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Article

Effect of Non-Fumigant Nematicides on Reproduction of Recently Detected Meloidogyne Species in Georgia Under Greenhouse Conditions in Tomato

by
Nabin Poudel
1,
Luis Torres
1,
Richard F. Davis
2,
Ganpati B. Jagdale
3,
Theodore McAvoy
4 and
Intiaz A. Chowdhury
1,*
1
Department of Plant Pathology, University of Georgia, Tifton, GA 31793, USA
2
Crop Genetics and Breeding Research Unit, United States Department of Agriculture—Agricultural Research Service, Tifton, GA 31793, USA
3
Extension Nematology Lab, Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA
4
Department of Horticulture, University of Georgia, Tifton, GA 31793, USA
*
Author to whom correspondence should be addressed.
Horticulturae 2025, 11(1), 36; https://doi.org/10.3390/horticulturae11010036
Submission received: 25 November 2024 / Revised: 20 December 2024 / Accepted: 31 December 2024 / Published: 3 January 2025
(This article belongs to the Section Plant Pathology and Disease Management (PPDM))
Versions Notes

Abstract

:
Root-knot nematodes (Meloidogyne spp.; RKNs) are among the most destructive soil-borne pathogens affecting tomato production. Recently, aggressive species such as M. enterolobii, M. floridensis, and M. haplanaria have been reported in several tomato fields across the southern United States. Host resistance in tomato, effective against commonly prevalent M. incognita, is ineffective against these emerging species, making chemical nematicides the primary management approach. However, studies on the efficacy of chemical nematicides on these emerging RKN species remain limited. This study evaluated the efficacy of four non-fumigant nematicides—fluazaindolizine, fluensulfone, fluopyram, and oxamyl—on the reproduction of these emerging species and M. incognita. Fluensulfone consistently suppressed nematode reproduction by over 90.0% across all species. Fluopyram reduced reproduction by over 50.0% in most species but was less effective against M. enterolobii, with suppression of only 24.3%. Similarly, fluazaindolizine suppressed egg counts by more than 50.0% across all species except M. enterolobii, where it suppressed only 41.1%. Oxamyl suppressed egg counts in M. floridensis and M. incognita by more than 50.0%, but reductions in M. enterolobii and M. haplanaria were lower at 23.2% and 38.7%, respectively. These results highlight species-specific differences in nematicide efficacy and provide a crucial baseline for future research for the management of specific RKN species.

1. Introduction

Tomato (Solanum lycopersicum L.) is an economically important vegetable crop, grown worldwide. According to the United States Department of Agriculture (USDA) Economic Research Service, tomato is among the most consumed vegetables in the United States. In 2023, the U.S. produced approximately 12.3 billion kg of tomatoes, with the value of utilized production estimated at USD 2.7 billion [1]. Despite the economic demand, tomato production is largely constrained by various plant pathogens. Among them, root-knot nematodes (RKNs, Meloidogyne spp.) are one of the most economically damaging pests, causing significant yield losses in tomato production [2]. These sedentary endoparasites transform host vascular tissues into giant cells, which act as a sink to provide the nutrients for the completion of their life cycle [3]. This reduces the plant’s ability to uptake nutrients and water from the soil, leading to symptoms such as stunting and chlorosis, ultimately reducing crop yield [4].
Among the Meloidogyne species, M. arenaria, M. hapla, M. incognita, and M. javanica have been the most prevalent in the United States for decades. However, in recent years, several aggressive RKN species, including M. enterolobii, M. floridensis, and M. haplanaria have been detected in multiple vegetable fields across the southern United States [5,6,7,8,9]. Host resistance in commercial vegetable crops, such as tomato, which is effective against M. incognita, has been proven ineffective against these emerging RKN species. Furthermore, the wide host range of these nematode species also limits the management tools like crop rotation with poor or non-host crops. As a result, chemical nematicides have become the primary approach for managing these pests.
Chemical nematicides, including fumigants, have been widely employed to manage RKNs for decades. Methyl bromide, a notable fumigant with high efficacy against plant-parasitic nematodes as well as numerous other pests, was extensively used until its global phaseout in 2015, being a major ozone-depleting substance [10,11]. Alternative fumigants like 1,3-dichloropropene and methyl isothiocyanate-generating compounds, such as metam sodium/potassium, are used in many countries for RKNs management [11]. While these fumigants are effective in managing RKNs, they present challenges such as high costs, supply shortages, complex application procedures, buffer zone requirements (minimum width of 7.6 m), long plant back intervals (interval between the application of fumigants and planting of a crop), and worker safety concerns [10,11,12]. The occupational exposure of these fumigants can often lead to respiratory, eye, and neurological damage in workers [13]. Studies indicate that RKN populations can rebound more rapidly in fumigant-treated plots compared to untreated plots by the end of the cropping season [14,15]. Furthermore, the future use of fumigants is unclear as they are heavily regulated by the Environmental Protection Agency (EPA).
Non-fumigant nematicides offer several advantages over fumigants, including lower application rates, less expensive, easier application methods, and reduced phytotoxicity, making them suitable for both pre- and post-planting applications [11]. Historically, many non-fumigant nematicides used to manage RKNs were organophosphate or carbamate-based. Nematicides from both the organophosphate and carbamate groups affect the central nervous system of nematodes by inhibiting acetylcholinesterase activity. Hence, these pesticides, being linked to the nervous system, are dangerous to humans and non-target organisms and have been withdrawn from using anymore [10,11]. Currently, oxamyl stands as the sole remaining old chemistry non-fumigant nematicide labeled for the management of RKNs in vegetables in the U.S. [16]. To address the need for safer alternatives with novel modes of action, new non-fumigant nematicides, including fluazaindolizine, fluensulfone, and fluopyram, have been developed and labeled for use in various crops [17].
Fluazaindolizine, an imidazopyridine, has specificity with the nematodes, coupled with the absence of activity against target sites of commercial nematicides, suggesting that it has a novel mode of action [18]. Fluensulfone, a member of the fluoroalkenyl thioether group, has an unknown but novel mode of action different than traditional nematicides. Both fluazaindolizine and fluensulfone have irreversible nematicidal effects on the juveniles of RKNs [19]. Fluopyram, a compound belonging to the pyridinyl-ethyl-benzamide group, functions as a succinate dehydrogenase (SDH) inhibitor, leading to nematode paralysis, i.e., it has a nematostatic effect [20].
Previous studies have demonstrated the efficacy of these non-fumigant nematicides in managing the commonly detected RKN species. The sensitivity of RKN species to specific nematicides can vary based on the species and the chemical compound used [21,22,23], highlighting the necessity for species-specific assessments of nematicide efficacy. However, studies on the effectiveness of the non-fumigant nematicides against these aggressive RKN species, such as M. enterolobii, M. floridensis, and M. haplanaria remain limited. Hence, this study was conducted to evaluate the efficacy of four non-fumigant chemical nematicides (fluazaindolizine, fluensulfone, fluopyram, and oxamyl) on the reproduction of recently detected aggressive RKN species, M. enterolobii, M. floridensis, and M. haplanaria, as well as the commonly detected M. incognita under greenhouse conditions.

2. Materials and Methods

2.1. Preparation of Nematode Inoculum

The nematode species used in this study were maintained as pure cultures under controlled greenhouse conditions to avoid cross-contamination. These pure cultures of M. enterolobii, M. floridensis, M. haplanaria, and M. incognita were originally detected in vegetable fields in Georgia and maintained on tomato (Solanum lycopersicum L., cv. ‘Rutgers’) under greenhouse conditions at the University of Georgia, Tifton campus, for three months prior to their use in the experiments. Species identification was carried out using species-specific PCR and DNA sequencing. For M. enterolobii identification, species-specific PCR was carried out using the primers Me-F (5′-AACTTTTGTGAAAGTGCCGCTG-3′) and Me-R (5′-TCAGTTCAGGCAGGATCAACC-3′) [24]. Similarly, M. incognita was identified using the species-specific primers Mi-F (5′-GTGAGGATTCAGCTCCCCAG-3′) and Mi-R (5′-ACGAGGAACATACTTCTCCGTCC-3′) [25]. Meloidogyne floridensis and M. haplanria were identified through DNA sequencing. Briefly, PCR products from the primers TRANH (5′-TGAATTTTTTATTGTGATTAA-3′) and MRH106 (5′-AATTTCTAAAGACTTTTCTTAGT-3′) that amplify a region covering the cytochrome c oxidase subunit II (COII) and the large subunit 16S rDNA (16S) genes [26,27] were sequenced by Eurofins Genomics (Louisville, Kentucky). The DNA sequence for M. floridensis (accession no. MT787563) was 99.76% identical (421/422 bp) to a Florida isolate (accession no. DQ228697). For M. haplanaria, the amplified COII and 16S gene sequence (accession no. OL893015) showed 99.6% identity (510/512 bp) with 100% query coverage to an Arkansas isolate (accession no. DQ228697). The PCR amplification procedures for all of these specific primers to identify the Meloidogyne species were based on the protocols recommended [28]. The three-month-old inoculated plants were uprooted, and the infected roots were rinsed free of soil, chopped into small fragments, and placed on a screen that rested on top of stainless-steel collection pots. The pots were then placed in a mist chamber for 7 days to encourage egg hatching, after which the collected water was passed through nested 149 and 25 μm pore sieves. Fresh second-stage juveniles (J2s) remaining on the 25 μm pore sieve were then collected and enumerated under an inverted compound microscope (ZEISS Axio Vert.A1, Jena, Germany) at 40× magnification [29].

2.2. Nematicides

Fluopyram (Velum® Prime; 41.5%; Bayer CropScience, Research Triangle Park, NC, USA), fluensulfone (Nimitz®; 40%; ADAMA Agricultural Solutions Ltd., Raleigh, NC, USA), fluazaindolizine (Salibro™; 41.15%; Corteva Agriscience, Indianapolis, IN, USA), and oxamyl (Vydate® L; 24%; Corteva Agriscience) were used in the experiments.

2.3. Establishment of the Experiment

Separate trials were conducted for each RKN species under greenhouse conditions at the University of Georgia, Tifton Campus, in summer 2023 and summer 2024. The average daily room temperature during summer 2023 was 29 ± 4 °C and summer 2024 was 27 ± 5 °C. For each nematode species, treatments included four above-mentioned chemical nematicides and RKNs inoculated control without nematicide. Plastic pots with 10 cm diameter were filled with 1 kg sandy loam soil steam-sterilized at 145 °C for 12 h. Twenty-five hundred J2s of RKNs were inoculated in each pot and watered to ensure nematode viability. Tomato seedlings were transplanted seven days after the nematode inoculation. All nematicides, except fluensulfone, were applied on the day of tomato transplantation, seven days post-inoculation. Fluensulfone was applied seven days prior to transplantation and on the same day as nematode, inoculation to prevent potential phytotoxic effects in accordance with the manufacturer’s recommendations. Nematicides were applied at commercial product rate based on manufacturer’s recommendation, which was 2.24 L/ha for fluazaindalizine, 0.30 L/ha for fluopyram, 4.14 L/ha for fluensulfone, and 1.40 L/ha for oxamyl. These application rates were adjusted for the pot scale, with the amount of nematicide applied based on the surface area of each pot. Pots were arranged in randomized complete block design with six replications, and each trial was repeated once for each nematode species. Pots were watered as necessary throughout the experiment to maintain adequate soil moisture. Plants were once fertilized with 2 g of Osmocote smart-release fertilizer (15-9-12; The Scotts Miracle-Gro Company, Marysville, OH, USA) at the time of planting. Knack® (a.i. Pyriproxyfen 11.23%, Valent®, San Ramon, CA, USA) and PQZ® insecticide (a.i. Pyrifluquinazon 20.0%, Nichino America, Wilmington, DE, USA) were applied in rotation at the rate of 65.6 mL a.i./ha and 41.0 mL a.i./ha, respectively, targeting whiteflies. Coragen® (a.i. Chlorantraniliprole 18.4%, FMC Corporation, Philadelphia, PA, USA) was used at a rate of 67.1 mL a.i./ha to control armyworms. All these products were applied as foliar sprays using a backpack sprayer. Based on label information and the available literature, the active ingredients of these insecticides lack nematicidal activity and are, therefore, not capable of directly influencing RKNs reproduction.

2.4. Data Collection

The trials were terminated eight weeks after the nematode inoculation. At harvest, plant materials such as shoots and roots were gently separated from the soil and wrapped in a paper towel. Fresh shoot and root biomass of each plant were then weighed on a measuring scale (Mettler-Toledo, Leicester, UK). Roots were then examined to determine root gall index. Galling indices were based on a combination of rating scales, where 0 = no galls and 1 = 1 to 2, 2 = 3 to 10, 3 = 11 to 30, 4 = 31 to 100 galls. Plants with more than 100 root galls were rated as 5 = 25%, 6 = 50%, and 7 = 75% of roots are galled; 8 = roots are completely galled; 9 = roots are completely galled and rotting; and 10 = dead plant [9]. Nematode eggs were extracted from the plant roots by soaking them in a 1% sodium hypochlorite solution and agitating the roots on an orbital shaker (Thermo MaxQ 2000, Thermo Fisher Scientific, Waltham, MA, USA) at 250 RPM for 4 min to facilitate egg release. Subsequently, the root material and hypochlorite solution were passed through a series of sieves (150 µm, 75 µm, and 25 µm) to separate and retain the nematode eggs, followed by rinsing with tap water to remove any remaining debris. The resulting suspension was then collected in a 50 mL tube, and eggs were counted under an inverted microscope. A similar sieving and decanting methodology followed by centrifugal sugar floatation techniques was used to determine soil juvenile population per 100 cm3 of soil [30]. Eggs were enumerated with a nematode counting slide (Chalex LLC, Park City, UT, USA) under an inverted compound microscope (ZEISS Axio Vert.A1, Jena, Germany) at 40× magnification.

2.5. Data Analysis

Data were analyzed using R studio (version 2021.09.0 Build 351). For each nematode species, nematicides and trials were considered as a fixed effect in a two-way ANOVA, and data of repeated trials of each nematode species were pooled as there was no nematicide × trial effect at p ≤ 0.05. Nematode reproduction data were subjected to log10(x) transformation to meet the assumptions of normality; however, non-transformed values are shown in the tables. Residual analysis was performed to identify and remove outliers. Tukey’s HSD (p ≤ 0.05) was used as post hoc mean comparisons.

3. Results

3.1. Effect of Nematicides on Reproduction and Pathogenicity of RKN Species

3.1.1. Meloidogyne enterolobii

Nematicide treatments had a significant effect on the reproduction of M. enterolobii (Table 1). Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced the total number of eggs per root system by 41.7%, 96.9%, 24.9%, and 23.7%, respectively, compared to the control. Similarly, nematicide treatments significantly reduced the number of eggs per gram of root. Fluazaindolizine, fluensulfone, fluopyram, and oxamyl decreased the egg counts per gram of root by 56.8%, 97.2%, 50.8%, and 41.6%, respectively, relative to the control. Nematicide treatments showed a significant effect on the soil population density of M. enterolobii. Fluazaindolizine and fluensulfone significantly reduced the number of J2s/100 cm3 soil, whereas oxamyl, velum, and control recorded statistically similar numbers of J2s/100 cm3 soil (Table S1). Nematicide treatments also had a significant effect on the root gall index in tomato plants (Table 1). All nematicides resulted in significantly lower root gall indices compared to the control. Among the treatments, fluensulfone produced the lowest root gall index. Although the other nematicides showed comparable gall indices, they were still significantly lower than the control but higher than that of fluensulfone.
Nematicide treatments significantly affected both the root and shoot biomass of tomato plants (Table 1). Fluopyram-treated plants showed a statistically significant increase in root biomass, with 41.7% more root mass compared to the control. Although not statistically significant, plants treated with fluazaindolizine and oxamyl had 17.6% and 11.9% more root biomass, respectively, than the control. Fluopyram-treated plants also had significantly greater shoot biomass, with a 16.8% increase compared to the control. Although not statistically significant, fluazaindolizine-treated plants had 15.0% more shoot biomass than the control. In contrast, fluensulfone-treated plants exhibited 22.5% less shoot biomass relative to the control.

3.1.2. Meloidogyne floridensis

Nematicide treatments significantly affected the reproduction of M. floridensis (Table 2). Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced egg counts by 57.9%, 99.0%, 50.0%, and 62.3%, respectively, compared to the control. Similarly, the number of eggs per gram of root was significantly lesser in nematicide-treated plants. Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced the number of eggs per gram of root by 58.4%, 98.8%, 55.6%, and 63.4%, respectively, relative to the control. All nematicide treatments significantly reduced the number of J2s/100 cm3 soil. Within the nematicide treatments, fluensulfone recorded the lowest number of J2s/100 cm3 soil (Table S1). Nematicide treatments also had a significant effect on the root gall index in tomato plants (Table 2). All nematicides resulted in significantly lower root gall indices compared to the control. Among the treatments, fluensulfone produced the lowest gall index. Although the other nematicides showed comparable gall indices, they were still significantly lower than the control but higher than that of fluensulfone.
Nematicide treatments had a significant effect on fresh root and shoot biomass in tomato plants (Table 2). Although not statistically significant, fluopyram-treated plants showed a 9.7% increase in root biomass compared to the control, while fluensulfone-treated plants had 20% less root biomass. Similarly, fluopyram-treated plants had 8.8% more shoot biomass than the control, though this was not statistically significant, whereas fluensulfone-treated plants recorded 37.6% less shoot biomass relative to the control.

3.1.3. Meloidogyne haplanaria

Nematicide treatments significantly affected the reproduction of M. haplanaria (Table 3). Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced egg counts by 53.8%, 97.8%, 52.6%, and 38.7%, respectively, compared to the control. Similarly, the number of eggs per gram of root was significantly lesser in nematicide-treated plants. Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced the number of eggs per gram of root by 60.0%, 98.0%, 64.6%, and 51.0%, respectively, relative to the control. All nematicide treatments significantly reduced the number of J2s/100 cm3 soil. Within the nematicide treatments, fluensulfone recorded the lowest number of J2s/100 cm3 soil (Table S1). Nematicide treatments also significantly affected the root gall index in tomato plants (Table 3). All nematicides resulted in significantly lower root gall indices compared to the control. Among the treatments, fluensulfone produced the lowest gall index. Although the other nematicides showed comparable gall indices, they were still significantly lower than the control but higher than that of fluensulfone.
Nematicide treatments had a significant effect on both fresh root and shoot biomass of tomato plants (Table 3). Although not statistically significant, Fluazaindolizine, fluopyram, and oxamyl-treated plants exhibited 6.7%, 29.9%, and 9.9% more root biomass, respectively, compared to the control. In contrast, fluensulfone-treated plants had 13.5% less root biomass than the control. Fluopyram-treated plants also had significantly greater shoot biomass, with an increase of 24.8% compared to the control.

3.1.4. Meloidogyne incognita

Nematicide treatments had a significant effect on the reproduction of M. incognita (Table 4). Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced the egg counts by 65.7%, 97.8%, 62.5%, and 58.7%, respectively, compared to the control. Similarly, the number of eggs per gram of root was significantly lesser in the nematicide treatments. Fluazaindolizine, fluensulfone, fluopyram, and oxamyl reduced the number of eggs per gram of root by 68.3%, 97.1%, 71.8%, and 62.1%, respectively, compared to the control. All nematicide treatments significantly reduced the number of J2s/100 cm3 soil than control. Within the nematicide treatments, fluensulfone recorded the lowest number of J2s/100 cm3 soil (Table S1). Nematicide treatments also had a significant effect on the root gall index in tomato plants (Table 4). All nematicides resulted in significantly lower root gall indices compared to the control. Among the treatments, fluensulfone produced the lowest gall index. Although the other nematicides showed comparable gall indices, they were still significantly lower than the control but higher than that of fluensulfone.
Additionally, nematicide treatments significantly affected fresh root and shoot biomass in tomato plants (Table 4). Fluopyram-treated plants showed a significant increase in root biomass, with 21.4% more root mass than the control. Although not statistically significant, plants treated with fluazaindolizine and oxamyl had 11.3% and 10.9% more root biomass than the control, respectively. In contrast, fluensulfone-treated plants exhibited a 30.9% reduction in root biomass relative to the control. At the same time, not statistically significant, fluazaindolizine- and fluopyram-treated plants had 7.3% and 9.4% more shoot biomass than the control, respectively. Fluensulfone-treated plants recorded 21.8% less shoot biomass compared to the control.

4. Discussion

Meloidogyne enterolobii, M. floridensis, and M. haplanaria are emerging threats in vegetable production across the southern United States. These species possess a broad host range, affecting vegetables, weeds, fruit trees, and ornamentals [5,31,32]. Notably, vegetable cultivars that are resistant to M. incognita are not resistant to these species [31,32,33,34], making chemical nematicides a more readily available management option. Due to the environmental and worker safety challenges associated with fumigants, alternative non-fumigant nematicides have been developed to address these issues [10,11,12].
Among the recently released non-fumigant nematicides, fluazaindolizine, fluensulfone, and fluopyram stand out, with fluopyram being the only one with a known mode of action. Fluopyram functions as a succinate dehydrogenase (SDH) inhibitor, leading to nematode paralysis, i.e., nematostatic effect [20]. However, the nematostatic effect is reversible, i.e., it causes temporary paralysis of the nematodes [11]. The precise modes of action of fluensulfone and fluazaindolizine remain unknown. However, studies suggest that they differ from traditional nematicides such as carbamates (e.g., oxamyl) and organophosphates, whose molecular target is acetylcholinesterase. This distinction indicates that fluensulfone and fluazaindolizine are unlikely to inhibit acetylcholinesterase as part of their mode of action. [11,18,19]. Both of these nematicides cause irreversible paralysis (nematicidal effect) in nematodes, significantly reducing their infectivity on plants [11,18,19]. While the efficacy of these non-fumigant nematicides has been tested primarily on common RKN species such as M. incognita, M. javanica, M. arenaria, and M. hapla [11,35], research on their effectiveness against the emerging species mentioned above is limited.
Our study demonstrated that all the non-fumigant nematicides were capable of suppressing the emerging RKN species when applied at the labeled field rates, although the level of suppression varied among them. Fluensulfone was the most consistent and effective, reducing nematode populations by over 90.0% across all species. While the other nematicides also reduced nematode populations, none were as effective or consistent as fluensulfone. This variation highlights potential differences in sensitivity among RKN species to non-fumigant nematicides at their labeled rates. Prior research has indicated that RKN species can exhibit varying sensitivity under in vitro and in vivo conditions when exposed to non-fumigant nematicides. For instance, M. chitwoodi demonstrated lower sensitivity and higher infectivity than M. hapla and M. incognita when treated with sub-lethal doses of fluazaindolizine [23]. Similarly, M. javanica showed reduced sensitivity to fluazaindolizine compared to M. incognita in terms of its ability to move through sand, a key fitness parameter influencing infectivity [21]. Additionally, M. enterolobii was found to be less sensitive to non-fumigant nematicides, exhibiting a higher EC50 value (the concentration required to kill 50% of the nematodes) than M. incognita [22]. These findings, together with our results, indicate that the sensitivity of RKN species to nematicides can vary based on both the species and the specific nematicide applied.
It is important to note that although fluensulfone effectively reduced the egg counts of all nematode species, the root and shoot biomass of plants treated with fluensulfone was significantly lower in most experiments. This reduction in biomass may be attributed to the potential phytotoxic effect of fluensulfone [36,37]. Including a control without nematode infestation would have provided the estimation for the expected fresh root and shoot biomass of unaffected plants, allowing for an estimation of the phytotoxic effects of fluensulfone. While such a control was not included in this study, the consistently low root and shoot biomass observed across all experiments in fluensulfone-treated tomato plants, even under conditions of reduced nematode infestation, suggests that fluensulfone may exhibit some degree of phytotoxicity in tomato plants even if the nematicide is applied seven days before the transplanting. In contrast, while fluopyram was less effective than fluensulfone in suppressing nematode populations, plants treated with fluopyram consistently exhibited greater root and shoot biomass across all experiments. Similar findings have been reported in a previous study [38], where fluopyram-treated tobacco plants showed higher biomass compared to the M. enterolobii-inoculated controls under greenhouse conditions.
In this study, all nematicides were applied at the highest recommended doses as per the manufacturers’ guidelines. The observed phytotoxic effects of fluensulfone in this study may be due to its application at the maximum recommended dose (4.14 L/ha with 40% active ingredient). Future studies exploring a range of fluensulfone doses could provide valuable insights into whether lower doses might reduce phytotoxicity while maintaining efficacy in suppressing Meloidogyne species reproduction. Additionally, investigating the sensitivity of Meloidogyne species to varying concentrations of non-fumigant nematicides would allow for a more detailed comparison of their activities, such as EC50 values. Such studies could provide a further understanding of whether fluensulfone’s effectiveness at reducing nematode populations truly surpasses other nematicides when tested under equivalent concentrations. Although our study demonstrated the suppression of these aggressive RKN species by non-fumigant nematicides, future research should be conducted under infested field conditions to determine whether these nematicides provide similar efficacy in real-world scenarios. Since these aggressive RKN species were detected from only a few locations in Georgia, and the fields were not uniformly infested with a single RKN species, it was not feasible to conduct experiments under open field conditions. It is important to note that our pot experiment offered a more controlled environment, particularly in terms of inoculum levels and final nematode counts, which ensured consistency and minimized variability providing a foundation for the future field trials. Field studies are subjected to greater variability due to environmental and soil-related factors such as soil temperature, precipitation, soil texture, pH, and organic matter content [39,40,41]. Moreover, sublethal doses encountered by nematodes in the field may differ from those used in our assays, as these factors can significantly influence nematicide availability and efficacy. Conducting the study in pots allowed us to assess the efficacy of these nematicides under controlled conditions, providing a foundation for future field trials. Our experiment lasted for eight weeks, which likely allowed two nematode generations to develop. While egg counts were significantly lower in nematicide-treated pots compared to the control, a considerable number of eggs were still produced. In longer cropping seasons, where multiple nematode generations occur, the differences observed in egg counts may diminish over time. This indicates that the effect of nematicides in reducing egg production might be temporary. By the end of the cropping season, the remaining nematode population in the soil could be high enough to cause damage to subsequent crops.
This is the first study to evaluate the effect of non-fumigant nematicides on the reproduction of M. floridensis and M. haplanaria. Additionally, it is the first to assess the impact of non-fumigant nematicides on the reproduction of a Georgia-specific isolate of M. enterolobii. While our study does not directly address yield loss, it provides critical insights into managing emerging Meloidogyne species. Results from this study demonstrate the efficacy of non-fumigant nematicides in suppressing the reproduction of emerging Meloidogyne species, which is a key parameter in nematode management that directly impacts crop yield [42]. Notably, we observed that M. enterolobii is less sensitive to certain nematicides compared to other species. This finding highlights the need for targeted management strategies and serves as a foundation for future research. Further studies, including field trials, can build on this baseline to assess the impact of nematode suppression on yield and to evaluate the cost-effectiveness of these nematicides for growers.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae11010036/s1, Table S1: Effect of nematicides on the population of second-stage juveniles (J2s)/100 cm3 soil.

Author Contributions

Conceptualization, N.P. and I.A.C.; methodology, N.P., L.T. and I.A.C.; formal analysis, N.P.; investigation, N.P.; resources, I.A.C.; data curation, N.P.; writing—original draft preparation, N.P.; writing—review and editing, N.P., L.T., R.F.D., G.B.J., T.M. and I.A.C.; supervision, L.T., R.F.D., G.B.J., T.M. and I.A.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data will be made available upon request.

Acknowledgments

We would like to thank Allan Dondi Umaña and Arnold Aldair Martinez for their help in maintaining the experiment throughout the study.

Conflicts of Interest

The authors declare no conflicts of interest.

References

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Table 1. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. enterolobii in tomato.
Table 1. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. enterolobii in tomato.
TreatmentsNumber of Eggs/Root SystemNumber of Eggs/g RootRoot Gall Index 3Fresh Root Biomass (g)Fresh Shoot Biomass (g)
Fluazaindolizine16,745.4 1 b 21452.3 b4.0 b11.6 ab18.3 bc
Fluensulfone870.6 c93.5 c1.2 c9.8 b15.3 c
Fluopyram21,570.9 ab1655.0 b4.2 b13.9 a22.5 a
Oxamyl21,909.0 ab1963.8 b4.7 b11.0 ab20.8 ab
Control28,727.2 a3364.8 a6.6 a9.8 b18.7 b
p value
Treatment<0.001<0.001<0.001<0.001<0.001
Trial0.090.950.700.690.59
Treatment × Trial0.100.970.590.500.06
1 Values are mean of twelve replications from two trials. 2 Values followed by the same letter within a column are not significantly different according to Tukey’s HSD test (α = 0.05). 3 Root gall indices of tomato following the nematode inoculation (0–10 scale).
Table 2. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. floridensis in tomato.
Table 2. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. floridensis in tomato.
TreatmentsNumber of Eggs/Root SystemNumber of Eggs/g RootRoot Gall Index 3Fresh Root Biomass (g)Fresh Shoot Biomass (g)
Fluazaindolizine12,409.0 1 b 21096.3 b2.9 b11.3 ab24.3 ab
Fluensulfone291.5 c29.4 c0.8 c9.8 b18.2 c
Fluopyram15,000.0 b1171.9 b3.7 b12.9 a27.3 a
Oxamyl11,092.7 b964.6 b3.3 b11.4 ab20.7 bc
Control29,490.9 a2641.0 a6.2 a11.8 ab25.1 b
p value
Treatment<0.001<0.001<0.001<0.001<0.001
Trial0.060.070.080.770.26
Treatment × Trial 0.080.100.150.890.87
1 Values are mean of twelve replications from two trials. 2 Values followed by the same letter within a column are not significantly different according to Tukey’s HSD test (α = 0.05). 3 Root gall indices of tomato following the nematode inoculation (0–10 scale).
Table 3. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. haplanaria in tomato.
Table 3. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. haplanaria in tomato.
TreatmentsNumber of Eggs/Root SystemNumber of Eggs/g RootRoot Gall Index 3Fresh Root Biomass (g)Fresh Shoot Biomass (g)
Fluazaindolizine12,290.9 1 b 21146.5 b2.8 b11.7 ab19.5 ab
Fluensulfone577.1 c55.3 c1.1 c9.6 b18.0 ab
Fluopyram12,609.0 b1014.0 b3.8 b14.2 a23.9 a
Oxamyl16,327.2 b1405.4 b3.4 b12.0 ab19.4 ab
Control26,654.5 a2870.8 a6.0 a10.9 ab19.1 b
p value
Treatment<0.001<0.001<0.0010.0030.005
Trial0.040.070.290.220.97
Treatment × Trial0.070.340.300.220.15
1 Values are mean of twelve replications from two trials. 2 Values followed by the same letter within a column are not significantly different according to Tukey’s HSD test (α = 0.05). 3 Root gall indices of tomato following the nematode inoculation (0–10 scale).
Table 4. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. incognita in tomato.
Table 4. Effect of non-fumigant nematicides on reproduction and pathogenicity of M. incognita in tomato.
TreatmentsNumber of Eggs/Root SystemNumber of Eggs/g RootRoot Gall Index 3Fresh Root Biomass (g)Fresh Shoot Biomass (g)
Fluazaindolizine10,581.8 1 b 2940.4 b2.9 b12.9 ab24.1 a
Fluensulfone659.0 c84.2 c0.5 c7.8 c17.4 b
Fluopyram11,590.0 b835.7 b2.8 b14.5 a24.7 a
Oxamyl12,763.6 b1122.6 b3.5 b12.8 ab22.4 a
Control30,909.0 a2968.4 a5.9 a11.4 b22.3 a
p value
Treatment<0.001<0.001<0.001<0.001<0.001
Trial0.010.0080.350.250.74
Treatment × Trial0.290.330.880.050.40
1 Values are mean of twelve replications from two trials. 2 Values followed by the same letter within a column are not significantly different according to Tukey’s HSD test (α = 0.05). 3 Root gall indices of tomato following the nematode inoculation (0–10 scale).
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Poudel, N.; Torres, L.; Davis, R.F.; Jagdale, G.B.; McAvoy, T.; Chowdhury, I.A. Effect of Non-Fumigant Nematicides on Reproduction of Recently Detected Meloidogyne Species in Georgia Under Greenhouse Conditions in Tomato. Horticulturae 2025, 11, 36. https://doi.org/10.3390/horticulturae11010036

AMA Style

Poudel N, Torres L, Davis RF, Jagdale GB, McAvoy T, Chowdhury IA. Effect of Non-Fumigant Nematicides on Reproduction of Recently Detected Meloidogyne Species in Georgia Under Greenhouse Conditions in Tomato. Horticulturae. 2025; 11(1):36. https://doi.org/10.3390/horticulturae11010036

Chicago/Turabian Style

Poudel, Nabin, Luis Torres, Richard F. Davis, Ganpati B. Jagdale, Theodore McAvoy, and Intiaz A. Chowdhury. 2025. "Effect of Non-Fumigant Nematicides on Reproduction of Recently Detected Meloidogyne Species in Georgia Under Greenhouse Conditions in Tomato" Horticulturae 11, no. 1: 36. https://doi.org/10.3390/horticulturae11010036

APA Style

Poudel, N., Torres, L., Davis, R. F., Jagdale, G. B., McAvoy, T., & Chowdhury, I. A. (2025). Effect of Non-Fumigant Nematicides on Reproduction of Recently Detected Meloidogyne Species in Georgia Under Greenhouse Conditions in Tomato. Horticulturae, 11(1), 36. https://doi.org/10.3390/horticulturae11010036

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