from many sources, including infested rainwater, surface water, growth media, and infected plant material (Ehret et al. 2001). Hence, frequent disinfection of working tools and nutrient solutions are reliable ‘exercises’ to eliminate pathogen infestation.
Additional technicalities, risks surrounding their use, are summarized in the supplementary text. However, they can reduce microbial populations to near zero when directly applied to water (Barta 2000), making them unsuitable for coupled aquaponics.
These chemicals naturally react with water molecules and other components to produce reactions that would largely be toxic to either fish or beneficial bacteria or both. Hence, their direct application into nutrient solution in coupled aquaponics might be destructive to the entire system.
Decoupled aquaponic farmers would have the advantage to discard such nutrient solutions or be left to neutralize (depending on the type of chemical) before being used in the RAS unit. For disinfection of working tools, such as pruning shears, containers, pipes, and hoses, they should be left to dry after disinfection, before their further use. Where they are used to disinfect rock wools and growth media, the rock wools or growth media should either be autoclaved or left to be completely dry before being put back to use.
Natural elements
Some naturally existing minerals such as copper, sulfur, zinc, and iodine have been found effective in controlling pests and diseases in hydroponics. Copper, zinc, and iodine use have majorly been adopted to eliminate root pathogens (Fusarium, Pythium) and necrosis by direct addition to the nutrient solution (Duffy and Defago, 1997; Runia 1994).
Sulfur granules or micronized sulfur spray are used as fungicides (Crisp et al. 2006). Few risks associated with the use of sulfur are highlighted in the supplementary text. Generally, the direct addition of elements in a common nutrient solution can create loads of additional minerals being transported to the RAS unit, which would exceed the maximum nutrient tolerance for fish and biofilter bacteria.
However, the farmer can dilute the nutrient solution with fresh water to reduce the possible aftermath effects. Strategy inventory for IPDM in aquaponics. Keeping the space size limitations in mind, a brief executive summary of the aquaponic IPDM arsenal for the farmers is provided below, further elaborated in the supplementary text. The potential alternatives to specific scenarios are briefly outlined below.
Alternatives to insecticides
The use of natural enemies, which predate or live as a parasite on pests, has been severally identified as an existing considerable alternative with a high level of success. The use of biological control in agriculture has long emerged, and the use in indoor systems such as greenhouse is more effective because the farmers can optimize the efficiency of the natural enemies in the ‘mini’ ecosystem of the greenhouse than in the field (Van Lenteren & Woets 1988; Vincent et al. 2007).
There is the existing large commercial availability of larvae, pupae, nymph, eggs, and adults of the common natural enemies of pests available around the world almost all insects and pests have commercial biological control solution (Vincent et al. 2007). The predatorial and parasitic activities of the natural enemies are not perceived to create any negative feedback on any aquaponic design.
Also, the use of barrier netting, screening of openings, and manipulation of temperature, and other cultural methods in IPDM mentioned above are safety measures to shut out the insect pests from greenhouse or production enclosures. These measures and the alternative stated above if well implemented in the IPDM steps can address insect pest infestation in aquaponics; hence, the use of insecticides in aquaponics can be of little or no relevance in successful aquaponic production.
Plant insect pests
Adequate alternatives in the form of biocontrol agents are available (entomopathogenic bacteria + fungus, or, natural enemies with banker plant system, or, organic derived/natural pesticides, etc.). The use of chemical pesticides is avoidable.
Plant fungus
Chemical fungicides remain the most reliable option yet. Sulfur fumigation or spraying with natural elements is safer than fungicides. Better is to avoid fungal outbreaks at all costs by routine environmental manipulation (temperature, humidity, ventilation control). There is limited scope for biocontrol. A future alternative needs to be developed.
Plant pathogenic microbes
The use of non-discriminative chemical antimicrobials must be avoided. Combined usage of slow filtration techniques + disinfection of incoming freshwater (with UV) + encouraging aquaponic microbial community itself (selective inoculants of proteobacteria, bacteriodetes, trichoderma, etc., referred to as biopesticides) offers excellent plant biosecurity. For acute cases, natural elements or organic/natural pesticides may be used.
Plant nematode infestation
Chemical nematicides, sanitizers, remain the most reliable control. Organic/natural pesticides (herbal, essential oil extracts) are safer, but less efficient alternatives. Filtration of incoming water, screening of stocking material, and periodic sanitization of units ensure enough biosecurity against nematodes.
Nutrient solution algae bloom
The application of algaecides can be avoided completely with physical barriers (covering reservoirs/ black coloration of reservoirs to avoid light), routine cleaning, and periodic sanitization.
Pathogenic microbes for fish
Antibiotics/ medicated feed can be avoided. The use of UV and/or ozonation (carefully) was integrated with filtration units to screen incoming freshwater. Encouragement of endemic probiotics and bioremediation may be considered through inoculation.
Fungus and parasites for fish
Chemical therapeutics should be preferably applied through bath treatment in quarantine tanks and thus avoiding contamination of the system water. Medicated feed (herbal extracts) provides a safer, yet less efficient alternative. Lesser stocking density, good prophylactics, and biosecurity screening will most likely avoid occurrence.
Conclusive assessments of control methods
Conclusion on biological control
The use of microbial inoculants as biological control agents might be a great potential in aquaponics, but the potential influence they can have on beneficial bacteria and their activities raise questions about their use especially in coupled aquaponics. There seems to be good potential in the microbial community of aquaponics as biocontrol agents, but there is a need for further studies on taxonomic identification and usage characteristics. On the other hand, the natural enemies (predators and parasites) are not perceived to create any problem in all designs.
However, the periodic cost of acquiring the natural enemies for the augmentative release can reduce farmer’s profit in the long run. Hence, rapid pest detection, identification, and subsequent monitoring can simply keep the pest population below the economic threshold (action threshold). Also, effective barrier netting and screening of openings in the greenhouse are preventive measures against pest infestation that can reduce the frequency of pest attacks.
Conclusion on physical control
Physical control adoption in aquaponics might be considered complicated, and farmers would have to strictly consider the level of interaction between the units of the aquaponic design before positioning or location of UV, filtration, and ozonation.
Coupled aquaponic farmers should only adopt slow filtration, ozone, and UV sterilizers as water treatments for freshwater (water source) right before impounding the biofilter, because of the possible deleterious effects on the beneficial bacteria.
On the other hand, decoupled aquaponic farmers might want to use them between the units (especially to control algae growth), but a well-planned preventive and cultural control would rather curb existence or reduce pathogens and algae in the system.
Conclusion on chemical control
To control fungi and other pathogens, coupled aquaponic farmers would have to completely rely on preventive approaches and other IPDM methods other than chemical control, as effects of pesticides can be destructive to the system and make aquaponic products unhealthy for human consumption.
On the other hand, decoupled aquaponic farmers should also rather explore the possibilities of controlling pathogen attacks with cultural, physical, and biological control alternatives. However, if desired results are not obtained, farmers should cautiously use natural pesticides with adequate assessment of the nutrient solution to investigate pesticide compounds before reusing in the RAS unit; otherwise, the nutrient solution should be discarded.
Conclusion
For the first time, we have reviewed the existing IPDM methods in hydroponics for adoption in different aquaponic designs. Prophylactic measures (except chemical sanitary) such as tool disinfection, general sanitation routines, barrier settings, and environmental condition manipulations such as increasing temperature and lowering of relative humidity are not found to create problems for any aquaponic design.
The use of physical control methods, UV, ozone, and slow sand filtration should be limited to treating water sources right before impounding the biofilter due to the possible deleterious effects on beneficial bacteria in the system. On the other hand, chemical control methods are highly complicated for all systems.
While insecticides and herbicides are completely replaceable by well-established commercial biocontrol and prophylactic measures, fungicides and nematicides would still be relevant in aquaponics due to low-efficiency levels of alternative IPDM methods. We investigated the possible effects of 9 pesticide runoff in aquaponics and found endosulfan showing the highest toxicity followed by cypermethrin, deltamethrin, and carbofuran.
All pesticides influence phosphorus and nitrogen availability in water. Natural pesticides show no acute toxicity to fish at runoff concentrations, but they should be avoided in coupled systems – future researches are needed to evaluate their side effects on non-target components of the system (such as the biofilter-rhizosphere community).
Similarly, synthetic pesticides in which runoff concentrations are higher than corresponding NOECs cannot be guaranteed for use, as they are capable of disrupting nitrogen and phosphorus availability, among other possible effects. In biological control, except microbial inoculants, natural enemies of pests (predators and parasites) are mostly safe for any aquaponic design.
The microbial community of aquaponics itself, dominated by Proteobacteria, shows great potential for biological control – effective at microbial load 103-109 CFU mL 1. The prophylactic measures involving little or no physical application into the nutrient solution are highly recommendable approaches for all aquaponic designs.
Source: Folorunso, E. A., Roy, K., Gebauer, R., Bohatá, A., & Mraz, J. (2021). Integrated pest and disease management in aquaponics: A metadata‐based review. Reviews in Aquaculture, 13(2), 971-995.
Useful Article: Aquaponics Microbiome: Importance Of Bacterial Ecosystem
