Efficacy of Fluorinated Nematicides for Management of Root-knot Nematodes in California Processing Tomatoes

The initial RKN levels (Pi) ranged between 1 and 110 J2/100g soil for trial VIII treatment 2 and trial V treatment 7, respectively, and at-harvest RKN levels (Pf) between 9 and 2,477 J2/100g soil for trial VIII treatment 2 and trial I treatment 1, respectively. The soil J2 multiplication factor ranged from 2.2 to 74.2 in trial VI treatment 2 and trial III treatment 1 (Table 1), respectively. Statistical analysis of the soil J2 multiplication factor showed that log₁₀[(Pf/Pi)+1]-transformed data were normally distributed in each trial (Shapiro-Wilk test, P > 0.05). The soil J2 multiplication factor was never significantly different among the treatments (P > 0.05; data not shown).

The yield data (kg fruit per plant) were also normally distributed in each trial (Shapiro-Wilk test, P > 0.05), and the treatments significantly affected the yield in only three of the ten trials (Table 1). In trials I, II, and V, a single pre-plant fluensulfone application at 3.84–4 kg ai/ha increased yields compared with the untreated control. In trial V, oxamyl, fluazaindolizine, and fluopyram treatments also resulted in significantly higher tomato yields than the untreated control (Table 1).

Treatment effects on tomato root-galling were more common, with eight trials showing significant effects of the treatments on galling. In the remaining two trials (IX and X), treatment P-values were 0.07 (Table 1). The untreated control treatment resulted in the highest galling index in each trial. However, in two trials (VI and VII), one of the nematicide treatments resulted in an equally high galling index.

The first three trials focused on comparing the efficacy of fluensulfone with oxamyl. In trial I, a repeated application of oxamyl and a single pre-plant application of fluensulfone both reduced root-galling compared with the untreated control, but fluensulfone was more effective. Furthermore, fluensulfone increased yields, whereas oxamyl did not. In trials II and III, the oxamyl treatments did not significantly reduce galling or improve yields, but three of four fluensulfone treatments were effective in reducing root-galling (Table 1).

In trial IV, fluazaindolizine was evaluated for the first time and compared to oxamyl and fluensulfone. In this trial, the two higher rates of pre-plant applied fluensulfone (1.96 and 2.81 kg/ha), and all three fluazaindolizine treatments (once 0.56 kg/ha, twice 0.28 kg/ha, 0.56 kg/ha followed by 0.28 kg/ha) significantly reduced galling. Oxamyl was not effective (Table 1).

Fluopyram was first included as a treatment in trial V, which also included oxamyl, fluensulfone, and fluazaindolizine. Oxamyl was the only nematicide treatment that failed to reduce galling. The two fluazaindolizine treatments resulted in strong and significant reductions in galling and also resulted in the highest yield increase compared to the untreated control treatment. The fluopyram treatment also reduced galling but not as effectively as fluazaindolizine. The efficacy of the two fluensulfone treatments in this trial was intermediate between fluazaindolizine and fluopyram.

In trial VI, three treatments of fluazaindolizine and fluopyram were compared to oxamyl. The latter again failed to significantly reduce galling, and the fluazaindolizine treatments again were very effective in reducing root-galling. The fluopyram treatments were also effective, particularly when applied as a split application of two times 0.25 kg/ha (Table 1). Because of the generally poor performance of oxamyl in trials I-VI, it was no longer included as a treatment in subsequent trials.

All three fluorinated nematicides were included as treatments in trial VII, with an emphasis on fluazaindolizine, which was applied in different formulations, at different rates, and as a single or split application resulting in a total of six fluazaindolizine treatments. The four single pre-plant soil-incorporated applications of the liquid or granular formulation at 2.26 kg/ha (treatments 7–10, Table 1) did not significantly reduce galling. However, the two drip-tubing-applied split applications (treatments 5 and 6, Table 1) significantly reduced galling. Fluopyram was again effective. The two fluensulfone treatments did not result in significantly lower root-galling compared with the untreated control.

In trial VIII, only a single pre-plant incorporated fluensulfone treatment was included. Although the average at-harvest root-galling was low even in the untreated control (galling index 3.4), the fluensulfone treatment still significantly reduced galling to a very low level (Table 1).

Treatment effects on root-galling in trials IX and X, both done in 2021, were not significant at the 95% confidence level (treatment effect on root-galling: P = 0.07 in both trials). However, in both trials, each nematicide treatment resulted in numerically lower root-galling levels than the untreated control (Table 1).

Rates of single pre-plant fluensulfone applications in the trials ranged between 1.4 and 4.0 kg/ha. In trial IV, where rates of 1.4, 1.96, and 2.81 were compared, the lower rate did not significantly reduce galling compared to the untreated control. It was less effective than the two equally effective higher rates which did significantly reduce galling. Direct comparisons between fluensulfone rates of 2.97 and 4.00 kg/ha were included in four trials (III, V, VII, X). There were no significant differences in efficacy to reduce root-galling between these two rates in any of these four trials (Table 1). Following a pre-plant application of fluensulfone with a post-plant application was evaluated only once, in trial II. This treatment is, however, not allowed according to the US EPA label. Although this treatment reduced root-galling compared with the untreated control, it also significantly reduced yields compared with a one-time pre-plant fluensulfone application (Table 1).

Total amounts of fluazaindolizine applied in the trials ranged from 0.56 to 2.24 kg/ha and were applied as a one-time pre- or at-plant treatment or as at-plant followed by post-plant treatments. The lowest rate of 0.56 kg/ha was only used in trial IV in two treatments: a one-time at-plant treatment (trial IV treatment 6) or as a split application (twice 0.28 kg/ha, trial IV treatment 7). Even at these low rates, the two treatments were very effective in reducing root-galling (Table 1). A comparison between total amounts of 1.68 kg/ha and 2.24 kg/ha in split applications was included in trials V, VI, and IX. These treatments effectively reduced galling in trials V and VI but not in trial IX. However, there were no indications that the higher rate was more effective in reducing root-galling (Table 1). A granular formulation of fluazaindolizine was compared with the liquid formulation in trial VII at 2.24 kg/ha applied 3- or 10-days pre-plant. These treatments did not significantly reduce root-galling compared with the untreated control and were not different from each other (Table 1, trial VII treatments 7–10).

Total amounts of fluopyram applied in the trials were 0.19, 0.25, or 0.5 kg/ha. The lower rate was applied in trials IX and X, and in both these trials, there were no significant treatment effects (Table 1). The higher rate was only applied as a split application (at-plant and post-plant) of two times 0.25 kg/ha and significantly reduced root-galling in all three trials where it was included as a treatment (Table 1, trial V treatment 7, trial VI treatments 7 and 8, trial VII treatment 2). A single at-plant fluopyram treatment at 0.25 kg/ha, however, did not significantly reduce root-galling compared with the untreated control (Table 1, trial VI treatment 6).

Regression analysis of the difference in average tomato root-galling between untreated controls and nematicide treatments in each trial (gall_diff) and the percentage yield difference of the nematicide treatments relative to the untreated controls in each trial (yield_diff) showed that the quadratic model: yielddiff=0.63×galldiff2+4.43×galldiff {\rm{yiel}}{{\rm{d}}_{{\rm{diff}}}} = 0.63 \times {\rm{gal}}{{\rm{l}}_{\rm{diff}}}^{2} + 4.43 \times {\rm{gal}}{{\rm{l}}_{{\rm{diff}}}} best fitted the data (adjusted R² = 0.83, Figure 1). Averaged over all trials, fluensulfone reduced the galling index compared to the untreated control with 2.3, fluazaindolizine with 3.2, and fluopyram with 2.5. According to this model, achieving these reductions in root-galling corresponds with yield gains of 14%, 21%, and 15%, respectively, over the untreated control.

Figure 1.

Correlation between reduction in tomato root-galling (gall_diff) and percent yield difference (yield_diff) relative to untreated control treatments from ten field trials. Line fitted according yield_diff = 0.63 × gall_diff² + 4.43 × gall_diff. adjusted R²=0.83.

The use of Mi-resistant tomato cultivars has been the foundation of RKN management in California for many years. Populations of RKN able to overcome this resistance were rare in the past (Kaloshian et al., 1996) but have become more common in several major CA production areas (Ploeg et al., 2018). At the same time, back-to-back tomato planting in the same location on beds with semi-permanent deep-buried drip irrigation tubing is practiced. Winter cropping with wheat, which generally exhibits only minor RKN root symptoms but sustains the nematodes (Martin et al., 2021), may further enhance the survival of RKN in the absence of tomato.

The CA IPM Center at UC Davis identified two critical research issues on RKN management in processing tomatoes: 1) the development of cultivars with new sources of RKN resistance and 2) the evaluation of new nematicides (Martin et al., 2021). Although other RKN resistance genes have been identified in wild tomato germplasm (Veremis and Roberts, 1996; Ammiraju et al., 2003), they have not yet been incorporated into new tomato cultivars.

The development of fluorinated nematicides, a class of new contact nematicides, and, perhaps more importantly, active ingredients with novel modes of action has significantly changed our standard operating procedure (Desaeger et al., 2020; Oka, 2020). In our studies, results from ten years of field trials with susceptible processing tomato on a site infested with medium to high levels of an M. incognita race 3 RKN population confirmed the utility of the three tested nematicides as they reduced root-galling and improved yield.

The three tested nematicides have much improved toxicological profiles and are generally considered more benign to non-target organisms than previous carbamate and organophosphate nematicides. All three products showed excellent efficacy in initial pot trials (Loffredo et al., 2024), but their performance in the field was much more variable, and their field application presented some challenges. Fluensulfone can result in delayed germination and/or reduced vigor in direct-seeded crops such as carrots (Becker et al., 2019), cucumbers (Ploeg, unpublished data), and lima beans (Jones et al., 2017) when applied at or close to seeding. However, phytotoxic effects were not observed in any of the trials in this study with transplanted tomatoes, where fluensulfone applications ranged between 14 days pre-plant and 21 days post-plant. Fluopyram is, in vitro, an excellent nematicide at very low concentrations (Faske and Hurd, 2015), second only to abamectin. However, Grabau et al. (2021), in a review comparing the efficacy of the three fluorinated nematicides from lab, greenhouse, and field tests, reported that fluopyram was not consistently better than the other two. Fluopyram has low soil mobility (Becker et al., 2019; Faske and Brown, 2019; Rathod et al., 2022), and consequently, the activity does not extend much beyond the application zone. This effect was clearly demonstrated in carrot trials where only the upper part of the carrot roots remained free of galling after a shallow soil-incorporated application of fluopyram (Becker et al., 2019), whereas fluensulfone and fluazaindolizine protected the entire carrot roots from galling. The significant galling on the lower part of the carrot roots after a fluopyram application still rendered them unmarketable, resulting in fluopyram being much less effective in preventing a loss in marketable carrots compared to fluensulfone and fluazaindolizine (Becker et al., 2019). Whereas a carrot with a root-galling index of > 3 (0 – 10 scale) is considered unmarketable (Becker et al., 2019), in tomatoes, there is no such cut-off value for root-galling resulting in a complete crop loss. Consequently, in these trials, no major differences in the efficacy among the three fluorinated nematicides were observed.

In vitro tests with fluazaindolizine showed that nematode mortality occurred only after several days of exposure (Thoden and Wiles, 2019; Wu et al., 2020) but also that sublethal concentrations still reduced or inhibited nematode motility and infectivity (Wram and Zasada, 2019). Averaged over all trials, fluazaindolizine was the most efficacious product, reducing tomato root-galling by 3.2 compared to the untreated controls, which corresponds with a predicted yield increase of 21% over the untreated controls. A similar result was obtained in carrot field trials with the same three fluorinated nematicides, where fluazaindolizine was also the most effective product (Becker et al., 2019).

Oxamyl is still registered in California for nematode management in tomatoes, but it did not significantly reduce tomato root-galling compared to the untreated control in five out of the six trials that included an oxamyl treatment. This lack of efficacy has been observed previously, particularly in warm, moist, alkaline soils with elevated soil pH, which correlated with a short persistence of the nematicide (Haydock et al., 2012).

The fluorinated nematicides tested in these trials were effective in reducing root-galling in tomatoes. They could be used where resistance-breaking populations occur or in an integrated system with susceptible cultivars to avoid damage and selection of resistance-breaking populations. In trial IV, the high rate of fluensulfone reduced galling more than the low rate. In general, however, there were no differences between rates or application methods of the nematicides.

Recently, polyfluoroalkyl substances (PFAS) have become under scrutiny because of potential environmental and health concerns. These synthetic chemicals are highly stable and have a high attraction to lipids. This could result in bioaccumulation and ecotoxicological effects in soils and water environments (Alexandrino et al., 2022). All three fluorinated nematicides in this study are included in a list of PFAS pesticides published by the Minnesota Department of Agriculture (https://www.mda.state.mn.us/environment-sustainability/active-inert-pfas). The European Union has proposed a wide-ranging ban on fluorinated compounds (Rossen, 2023), and several US states have planned similar restrictions on PFAS-containing pesticides. The compounds are categorized as long-, short, and ultra-short-chain PFAS, which have >7, 4–7, and 2–3 fully fluorinated C-atoms, respectively (Wang et al., 2017). While most studies have focused on long-chain PFAS, uncertainty remains concerning the toxicity of ultra-short and short-chain PFASs, especially regarding long-term effects, emphasizing the need for further research (Ateia et al., 2019; Fenton et al., 2021). Thus, the future of the fluorinated nematicides used in our studies remains uncertain, but banning the whole spectrum of PFAS, which includes more than 12,000 compounds, would have many unexpected consequences, including impacting an increasing number of pharmaceutical and plant protection compounds (Spyrakis and Dragani, 2023; Tyrrell, 2023).