Experts’ opinion on the sustainable use of nematicides in Mediterranean intensive horticulture

Introduction

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., 2018Egea FJ, Torrente RG, Aguilar A, 2018. An efficient agro-industrial complex in Almería (Spain): Towards an integrated and sustainable bioeconomy model. N Biotechnol 40: 103-112. https://doi.org/10.1016/j.nbt.2017.06.009). 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, 2020MAPAMA, 2020. Anuario de estadística 2020. Ministerio de Agricultura, Pesca y Alimentación, Madrid, Spain.).

Plant parasitic nematodes are one of the most significant pests limiting global vegetable production (Nicol et al., 2011Nicol JM, Turner SJ, Coyne DL, den Nijs L, Hockland S, Thana Maafi Z, 2011. Current nematode threats to world agriculture. In: Genomics and molecular genetics of plant-nematode interactions; Jones J, Gheysen G, Fenoll C (Eds.). Springer, Dordrecht, pp. 21-43. https://doi.org/10.1007/978-94-007-0434-3_2; Singh et al., 2015Singh S, Singh B, Singh AP, 2015. Nematodes: A threat to sustainability of agriculture. Procedia Environ Sci 29: 215-216. https://doi.org/10.1016/j.proenv.2015.07.270). 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., 2012Talavera M, Sayadi S, Chirosa-Ríos M, Salmerón T, Flor-Peregrín E, Verdejo-Lucas S, 2012. Perception of the impact of root-knot nematode-induced diseases in horticultural protected crops of south-eastern Spain. Nematology 14: 517-527. https://doi.org/10.1163/156854112X635850, 2019Talavera M, Miranda L, Gómez-Mora JA, Vela MD, Verdejo-Lucas S, 2019. Nematode management in the strawberry fields of southern Spain. Agronomy 9: 1-17. https://doi.org/10.3390/agronomy9050252).

Since nematode-caused yield losses are directly proportional to nematode soil densities at planting (Seinhorst, 1965Seinhorst JW, 1965. The relation between nematode density and damage to plants. Nematologica 11: 137-154. https://doi.org/10.1163/187529265X00582), 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, 2014Jacobsen CS, Hjelmsø MH (2014). Agricultural soils, pesticides and microbial diversity. Curr Opin Biotechnol 27: 15-20. https://doi.org/10.1016/j.copbio.2013.09.003). 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., 2021Sasanelli N, Konrat A, Migunova V, Toderas I, Iurcu-Straistaru E, Rusu S, et al., 2021. Review on control methods against plant parasitic nematodes applied in southern member states (C zone) of the European Union. Agriculture 11: 1-19. https://doi.org/10.3390/agriculture11070602). 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, 2020Forghani F, Hajihassani A, 2020. Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Front Plant Sci 11: 1-13. https://doi.org/10.3389/fpls.2020.01125).

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., 2012Talavera M, Sayadi S, Chirosa-Ríos M, Salmerón T, Flor-Peregrín E, Verdejo-Lucas S, 2012. Perception of the impact of root-knot nematode-induced diseases in horticultural protected crops of south-eastern Spain. Nematology 14: 517-527. https://doi.org/10.1163/156854112X635850, 2019Talavera M, Miranda L, Gómez-Mora JA, Vela MD, Verdejo-Lucas S, 2019. Nematode management in the strawberry fields of southern Spain. Agronomy 9: 1-17. https://doi.org/10.3390/agronomy9050252; Greco et al., 2020Greco N, López-Aranda JM, Saporiti M, Maccarini C, de Tommaso N, Myrta A (2020). Sustainability of European vegetable and strawberry production in relation to fumigation practices in the EU. Acta Hortic 1270: 203-210. https://doi.org/10.17660/ActaHortic.2020.1270.24). Soil fumigation has been used regularly by 83-90% of the farmers in these intensive horticultural crops (Talavera et al., 2012Talavera M, Sayadi S, Chirosa-Ríos M, Salmerón T, Flor-Peregrín E, Verdejo-Lucas S, 2012. Perception of the impact of root-knot nematode-induced diseases in horticultural protected crops of south-eastern Spain. Nematology 14: 517-527. https://doi.org/10.1163/156854112X635850, 2019Talavera M, Miranda L, Gómez-Mora JA, Vela MD, Verdejo-Lucas S, 2019. Nematode management in the strawberry fields of southern Spain. Agronomy 9: 1-17. https://doi.org/10.3390/agronomy9050252; Greco et al., 2020Greco N, López-Aranda JM, Saporiti M, Maccarini C, de Tommaso N, Myrta A (2020). Sustainability of European vegetable and strawberry production in relation to fumigation practices in the EU. Acta Hortic 1270: 203-210. https://doi.org/10.17660/ActaHortic.2020.1270.24), 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., 2021Sasanelli N, Konrat A, Migunova V, Toderas I, Iurcu-Straistaru E, Rusu S, et al., 2021. Review on control methods against plant parasitic nematodes applied in southern member states (C zone) of the European Union. Agriculture 11: 1-19. https://doi.org/10.3390/agriculture11070602). 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., 2023Nagesh P, Edelenbosch OY, Dekker SC, de Boer HJ, Mitter H, van Vuuren DP, 2023. Extending shared socio-economic pathways for pesticide use in Europe: Pest-Agri-SSPs. J Environ Manage 342: 118078. https://doi.org/10.1016/j.jenvman.2023.118078).

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.

Material and methods

Assessing the experts’ opinion on nematode control methods

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To obtain data on the perception of the relative effectiveness and environmental sustainability of nematode control methods, what drives the decision-making process on the use of a particular nematicidal treatment, as well as their sustainability, a survey was designed and oriented to experts with experience in soil disinfestation against plant parasitic nematodes.

Forty experts were selected from the group of farm advisors dealing with nematode control in the intensive vegetable-growing areas of southern Spain. Farm advisors are qualified agronomists that deal with vegetable crop pests and diseases in commercial fields daily, thus providing a valuable source of accumulated local knowledge.

A survey involving a self-administered questionnaire (see Appendix [suppl]) distributed by email was carried out in October 2021. To select the nematode control methods and to assess the general structure of the questionnaire, a discussion group, composed of six experts, was conducted. The questionnaire was divided into two parts, first assessing five nematode control methods in terms of (i) effectiveness in suppression of nematode diseases, (ii) environmental impact, and (iii) side effects on human health; and second, an overall appraisal of the contribution of these criteria to the sustainability of nematode control strategy.

The Analytic Hierarchy Process (AHP) was developed as a decision-making aid tool to handle complex problems by using a hierarchical framework (Saaty, 1980Saaty TL, 1980. The analytic hierarchy process. McGraw-Hill, New York, USA. 287 pp. https://doi.org/10.21236/ADA214804; Vaidya & Kumar, 2006Vaidya OS, Kumar S, 2006. Analytic hierarchy process: An overview of applications. Eur J Oper Res 169: 1-29. https://doi.org/10.1016/j.ejor.2004.04.028). Briefly, in each level, the relative importance (or weightings) of its elements with respect to the higher level was obtained by a series of pairwise comparisons that determine which option is preferred and for how much, using, among other options, the linear scale proposed by Saaty (1980)Saaty TL, 1980. The analytic hierarchy process. McGraw-Hill, New York, USA. 287 pp. https://doi.org/10.21236/ADA214804 that ranges from 1 (equally importance) to 9 (absolutely preferred over the other). In our study, the hierarchical structure had three levels: (a) at the top the overall goal, that is, finding the most sustainable nematode control strategy; (b) in the intermediate level the sustainability criteria (nematicidal efficacy, environmental impact, and human health risk); and (c) at the lowest level, the nematicidal treatments alternatives (Fig. 1). The hierarchical structure of the AHP method means that the weightings obtained at each level add up to one, therefore, the normalized importance that the decision maker assigns to alternative i to the goal, , is calculated as follows:

Figure 1.  The AHP’s hierarchical structure for evaluating nematicidal treatments.

$w_i^{*}=\sum _{j=1}^3 w_{ij}*w_j$  

where w _ij is the weighting of alternative i with respect to criterion j and w _j is the weighting assigned to criterion j.

Although AHP assumes evaluation consistency by the decision makers, perfect consistency is rare, therefore, a consistency index (CI), must be calculated to avoid exceeding a predefined value (Dodd et al., 1993Dodd F, Donegan HA, McMaster TBM, 1993. A statistical approach to consistency in AHP. Math Comput Model 18: 19-22. https://doi.org/10.1016/0895-7177(93)90123-G). Once the individual experts’ judgements were calculated, before the aggregation, we assessed the degree of agreement between the experts’ weightings using the intraclass correlation coefficient (ICC), with 1 indicating perfect agreement and 0 only random agreement (Hallgren, 2012Hallgren KA (2012). Computing inter-rater reliability for observational data: An overview and tutorial. Tutor Quant Methods Psychol 8: 23-34. https://doi.org/10.20982/tqmp.08.1.p023). Since the 40 experts, viewed as random effects, rated all the five nematicidal methods the model of choice is a 2- two-way mixed-effects model. Additionally, we were interested in the reliability of the mean in terms of consistency, therefore, we used the ICC3k coefficient (Koo & Li, 2016Koo TK, Li MY (2016). A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15: 155-163. https://doi.org/10.1016/j.jcm.2016.02.012). Finally, once the experts’ consistency was assessed, we followed the Forman and Peniwati aggregation procedure (Forman & Peniwati, 1998Forman E, Peniwati K (1998). Aggregating individual judgments and priorities with the analytic hierarchy process. Eur J Oper Res 108: 165-169. https://doi.org/10.1016/S0377-2217(97)00244-0), using the geometric mean to obtain the group decision-making.

Results

Discussion

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., 2022Talavera-Rubia M, Vela-Delgado MD, Verdejo-Lucas S, 2022. A cost-benefit analysis of soil disinfestation methods against root-knot nematodes in Mediterranean intensive horticulture. Plants 11: 2774. https://doi.org/10.3390/plants11202774). 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., 2019Talavera M, Miranda L, Gómez-Mora JA, Vela MD, Verdejo-Lucas S, 2019. Nematode management in the strawberry fields of southern Spain. Agronomy 9: 1-17. https://doi.org/10.3390/agronomy9050252, 2012Talavera M, Sayadi S, Chirosa-Ríos M, Salmerón T, Flor-Peregrín E, Verdejo-Lucas S, 2012. Perception of the impact of root-knot nematode-induced diseases in horticultural protected crops of south-eastern Spain. Nematology 14: 517-527. https://doi.org/10.1163/156854112X635850).

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., 2022Talavera-Rubia M, Vela-Delgado MD, Verdejo-Lucas S, 2022. A cost-benefit analysis of soil disinfestation methods against root-knot nematodes in Mediterranean intensive horticulture. Plants 11: 2774. https://doi.org/10.3390/plants11202774) 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., 2009Sánchez-Moreno S, Alonso-Prados E, Alonso-Prados JL, García-Baudín JM, 2009. Multivariate analysis of toxicological and environmental properties of soil nematicides. Pest Manag Sci 65: 82-92. https://doi.org/10.1002/ps.1650), 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., 2017Lahm GP, Desaeger J, Smith BK, Pahutski TF, Rivera MA, Meloro T, et al., 2017. The discovery of fluazaindolizine: A new product for the control of plant parasitic nematodes. Bioorg Med Chem Lett 27: 1572-1575. https://doi.org/10.1016/j.bmcl.2017.02.029; Oka, 2020Oka Y, 2020. From old-generation to next-generation nematicides. Agronomy 10: 1-16. https://doi.org/10.3390/agronomy10091387; Talavera et al., 2021Talavera M, Thoden TC, Vela-Delgado MD, Verdejo-Lucas S, Sánchez-Moreno S, 2021. The impact of fluazaindolizine on free-living nematodes and the nematode community structure in a root-knot nematode infested vegetable production system. Pest Manag Sci 77(11): 5220-5227. https://doi.org/10.1002/ps.6563).

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.