In southern Spain, intensive horticulture is a crucial agricultural business that contributes up to 40% of the gross domestic product in some regions (Egea et al., 2018). There are about 40,000 hectares of protected vegetable crops, under plastic greenhouses or macro-tunnels, producing over 4,000,000 tons of high-value solanaceous, cucurbitaceous and berry crops that are shipped for fresh consumption in European markets with a yearly commercial value of approximately €3 billion (MAPAMA, 2020).

Plant parasitic nematodes are one of the most significant pests limiting global vegetable production (Nicol et al., 2011; Singh et al., 2015). In southern Spain intensive horticultural crops, root-knot nematodes (RKN: Meloidogyne spp.) prevalence ranges 20-70% and are viewed as the most common limiting factor to reaching premium quality and economically viable vegetable yields (Talavera et al., 2012, 2019).

Since nematode-caused yield losses are directly proportional to nematode soil densities at planting (Seinhorst, 1965), nematode management strategies have primarily focused on reducing nematode soil inocula prior to planting. Conventionally, RKN management in intensive crops has relied on fumigant chemical nematicides to disinfest soil. Fumigants are biocides with a broad spectrum that are most effective at reducing RKN soil populations but have adverse side effects on beneficial soil organisms (Jacobsen & Hjelmsø, 2014). The environmental impact of plant protection products is becoming increasingly relevant from both an ecological and political standpoint.

Currently, six non-fumigant nematicides (abamectin, azadirachtin, dazomet, fosthiazate, fluopyram, and oxamyl), two botanical pesticides (based on garlic extract and terpenes from essential oils) and two biological control agents (Bacillus firmus and Purpureocillium lilacinum) are registered and approved for use in the European Union (EU) against plant parasitic nematodes (Sasanelli et al., 2021). In addition, some other products, categorized as biostimulants or soil improvers, such as amino acids, humic and fulvic acids, plant growth promoting rhizobacteria, arbuscular mycorrhizae fungi, Trichoderma spp. and other plant extracts or essential oils, have been reported as partial suppressors of RKN diseases in vegetables and are used occasionally by farmers to improve yields in nematode-infested soils. Alternative physical and cultural nematode management strategies, such as biosolarization or the use of ozone as ozonated water to disinfest soil are also available (Forghani & Hajihassani, 2020).

Farmers in southern Europe have considered soil chemical fumigation, as the most effective method for controlling RKN diseases in intensive horticultural crops, since the efficacy of other nematode control methods has not proven consistent enough when high RKN soil infestations occur (Talavera et al., 2012, 2019; Greco et al., 2020). Soil fumigation has been used regularly by 83-90% of the farmers in these intensive horticultural crops (Talavera et al., 2012, 2019; Greco et al., 2020), but owing to rising social awareness of the environmental concerns associated with agrochemicals’ usage, most soil fumigants have been banned or heavily restricted in EU, as part of the European Green Deal and the ‘farm to fork strategy’. Therefore, in a new scenario without fumigants farmers will have to use more complex strategies based on the integration of multiple control methods (IPM: Integrated Pest Management) to reach sufficient efficacies in reducing high RKN soil inocula (Sasanelli et al., 2021). IPM aims to limit the use of pesticides to economically and ecologically justifiable levels that reduce the risks to human health and environment. According to the EU policies, sustainable biological, physical, and other non-chemical methods must be favored over chemical methods if they provide adequate pest control.

Programming activities designed to implement any IPM system for nematode management should ideally account for both agricultural properties of an IPM system and farmer’s decision-making process. However, due to the lack of data on the specific systems to be implemented a great deal of uncertainty exists as to how growers will deal with high nematode infestations in intensive horticulture. This lack of information makes predictions of farmers’ responses to the sustainable use of nematicides imprecise at best (Nagesh et al., 2023).

This paper examines farm advisors’ preferences on the use of currently available methods for RKN control in the EU according to the opinion of a group of experts in nematode control: field nematologists and agricultural advisors, who are employed by the co-operatives in which farmers associate to sell their production and are in charge of dealing with RKN diseases in most fields.

Conventionally farm advisors have recommended nematode management strategies according mainly to the nematicidal effectiveness and secondarily to a cost-benefit analysis of the treatment (Talavera-Rubia et al., 2022). For nematicidal efficacy, agricultural advisors consider that fumigant nematicides are the most efficient method for RKN control, followed by biosolarization and non-fumigant nematicides in third place, what agrees with previous reports about nematicide efficacies in most horticultural crops in Spain (Talavera et al., 2019, 2012).

However, our results indicate that the most important criterion among farm advisors for choosing nematicidal treatments is now the preservation of human health, followed by nematicidal efficacy and reduction of harmful environmental side effects, in that order. Biosolarization and biological pesticides were regarded as the two best ways for reducing environmental impacts and adverse effects on human health, in line with the ecotoxicological results observed for these group of treatments (Table 1). When compared to non-fumigant nematicides, which are classified as being highly toxic for the environment, biosolarization and biological pesticides have reportedly been found to be relatively non-toxic or slightly toxic (Table 1).

Considering the three criteria together, the most sustainable RKN control method for farm advisors was biosolarization, followed by biological pesticides. Despite being the most effective, fumigant nematicides ranked third in terms of sustainability. Finally, according to these results, the less sustainable treatments were ozone and non-fumigant nematicides. The prioritizing criteria used by farm advisers to recommend nematode management techniques have changed, shifting away from the effectiveness side of these treatments toward environmental and health preservation.

Particularly interesting is the case of soil disinfestation with 1,3-dichloropropene. A cost-benefit analysis of soil disinfestation methods against RKN in Mediterranean intensive horticulture (Talavera-Rubia et al., 2022) showed that fumigation with 1.3-dichloropropene and biosolarization with chicken manure were the only treatments able to reduce high RKN soil inocula to levels below the nematode economic damage threshold, keeping profitability in the most susceptible crops as eggplant or cucumber. Other nematicidal treatments were not able to reduce RKN populations above 200-300 J2/100 cm³ of soil below the economic thresholds. Therefore, when high RKN inocula occurs fumigant treatments with 1,3-dichloropropene could be still required since other options may not be profitable. Despite of 1,3-dichloropropene was included in the lowest toxicity group due to its low-medium persistence in the environment and its low EHI (Sánchez-Moreno et al., 2009), its use is currently banned in the EU, in contrast with other chemical nematicides with higher toxicities and thus higher EHI, whose use is still allowed within the EU. This apparently contradictory regulation could be explained considering the widespread use of 1,3-dichloropropene, and the great impact of banning one single agrochemical to easily get the objectives of reduction in the use of pesticides required by the EU.

However, in most cases, RKN soil densities in field are below the limits of 200-300 J2/100 cm³ of soil and thus other RKN management options are feasible and will be recommended by farm advisors, prioritizing those with less side effects on human health and environment. Next generation nematicides as fluensulfone, fluopyram, and fluazaindolizine, which have a relatively high control efficacy with a low toxicity to non-target organisms are also a promising alternative tool in sustainable RKN management strategies (Lahm et al., 2017; Oka, 2020; Talavera et al., 2021).

Providing that current RKN available method give enough nematicidal effectiveness to get a profitable yield, the group of farm advisors show a great consciousness on the use of sustainable alternatives for RKN control in intensive horticultural crops. The first option as RKN control method for them, is biosolarization followed by biopesticides and fumigant nematicides in third place, due to their superior effectiveness in fields infested with high RKN soil inocula. The use of ozone and non-fumigant nematicides with high toxicity profiles were considered the last options.

The results of this study indicate that farm advisors are highly inclined to adjust their methods for managing plant-parasitic nematodes in intensive crops, with a preference for sustainability above effectiveness. Biosolarization and other environmentally friendly methods are expected to become more widely utilized in the next years, while the use of chemical nematicides is anticipated to decrease. Only in exceptional circumstances characterized by high nematode densities in soil at planting time, should the most effective chemical nematicides be utilized.