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Article

Efficacy of Foliar Applications of Entomopathogenic Nematodes in the Management of the Invasive Tomato Leaf Miner Phthorimaea absoluta Compared to Local Practices Under Open-Field Conditions

by
Joelle N. Kajuga
1,*,
Bancy W. Waweru
1,
Didace Bazagwira
1,
Primitive M. Ishimwe
1,
Stephano Ndacyayisaba
1,
Grace C. Mukundiyabo
2,
Marie Mutumwinka
1,
Jeanne d’Arc Uwimana
1 and
Stefan Toepfer
3,*
1
Rwanda Agriculture and Animal Resource Development Board, Kigali P.O. Box 5016, Rwanda
2
AgroPy Ltd., Musanze P.O. Box 81, Rwanda
3
CABI, 2800 Delemont, Switzerland
*
Authors to whom correspondence should be addressed.
Agronomy 2025, 15(6), 1417; https://doi.org/10.3390/agronomy15061417
Submission received: 6 May 2025 / Revised: 31 May 2025 / Accepted: 3 June 2025 / Published: 9 June 2025
(This article belongs to the Section Pest and Disease Management)

Abstract

The tomato leaf miner Phthorimaea (syn. Tuta) absoluta (Lepidoptera: Gelechiidae) is invasive in many agricultural regions. Its larvae feed inside leaf mines and tomato fruits, causing yield losses. Repeated sprays of insecticides disrupt agri-ecosystems. Conducting three open-field tomato experiments, we assessed whether formulations of entomopathogenic nematodes could improve the efficacy of these promising biocontrol agents or whether other nature-based agents such as pyrethrin or spinosad would be the better option(s), as compared to a standard insecticide. Steinernema carpocapsae formulated in an alkyl polyglycoside polymeric surfactant, in canola oil, or mixed in both reduced 37 to 68% of pest larvae within two weeks post-treatment, followed by the botanical pyrethrin (48%). Neither spinosad nor lambda cyhalothrin achieved sufficient control. Increasing the frequency of treatments to every two weeks moderately increased efficacy. Positively, the nematodes can, if properly formulated and applied, still be recovered alive from leaf surfaces up to two hours after spraying, indicating that they have time to enter the leaf mines. A small proportion can even be still extracted alive from the leaf mines one week later. Despite these promising results, further research is needed to improve the efficacy of nature-based management options for use against this pest, with the aim of ultimately reducing reliance on chemical insecticides and minimizing the impact on agri-ecosystems.

1. Introduction

The tomato leaf miner Phthorimaea (syn. Tuta) absoluta (Lepidoptera: Gelechiidae) is a pest that affects several solanaceous cash crops, such as tomato (Solanum lycopersicum) and pepper (Capsicum annuum). This pest is native to South America and has invaded large areas of Africa, Europe and Asia [1]. The larvae tunnel through tomato leaves, and the presence of several such mines can cause the leaves to turn brown and die [2]. The larvae can also enter tomato fruits, reducing the marketable value of the harvest.
The larvae are difficult to manage with plant protection products as they feed hidden and protected inside leaves and fruits. Infestation can occur throughout the entire cropping cycle, but is most problematic at fruit set Spraying insecticides during fruits set, which coincides with continuous flowering, is problematic due to the associated risk to pollinators. Spraying on tomato or pepper plants before harvest is restricted by pre-harvest intervals [3,4], which farmers often cannot comply with due to the extended harvesting period of the crop. Phthorimaea absoluta is also known to develop resistance to frequently used insecticides [5]. In such cases, farmers usually increase the dosages and frequencies of sprays. Therefore, alternative, less disruptive pest management tools that do not leave toxic residues are urgently needed to reduce risks to consumers and the environment.
Such pest management tools may include biological control agents such as parasitoids, predatory bugs, and entomopathogenic nematodes (EPNs), or microbial biopesticides such as insecticidal viruses or Bacillus thuringiensis kurstaki or aizwai [6,7]. Nature-based ingredients such as pyrethrin, azadirachtin or spinosad are known to successfully kill Ph. absoluta larvae at least under laboratory or semi-field conditions [8,9]. However, spinosad and pyrethrin do not exhibit a systemic mode of activity and may not effectively reach hidden larvae under open-air farming conditions. In contrast, azadirachtin exhibits a systemic and even translaminar mode of activity, which is more suitable for the control of hidden larvae. Among the biological control agents, EPNs are of particular interest as they can actively search for the target. Many EPN species and strains are known to be highly pathogenic to the larvae of Ph. absoluta [10,11,12]. Several products are registered, such as those based on Streinernema carpocapsae or Steinernema feltiae (Rhabditida: Steinernematidae) [6].
The difficulty of this approach is to develop a practical and effective above-ground application techniques for the usually soil-applied EPNs [13,14]. EPNs are sensitive to desiccation and UV light. Therefore, if applied on above-ground surfaces, they may die before reaching and attacking the pest [11]. Fortunately, behavioural observations have shown that EPNs only need 10 to 15 min to enter the leaf mines of Ph. absoluta (B. Vandenbossche, 2024, pers. comm.). Others scientists believe that up to two hours may be needed for EPNs to enter the mines where pest larvae can be attacked in their hidden environment [11]. It is believed that the protection of sprayed EPN is only needed for a relatively brief period. This is relatively easy to achieve in dense leafy vegetables grown in greenhouses or similar environments [15,16]. It is more challenging for the treatment of tomato or pepper plants in open-field situations. The EPNs would need to be formulated in such a way that the leaf surfaces are covered by the EPN solution, do not dry out within a few hours, and still allow for the movement of the EPNs towards and into the leaf mines. Recently, some progress has been made with EPN formulations. It has been shown that the addition of 1% xanthan gum or 1.5% liquid fire gel concentrate can increase the efficacy of EPN against Ph. absoluta larvae [14]. Recent open-air tomato leaflet bioassays [7] showed that alkyl polyglycoside polymeric surfactants and/or canola oil can improve the efficacy of EPNs.
Therefore, building on the few existing studies, we aimed to further study the use of EPN formulations against Ph. absoluta larvae and to compare them to local pest management practices, as well as other nature-based solutions. The EPN S. carpocapsae was chosen as it is one of the most robust with regard to surviving environmental stress. We then aimed (i) to test polyglycoside polymeric surfactants and canola oil formulations of the EPN for their suitability for application to tomato leaves against the larvae of this pest, (ii) to compare the efficacy levels with those of pyrethrin, spinosad, and a standard insecticide, and (iii) to investigate whether applied EPNs can survive on or inside the leaves. We hope that our findings will pave the way for the development of commercial EPN-based biocontrol solutions for use against this devastating leaf miner.

2. Material and Methods

2.1. Target Crop and Field Sites

The target crop was tomato (Solanum lycopersicum; Solanales: Solanaceae) (Figure 1). Seedlings of the tomato variety Rio Grande were raised by the Rwanda–Israel Horticulture Centre of Excellence in Kigali. Seedlings at 3-to-5-leaf stage were transplanted to experimental fields. Tomato plants were planted 50 cm apart at a 60 cm row distance in 2023 and 60 cm apart at a 60 cm row distance in 2024. This planting density corresponded to approximately 33,000 plants per hectare in 2023 and 28,000 plants per hectare in 2024. The plants were not staked.
In total, three open tomato fields naturally infested with Ph. absoluta were used to set up controlled, systematically arranged plot trials, referred to as field 1 in 2023 and fields 2 and 3 in 2024. Field 1 was situated in Mareba in the Bugesera district in eastern Rwanda, and fields 2 and 3 in Mututu in the Nyanza district in southern Rwanda. The experiment in field 1 was conducted in November 2023 during cropping season A. This is the short rain season, with regular rains totalling up to 110 to 160 mm per month in eastern Rwanda. The temperature in this period is typically between 16 °C and 27 °C with peaks above 30 °C during daytime. Those conditions appeared to be sub-optimal for the present study because of the high incidence of Phytophthora disease. Therefore, the experiments in fields 2 and 3 were implemented at the end of the cropping season C in September 2024. This is the end of the dry season and requires manual irrigation. During September, it usually rains 10 to 12 times in southern Rwanda (60–70 mm). The temperature in this period is typically between 19 °C and 28 °C.
In all experiments, mechanical weeding was implemented 3 times, and mulching with dry grass was applied twice. A mixture of metalaxyl-M and mancozeb was sprayed up to 4 times during the cropping season to prevent Phytophthora, as well as fungal infections. No insecticides were applied except the experimental treatments.

2.2. Target Pest

The study target were larvae of the tomato leaf miner, Phthorimaea (synonym Tuta) absoluta (Lepidoptera: Gelechiidae). Naturally infested tomato fields were used (Figure 1 and Figure 2). At the start of each experiment, the number of leaflets with damage symptoms was recorded, as well as larvae inside the leaflets, by checking tunnels and leaf lesions against light.

2.3. Treatments

In total, 6 different agents or ingredients were studied against Ph. absoluta larvae (Table 1). This included the EPN Steinernema carpocapsae (Rhabditida: Steinernematidae) as a biocontrol agent, formulated in a foamy surfactant with and without an UV protectant of canola oil. Furthermore, the study included the botanical pyrethrin, the natural-source product spinosad, and an untreated negative control. The standard insecticide lambda-cyhalothrin served as a positive control (Table 1).
All treatments were applied as fluid flat-sprays onto tomato leaves using 2-litre spray bottles or 3-litre knapsack sprayers. In total, 10 to 15 mL were applied per plant, achieving good coverage across all leaves, equalling about 330 to 420 litres per hectare. Treatments were repeated for a second time 14 days after the first treatment. The first treatments were applied at the 10 ± 3 leaf stage, just before the start of flowering, and the second treatment at the 16 ± 3 leaf stage, which coincides with the early flowering stage. The latter represented sub-optimal timing, because of potential non-target effects of the insecticides on pollinators. But it was good for targeting Ph. absoluta larvae. More repetitions of the treatments were not applied due to restrictions on pyrethrin, spinosad, and lambda-cyhalothrin regarding pollinator protection and pre-harvest intervals.
The EPN S. carpocapsae was used in the experiments [17] as it is one of the most robust EPN with regard to surviving environmental stress such as desiccation or UV light. Several strains of this EPN species have been reported to be highly pathogenic to larvae of Ph. absoluta [11], including the EPN used in this study [10]. The EPNs were reared in-vivo on larvae of Galleria mellonella (Lepidoptera: Pyralidae) or in-vitro on media-soaked sponges in flasks [18]. Harvested infective juveniles (IJ) of EPN were stored in tissue culture flasks at 16 °C for no more than one month before use. Different batches of EPN were used for the experiments. In total, 1800 EPNs were prepared per ml for treatments in field 1 in 2023 and 1000 EPNs per ml for fields 3 and 4 in 2024. In 2023, 18,000 EPN were applied at 10 mL per plant, leading to a total of about 0.6 billion in 330 litres per hectare. In 2024, 15,000 EPN were applied at doses of 15 mL per plant, with a total of about 0.4 billion per 420 litres per hectare. In 2023, EPNs were formulated in a high-dose alkyl polyglycoside surfactant that led to a foamy coverage of leaves after spray or in a low dose of UV-protecting canola oil. In 2024, EPNs were formulated either in the alkyl polyglycoside surfactant or in the same surfactant mixed with high-dose canola oil as a UV protectant (Table 1).

2.4. Experimental Setup

Each of the three experiments in open-air tomato fields was set up as a controlled systematic plot trial following the standard protocols of testing plant protection products [19] (Figure 2).
In detail, each experiment comprised 4 repetitions as plots per treatment. Each plot of about 1.8 or 2 × 6 m had 3 rows of 10 plants. This equals 120 plants per treatment per field. The plots were arranged in a systematic block design. Treatments were carried out across the entire 3 rows of plants per plot. No bare soil and plant-free buffers were installed between plots to ensure a realistic tomato production field. The first and third rows of a plot served as the treated buffer, as well as the first and last plants of the inner row. Data were only collected from 8 of 10 plants from the inner of the three rows of each plot. This led to a sample size of 24 assessed plants per treatment for each of the three experimental repetitions.

2.5. Assessing Control Efficacy

Data were collected at the start of the experiments, as well as on days 7 and 14 after each of the treatment dates (Figure 1). Data were collected from 8 to 10 plants of the middle row of each plot. Data collection was conducted in a single-blind manner, as far as possible (Figure 2).
The number of leaflets with mines and lesions typical of Ph. absoluta larvae were recorded [20]. Moreover, the number of living and dead larvae inside the leaf mines and lesions were assessed on all the leaflets of 3 leaves per plant in 2023 and on all the leaflets of one middle level leaf per plant in 2024. As most of the leaves and nearly all of the tomato plants were infested, it was considered sufficiently precise to assess the leaflets of one leaf per plant (which usually have seven) in the 2024 trials compared to three leaves in the 2023 trials. To record the larvae, the leaves were held against the light. Living larvae are usually of a grey-green colour and move when touched with a pin, while dead larvae often become darker as they start to decompose. At the first harvest, damaged fruits were assessed, as well as the weight of all yellow to red fruits hanging on a plant. The first harvest was considered the most informative as it was closest to the treatment dates. Protecting the tomato yield throughout the harvesting season would be problematic due to pre-harvest interval restrictions for botanical and chemical treatments.
Plant phenological stages, including plant height and width, were recorded weekly, as well as phytotoxicity symptoms such as chlorosis or other colour changes, necrosis, and changes in growth (Figure 1).

2.6. Assessing the Survival of EPN

The survival of the EPNs was assessed in the sprayer before and after treatment by taking 3 sets of 1 mL samples from each of the EPN-formulation types of treatments. Furthermore, EPNs were washed off with 10 mL water sprays into sample tubes from 3 leaflets per treatment approximately 30 min after spraying once dried, and again after 1 to 2 h. Finally, 3 leaflets were collected from 3 plants per EPN treatment at 7 and 14 days after each of the two treatments and then submersed into 5 mL of water in glass tubes for 3 to 4 h. Back at the laboratory, all samples were allowed to sediment for 20 min. Then, six sub-samples of 10 µL each were taken and observed under a stereomicroscope to calculate the living and dead EPNs per volume and per leaflet. An EPN was considered alive when moving and/or being curved or being straight but having slightly curved ends. An EPN was considered dead when it was entirely straight and/ or contained air bubbles in the body or when it showed signs of decomposition. Moreover, only nematodes of similar size were considered, reducing the chance of potentially recording saprophytic nematodes, which are, however, unlikely to be recovered from leaf surfaces.

2.7. Data Analyses

Damage and larvae data were standardised to per-leaflet proportional data, to per-leaf proportional data, and to per-plant proportional data. Data about the effects of treatments were normalized to the data of the negative control to reduce the potential effects of natural variation within and between experiments. This allowed for the pooling of data across experiments while not neglecting site-specific factors in the factorial analyses (Table 2). Data and skewness and kurtosis of residuals were observed using quantile–quantile plotting. Equality of variances was assessed using Levene’s test. The effects of treatments were analysed using one-way ANOVA. As most data appeared to have un-equal variances among treatments, the Games–Howell post hoc multiple comparison was applied. IBM SPPS statistical software 13 was used [21].

3. Results

A heavy pest infestation by Ph. absoluta was found in all three study fields from the start of the experiments onwards. In fields 1 and 3, each tomato plant was found to be infested, and 98% of plants in field 2. In field 1, 1.1 to 1.8 larvae were recorded per 10 tomato leaves per plant at day 0 and day 14 of the experiment, 6.2 to 7.8 larvae in field 2, and 10 to 5.6 larvae in field 3. The highest larvae numbers and most damage were found at the young vegetative crop stage (Figure 1).

3.1. Control Efficacy

Treatments reduced the number of pest larvae and the quantity of damaged fruits at harvest (Table 2). Neither treatment reduced the proportion of damaged leaves or leaflets of tomato plants or influenced the yield in terms of the weight of harvested tomatoes per plant.
In detail, the EPNs, which were formulated in an alkyl polyglycoside polymeric surfactant, in canola oil, or in a mix of both, reduced the pest larvae by 37 to 68% within two weeks of treatment (Figure 3). The formulation of the EPNs had no influence. The botanical pyrethrin achieved comparable efficacies (48%) to the EPNs. Spinosad and lambda-cyhalothrin did not achieve such effects.
An increasing frequency of treatments from one to two treatments increased the level of prevention of leaf or leaflet damage, as well as increasing the efficacies of larvae reduction. Field sites and their pest population levels also affected some of the efficacy data (Table 2).

3.2. EPN Survival

Only 6 ± 4.4% mortality of EPNs was observed for the surfactant formulations, and 8 ± 2.9% mortality was observed for the surfactant–oil formulations during preparation in the sprayers prior to the treatment (Figure 4). EPN mortality slightly increased to 16 to 20% during spraying and to 18 to 25% on the sprayed leaf surfaces from 30 min up to 2 h after spraying (between subject ANOVA “Time”, F 2; 61 = 7.8, p = 0.01). The formulation had no influence on the survival of the EPNs at each time step (between subject ANOVA “Formulation”, F 1;61 = 2.6, p = 0.11; see Figure 4 and Figure 5).
Many of the applied EPNs were found to still be alive on the tomato leaves from around 30 min up to 2 h after treatment, independent of the formulation (Figure 5). Specifically, 45–55% of the EPNs were recovered after 30 min and 42–49% after 1–2 h. This is, 123 ± 31 EPN formulated in alkyl polyglycoside and canola oil and 102 ± 22 EPN in alkyl polyglycoside were washed from a leaflet 30 min after spraying 500 to 600 EPNs per leaflet or 15,000 per plant. Within 1 to 2 h after spraying, this accounted for around 101 and 87 EPNs, respectively.
A small proportion (0.35 to 0.1%) of the EPNs was still extracted from inside the treated leaves about one week after treatment.

4. Discussion

Due to the widespread invasion of the tomato leaf miner Ph. absoluta into many agricultural regions [13,22], the pesticide burden has further increased in cash crops including tomato or pepper, despite already being heavily managed [3]. Repeated sprays of insecticides are often needed against this pest as only the hatching larvae can be effectively controlled before they enter the leaves or fruits [23]. This is problematic because Ph. absoluta adults can lay eggs over a relatively long period of up to two weeks and /or may have overlapping generations [24]. This leads to the need for repetitive sprays, which are particularly problematic when reaching the harvesting period due to pre-harvest interval restrictions. Less disruptive pest management options are urgently needed that are either not toxic or break down quickly in the environment.
Our study showed that EPN can, if properly formulated, find the pest larvae in the leaf mines and reduce them by 37 to 68%. Only a few studies are available on EPN usage against Ph. absoluta under open-field conditions, but the efficacy reported here seems comparable to findings from previous research [8,25]. In Morocco, one study [25] reported a 60 to 80% reduction in larvae in field tomatoes by steinernematid or hetororhabdit nematodes. In Rwanda, [8] did not assess larvae, but observed an approximately 10 to 50% reduction in leaf and leaflet damage when using S. carpocapsae under field conditions. EPN efficacies may be higher under the protected and high-humidity conditions of greenhouses [26] and are naturally also higher under laboratory conditions, as many studies have shown [27,28]. Protective formulations are needed for EPNs to reach sufficient efficacies for above-ground treatment under field conditions. The here-tested formulations, such as polyglycoside polymeric surfactants and canola oil, were chosen based on previous studies [7] and seem to have indeed improved the efficacy of the applied EPNs under the open-field conditions reported here. Our data show that the applied EPNs remain alive on the sprayed tomato leaves for up to 2 h, even under the sunny, dry, open-field conditions of tomato cultivation. Temperatures at the studied sites typically range from 16 to 28 °C in terms of daily averages, but they frequently reach above 30 °C during daytime with moderate UV indices.
Our results confirm those of [14], who proposed that EPNs can move on a sprayed leaf towards the leaf mines with Ph. absoluta larvae under open-field conditions, as well as protected conditions. Our study also showed that a small proportion of EPNs can be still extracted alive from the larvae up to one week after treatment. This suggests that some EPNs successfully entered the leaf mines created by the pest larvae. However, the successful propagation of EPNs on the relatively small larvae of this pest in the leaf mines is probably limited or unlikely [25]. The killed larvae decompose and potentially dry out in the leaf mines. This is confirmed by our difficulties in properly observing and recording the dead larvae and in calculating mortality precisely, although the overall reduction in larvae populations was evident. Moreover, even in cases of the successful propagation of the next generation, EPN may only be able to attack larvae in the same leaf mines but are unlikely to exit a leaf to search for other mines and larvae. Therefore, the proposed use of EPNs is comparable to pesticide treatments, which may need to be repeated if a pest population reaches the threshold again. The obvious advantage of EPNs is that they can search for the larvae protected in the leaf mines, do not leave problematic residues on the crop and the harvest, and are not problematic for pollinators or the wider environment.
The here-reported efficacies of larval control were not reflected in the sufficient prevention of leaf damage, particularly not at high pest densities. On the one hand, this may be due to the assessment method of recording the percentages of attacked leaves or leaflets instead of quantitatively recording the area, length, or number of leaf mines caused by Ph. absoluta on each leaf. The latter method would have been too laborious when assessing the effects of treatments on damage. On the other hand, further improvements in application techniques for EPNs may be needed. One may argue that different EPN strains should be further tested under harsh open-field conditions, focusing on the numerous EPNs known to be pathogenic to Ph. absoluta larvae [25,29]. However, the here-chosen S. carpocapsae is known to be among the EPN species that are comparatively tolerant to environmental stress [30,31] and are among the EPNs with longest shelf life [32]. Therefore, it may be difficult to find better EPNs for open-field applications. Nevertheless, [25] reported that S. feltiae might be another promising option. With regard to formulations, further types of fluid gel-type formulations may need testing, such as liquid gels, dense adjuvant-based formulations [33], and other UV protectants such as titanoxide [34] or plant-derived protectants [35]. Finally, it needs to be stated that the three experimental repetitions undertaken in our study are not sufficient to statistically assess the influence of other factors such as pest infestation levels, cropping practices, or environmental factors such as temperature or rainfall, calling for more studies.
One may also argue that other biological control agents such as insecticidal viruses or bacteria [36] or entomopathogenic fungi [27,29], as well as predators or parasitoids [22], might be options to further pursue. Insecticidal viruses and bacteria exist for the control of Ph. absoluta larvae [6] and have the advantage of being easy to store, handle, and apply. They are also less likely to suffer from environmental stress than EPN. However, the larvae must ingest these agents before they enter the leaf mines or fruits. Therefore, the timing of such treatments is a challenge, as it is with pesticides. Moreover, entomopathogenic fungi must come into contact with the pest larvae and need moist conditions to thrive. This is possible under greenhouse conditions but less likely under open-field conditions [37]. The use of several predatory bugs or parasitoids has shown relatively high efficacy against Ph. absoluta larvae or eggs [38,39]. All of those are environmentally friendly options and do not leave residues on the harvest. The latter point is crucial, as the damage caused by Ph. absoluta larvae is economically the most problematic when reducing the quality of harvested, to-be-sold tomatoes. However, their efficacy, practicability, availability and costs may need to be evaluated versus the use of EPNs or other control options.
For example, some botanicals or other nature-based ingredients maybe be less toxic compared to many pesticides and/or may break down more easily in the environment [9]. We therefore also included pyrethrin botanicals and spinosad in our study to determine whether they would be the better choice compared to the EPNs or standard insecticides. The botanical pyrethrin also reduced about half of the population of pest larvae in the here-studied open field conditions, as did the EPNs. This result was unexpected, as pyrethrin is a contact insecticide with limited residual activity, and, to our knowledge, it has not been reported to act translaminarily or systemically. Although pyrethrin likely killed some young larvae on the surface of leaves, this probably cannot explain the efficacy found here. It may be that the pyrethrin fluids sprayed onto the leaves entered some cracked or brittle leaf mines. The question remains as to why spinosad and lambda-cyhalothrin did not do the same. The disadvantage of pyrethrin is that it exhibits broad-spectrum activity, endangering non-target organisms and particularly pollinators. The advantage is that it breaks down faster than many synthetic pesticides and is easier to handle than some biological control products such as EPNs. In contrast to pyrethrin, the other insecticides tested and reported here, spinosad and lambda-cyhalothrin, did not achieve any major control efficacies or damage reductions, even not after a repeated spray within two weeks. Both ingredients also work on contact and are neither systemic nor translaminar. Therefore, larvae reduction can, as explained above, only be achieved using chemical sprays, insecticidal viruses, and bacteria against neonates just hatching from eggs, which is difficult to predict.

5. Conclusions

Managing Ph. absoluta larvae under open-field and realistic farming conditions remains difficult, despite the progress reported here and elsewhere [7,35,39]. To avoid residues on the harvest, as well as environmental contamination, biological control agents should be the preferred choice. The choice of biological control agents will depend on their local availability, the practicality of their handling, their efficacies, and their prices in the different regions. Despite the promising options and results, further research and development seem necessary to further improve the efficacy of nature-based management options, such as EPNs, against this pest. This will ultimately allow us to reduce both our reliance on chemical insecticides and their impact on agri-ecosystems.

Author Contributions

Conceptualization, J.N.K., B.W.W., G.C.M. and S.T.; methodology, J.N.K., B.W.W., M.M., P.M.I., D.B., G.C.M., J.d.U., S.N. and S.T.; data collection, J.N.K., M.M., P.M.I., D.B., J.d.U. and S.N.; data analysis and interpretation, S.T. and B.W.W.; original draft preparation, S.T.; review and editing, J.N.K., B.W.W., M.M., P.M.I., D.B., G.C.M. and S.T.; funding acquisition, B.W.W., J.N.K., M.M. and S.T. All authors have read and agreed to the published version of the manuscript.

Funding

This activity was carried out with the aid of a grant from the International Development Research Centre, Ottawa, Canada through the collaboration between the African Center for Technology Studies (ACTS) and the National Council for Science and Technology NCST of Rwanda (ACTS_RIMP_NCST-NRIF_RAB_2023), as well as from the CABI-led PlantwisePlus programme, which is financially supported by tax payers behind the following agencies: the Directorate General for International Cooperation, Netherlands (DGIS); European Commission Directorate General for International Partnerships (INTPA); the Foreign, Commonwealth and Development Office (FCDO) from the UK government; the Swiss Agency for Development and Cooperation (SDC).

Data Availability Statement

Datasets used and analysed during the current study are available from the corresponding author upon request.

Acknowledgments

We would like to thank the Biocontrol Facility at RAB in Rubona for providing entomopathogenic nematodes, as well as AgroPy ltd., Rwanda, for providing formulations and botanical plant protection products. We thank Geraldine Ingabire and Anatole Uwiringiye for their help in the biocontrol facility at RAB, the tomato farmers for their help with the field work, and the Mututu RAB station for help in setting up the experiment. We also thank Patrick Fallet (University of Neuchatel, Switzerland) for his practical advice on formulations for EPNs.

Conflicts of Interest

The author Grace C. Mukundiyabo is employed by the company AgroPy Ltd., Musanze, Rwanda. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Abbreviations

The following abbreviations are used in this manuscript:
EPNEntomopathogenic nematodes
IJInfective juveniles

References

  1. Ponti, L.; Gutierrez, A.P.; De Campos, M.R.; Desneux, N.; Biondi, A.; Neteler, M. Biological Invasion Risk Assessment of Tuta absoluta: Mechanistic versus Correlative Methods. Biol. Invasions 2021, 23, 3809–3829. [Google Scholar] [CrossRef]
  2. Bajracharya, A.S.R.; Mainali, R.P.; Bhat, B.; Bista, S.; Shashank, P.R.; Meshram, N.M. The First Record of South American Tomato Leaf Miner, Tuta absoluta (Meyrick 1917) (Lepidoptera: Gelechiidae) in Nepal. J. Entomol. Zool. Stud. 2016, 4, 1359–1363. [Google Scholar]
  3. Karimi, P.; Sadeghi, S.; Kariminejad, F.; Sadani, M.; Sheikh Asadi, A.M.; Oghazyan, A.; Bay, A.; Mahmudiono, T.; Fakhri, Y. The Concentration of Pesticides in Tomato: A Global Systematic Review, Meta-Analysis, and Health Risk Assessment. Environ. Sci. Pollut. Res. 2023, 30, 103390–103404. [Google Scholar] [CrossRef] [PubMed]
  4. Elgueta, S.; Valenzuela, M.; Fuentes, M.; Meza, P.; Manzur, J.P.; Liu, S.; Zhao, G.; Correa, A. Pesticide Residues and Health Risk Assessment in Tomatoes and Lettuces from Farms of Metropolitan Region Chile. Molecules 2020, 25, 355. [Google Scholar] [CrossRef]
  5. Adhikari, D.; Subedi, R.; Gautam, S.; Pandit, D.P.; Sharma, D.R. Monitoring and Management of Tomato Leaf Miner (Tuta absoluta, Meyrick) in Kavrepalanchowk, Nepal. J. Agric. Environ. 2019, 20, 1–9. [Google Scholar] [CrossRef]
  6. CABI Bioprotection Portal. Available online: https://bioprotectionportal.com/ (accessed on 30 January 2025).
  7. Waweru, B.W.; Kajuga, J.N.; Hategekimana, A.; Ndereyimana, A.; Kankundiye, L.; Umulisa, C.; Nyombayire, A.; Mutumwinka, M.; Ishimwe, P.M.; Bazagwira, D. Formulation of Entomopathogenic Nematodes for Above-Ground Use Against Tomato Leaf Miner, Phthorimaea absoluta. Insects 2025, 16, 189. [Google Scholar] [CrossRef]
  8. Ndereyimana, A.; Nyalala, S.; Murerwa, P.; Gaidashova, S. Field Efficacy of Entomopathogens and Plant Extracts on Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) Infesting Tomato in Rwanda. Crop Prot. 2020, 134, 105183. [Google Scholar] [CrossRef]
  9. Jallow, M.F.A.; Dahab, A.A.; Albaho, M.S.; Devi, V.Y. Efficacy of Some Biorational Insecticides against Tuta Absoluta (Meyrick) (Lepidoptera: Gelechiidae) under Laboratory and Greenhouse Conditions in Kuwait. J. Appl. Entomol. 2019, 143, 187–195. [Google Scholar] [CrossRef]
  10. Ndereyimana, A.; Nyalala, S.; Murerwa, P.; Gaidashova, S. Potential of Entomopathogenic Nematode Isolates from Rwanda to Control the Tomato Leaf Miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Egypt. J. Biol. Pest Control 2019, 29, 57. [Google Scholar] [CrossRef]
  11. Abonaem, M. Selection, Optimization and Technical Application of Entomopathogenic Nematodes for the Biological Control of Major Insect Pests on Tomato; TU Darmstadt: Darmstadt, Germany, 2021. [Google Scholar]
  12. Dlamini, B.E.; Dlamini, N.; Masarirambi, M.T.; Kwanele, A.N. Control of the Tomato Leaf Miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) Larvae in Laboratory Using Entomopathogenic Nematodes from Subtropical Environment. J. Nematol. 2020, 52, e2020-13. [Google Scholar] [CrossRef]
  13. Han, P.; Bayram, Y.; Shaltiel-Harpaz, L.; Sohrabi, F.; Saji, A.; Esenali, U.T.; Jalilov, A.; Ali, A.; Shashank, P.R.; Ismoilov, K.; et al. Tuta Absoluta Continues to Disperse in Asia: Damage, Ongoing Management and Future Challenges. J. Pest Sci. 2019, 92, 1317–1327. [Google Scholar] [CrossRef]
  14. Ben Husin, T.O.A. Biological Control of Tomato Leaf Miner Tuta absoluta Using Entomopathogenic Nematodes. Ph.D. Thesis, Newcastle University, Newcastle Upon Tyne, UK, 2017. [Google Scholar]
  15. Schroer, S.; Ziermann, D.; Ehlers, R.U. Mode of Action of a Surfactant-Polymer Formulation to Support Performance of the Entomopathogenic Nematode Steinernema carpocapsae for Control of Diamondback Moth Larvae (Plutella yylostella). Biocontrol Sci. Technol. 2005, 15, 601–613. [Google Scholar] [CrossRef]
  16. Briar, S.S.; Antwi, F.; Shrestha, G.; Sharma, A.; Reddy, G.V.P. Potential Biopesticides for Crucifer Flea Beetle, Phyllotreta cruciferae (Coleoptera: Chrysomelidae) Management under Dryland Canola Production in Montana. Phytoparasitica 2018, 46, 247–254. [Google Scholar] [CrossRef]
  17. Yan, X.; Waweru, B.; Qiu, X.; Hategekimana, A.; Kajuga, J.; Li, H.; Edgington, S.; Umulisa, C.; Han, R.; Toepfer, S. New Entomopathogenic Nematodes from Semi-Natural and Small-Holder Farming Habitats of Rwanda. Biocontrol Sci. Technol. 2016, 26, 820–834. [Google Scholar] [CrossRef]
  18. Devi, G. Mass Production of Entomopathogenic Nematodes—A Review. Int. J. Environ. Agric. Biotechnol. 2018, 3, 1032–1043. [Google Scholar] [CrossRef]
  19. EPPO. Design and Analysis of Efficacy Evaluation Trials. EPPO Bull. 2007, 37, 11–24. [Google Scholar] [CrossRef]
  20. Gharekhani, G.H.; Salek-Ebrahimi, H. Evaluating the Damage of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on Some Cultivars of Tomato under Greenhouse Condition. Arch. Phytopathol. Plant Prot. 2014, 47, 429–436. [Google Scholar] [CrossRef]
  21. Kinnear, P.R.; Gray, C.D. SPSS for Windows Made Simple; Psychology Press Ltd.: Hove, UK, 2000. [Google Scholar]
  22. Tarusikirwa, V.L.; Machekano, H.; Mutamiswa, R.; Chidawanyika, F.; Nyamukondiwa, C. Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on the “Offensive” in Africa: Prospects for Integrated Management Initiatives. Insects 2020, 11, 764. [Google Scholar] [CrossRef]
  23. Steyn, L.A.I.; Geertsema, H.; Malan, A.P.; Addison, P. A Review of Leaf-Mining Insects and Control Options for Their Management, with Special Reference to Holocacista capensis (Lepidoptera: Heliozelidae) in Vineyards in South Africa. S. Afr. J. Enol. Vitic. 2020, 41, 218–232. [Google Scholar] [CrossRef]
  24. Martins, J.C.; Picanço, M.C.; Bacci, L.; Guedes, R.N.C.; Santana, P.A.; Ferreira, D.O.; Chediak, M. Life Table Determination of Thermal Requirements of the Tomato Borer Tuta absoluta. J. Pest Sci. 2016, 89, 897–908. [Google Scholar] [CrossRef]
  25. El Aimani, A.; Mokrini, F.; Houari, A.; Laasli, S.E.; Sbaghi, M.; Mentag, R.; Iraqi, D.; Udupa, S.M.; Dababat, A.A.; Lahlali, R. Potential of Indigenous Entomopathogenic Nematodes for Controlling Tomato Leaf Miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under Laboratory and Field Conditions in Morocco. Physiol. Mol. Plant Pathol. 2021, 116, 101710. [Google Scholar] [CrossRef]
  26. Batalla-Carrera, L.; Morton, A.; Garcia-del-Pino, F. Efficacy of Entomopathogenic Nematodes against the Tomato Leafminer Tuta absoluta in Laboratory and Greenhouse Conditions. Biocontrol 2010, 55, 523–530. [Google Scholar] [CrossRef]
  27. Youssef, N.A. Efficacy of the Entomopathogenic Nematodes and Fungi for Controlling the Tomato Leaf Miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Arab. Univ. J. Agric. Sci. 2015, 23, 591–598. [Google Scholar] [CrossRef]
  28. Kaşkavalcı, G.; Türköz, S. Determination of the Efficacy of Some Entomopathogenic Nematodes against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under Laboratory Conditions. Turk. J. Entomol. 2016, 40. [Google Scholar] [CrossRef]
  29. Ndereyimana, A.; Nyalala, S.; Murerwa, P.; Gaidashova, S. Pathogenicity of Some Commercial Formulations of Entomopathogenic Fungi on the Tomato Leaf Miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Egypt. J. Biol. Pest. Control 2019, 29, 70. [Google Scholar] [CrossRef]
  30. Lello, E.R.; Patel, M.N.; Matthews, G.A.; Wright, D.J. Application Technology for Entomopathogenic Nematodes against Foliar Pests. Crop Prot. 1996, 15, 567–574. [Google Scholar] [CrossRef]
  31. Kung, S.P. Abiotic Factors Affecting the Persistence of Two Entomopathogenic Nematodes, Steinernema carpocapsae, and Steinernema glaseri (Nematoda:Steinernematidae) in the Soil. Diss. Abstr. International. B Sci. Eng. 1990, 51, 1620. [Google Scholar]
  32. Grewal, P.S. Formulations of Entomopathogenic Nematodes for Storage and Application. Nematol. Res. 1998, 28, 68–74. [Google Scholar] [CrossRef]
  33. Metwally, H.M.S.; Saleh, M.M.E.; Abonaem, M. Formulation for Foliar and Soil Application of Entomopathogenic Nematodes for Controlling the Onion Thrips Thrips tabaci Lindeman (Thysanoptera: Thripidae). Egypt. J. Biol. Pest Control 2025, 35, 4. [Google Scholar] [CrossRef]
  34. Kotliarevski, L.; Cohen, R.; Ramakrishnan, J.; Wu, S.; Mani, K.A.; Amar-Feldbaum, R.; Yaakov, N.; Zelinger, E.; Belausov, E.; Shapiro-Ilan, D.; et al. Individual Coating of Entomopathogenic Nematodes with Titania (TiO2) Nanoparticles Based on Oil-in-Water Pickering Emulsion: A New Formulation for Biopesticides. J. Agric. Food Chem. 2022, 70, 13518–13527. [Google Scholar] [CrossRef]
  35. Ha, B.; Wei, X.; Lu, P.; Qing, H.; Guo, J.; Zhang, R.; Chen, L.; Li, X.; Hu, B.; Wang, S.; et al. Natural UV Protectants and Humectants to Improve the Efficiency of Steinernema carpocapsae in Controlling Foliar Pests. Pest Manag. Sci. 2025, 81, 1422–1431. [Google Scholar] [CrossRef] [PubMed]
  36. Teixido, N.; De Cal, A.L.; Usall, J.; Guijarro, B.; Larena, I.; Torres, R.; Abadias, M.; Kohl, J. Biocomes: New Biological Products for Sustainable Farming and Forestry. III Int. Symp. Postharvest Pathol. 2016, 1144, 469–472. [Google Scholar] [CrossRef]
  37. Urbaneja, A.; Gonzalez-Cabrera, J.; Arno, J.; Gabarra, R. Prospects for the Biological Control of Tuta absoluta in Tomatoes of the Mediterranean Basin. Pest Manag. Sci. 2012, 68, 1215–1222. [Google Scholar] [CrossRef] [PubMed]
  38. Varshney, R.; Budhlakoti, N. Evaluation of the Potential of Predatory Mirid Bug, Dortus Primarius Distant as Biocontrol Agent of Tuta absoluta Meyrick. J. Plant Dis. Prot. 2025, 132, 50. [Google Scholar] [CrossRef]
  39. Nozad-Bonab, Z.; Hejazi, M.J.; Iranipour, S.; Arzanlou, M.; Biondi, A. Lethal and Sublethal Effects of Synthetic and Bio-Insecticides on Trichogramma brassicae Parasitizing Tuta absoluta. PLoS ONE 2021, 16, e0243334. [Google Scholar] [CrossRef]
Figure 1. Temporal dynamics of the tomato cropping cycle, the infestation with Phthorimaea (synonym Tuta) absoluta, and damage in three open field experiments in Rwanda in 2023 and 2024. Data from untreated control plots are shown. Harvest from week 8 post-transplanting onwards.
Figure 1. Temporal dynamics of the tomato cropping cycle, the infestation with Phthorimaea (synonym Tuta) absoluta, and damage in three open field experiments in Rwanda in 2023 and 2024. Data from untreated control plots are shown. Harvest from week 8 post-transplanting onwards.
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Figure 2. Example of tomato field experiment with leaf mines caused by the larvae of Phthorimaea (syn. Tuta) absoluta; the experimental layout and the flat-spray process (photos by B. W. Waweru and S. Toepfer).
Figure 2. Example of tomato field experiment with leaf mines caused by the larvae of Phthorimaea (syn. Tuta) absoluta; the experimental layout and the flat-spray process (photos by B. W. Waweru and S. Toepfer).
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Figure 3. Efficacy of differently formulated entomopathogenic nematodes, other nature-based products, and a standard insecticide in reducing the number of larvae of Phthorimaea absoluta in leaf mines of tomatoes, as well as in reducing the proportion of damaged fruits at the first harvest. Efficacy was calculated compared to the negative control. Three open-field tomato experiments in Rwanda in 2023 and 2024 with four plots per treatment per field. No data means too many fruits with damage, not allowing for a reliable analysis of differences in efficacies. Letters on bars indicate significant differences between treatments as per Games–Howell post hoc test at p < 0.05 following one-way-ANOVA.
Figure 3. Efficacy of differently formulated entomopathogenic nematodes, other nature-based products, and a standard insecticide in reducing the number of larvae of Phthorimaea absoluta in leaf mines of tomatoes, as well as in reducing the proportion of damaged fruits at the first harvest. Efficacy was calculated compared to the negative control. Three open-field tomato experiments in Rwanda in 2023 and 2024 with four plots per treatment per field. No data means too many fruits with damage, not allowing for a reliable analysis of differences in efficacies. Letters on bars indicate significant differences between treatments as per Games–Howell post hoc test at p < 0.05 following one-way-ANOVA.
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Figure 4. Quality control of the entomopathogenic nematode (EPN) Steinernema carpocapsae during preparation and spraying onto tomato leaves against Phthorimaea absoluta under open field conditions. Samples were observed for mortality using a stereomicroscope. Letters on bars indicate significant differences between treatments as per Games–Howell post hoc test at p < 0.05 following between-subject ANOVA of formulation and time.
Figure 4. Quality control of the entomopathogenic nematode (EPN) Steinernema carpocapsae during preparation and spraying onto tomato leaves against Phthorimaea absoluta under open field conditions. Samples were observed for mortality using a stereomicroscope. Letters on bars indicate significant differences between treatments as per Games–Howell post hoc test at p < 0.05 following between-subject ANOVA of formulation and time.
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Figure 5. Survival of the entomopathogenic nematode (EPN) Steinernema carpocapsae when sprayed onto tomato leaves against Phthorimaea absoluta under open-field conditions. In total, 15,000 EPNs were sprayed per tomato plant. Nematodes were washed from leaflets for analyses at 30 min and 1 to 2 h after treatment. At 1 or 2 weeks after treatments, leaflets were collected and submerged in water for 3 to 4 h to recover any nematodes. Letters on bars indicate significant differences between treatments as per Games–Howell post hoc test at p < 0.05 following between-subject ANOVA of formulation and time.
Figure 5. Survival of the entomopathogenic nematode (EPN) Steinernema carpocapsae when sprayed onto tomato leaves against Phthorimaea absoluta under open-field conditions. In total, 15,000 EPNs were sprayed per tomato plant. Nematodes were washed from leaflets for analyses at 30 min and 1 to 2 h after treatment. At 1 or 2 weeks after treatments, leaflets were collected and submerged in water for 3 to 4 h to recover any nematodes. Letters on bars indicate significant differences between treatments as per Games–Howell post hoc test at p < 0.05 following between-subject ANOVA of formulation and time.
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Table 1. Characteristics of treatments applied as foliar sprays onto tomato leaves in fields naturally infested with larvae of Phthorimaea (syn. Tuta) absoluta. Treatments include the entomopathogenic nematode (EPN) Steinernema carpocapsae with strain RW14-GR3a2 used in field 1 and S. carpocapsae strain All used in fields 2 and 3. Experiments were conducted in Rwanda in 2023 and 2024. In total, there were 33,000 plants per ha in 2023 and 28,000 plants per ha in 2024. Per plant, 10 mL water were used for the treatments equalling 330 litres per hectare in 2023, and 15 mL per plant and 420 litres per hectare in 2024. We applied 2 treatments in 2-week intervals.
Table 1. Characteristics of treatments applied as foliar sprays onto tomato leaves in fields naturally infested with larvae of Phthorimaea (syn. Tuta) absoluta. Treatments include the entomopathogenic nematode (EPN) Steinernema carpocapsae with strain RW14-GR3a2 used in field 1 and S. carpocapsae strain All used in fields 2 and 3. Experiments were conducted in Rwanda in 2023 and 2024. In total, there were 33,000 plants per ha in 2023 and 28,000 plants per ha in 2024. Per plant, 10 mL water were used for the treatments equalling 330 litres per hectare in 2023, and 15 mL per plant and 420 litres per hectare in 2024. We applied 2 treatments in 2-week intervals.
Active Ingredient Product Entomopathogenic Nematodes
Ingredients and FormulationsTradenameCompany g/Litreg/Plantg/ha /Litre (mL)/Plant (mL)/ha (Litre) /mL/Litre (Million)/Plant/ha (Million)
Field 1 in 2023
UV protectant + EPN
Canola seed oilRape seed oilAgroPy Ltd., Rwanda 10000.03825 2.50.030.8 18001.818,000594,000
Surfactant + EPN
Alkyl polyglycoside APG surfactantGlucopon 425BASF by AgroPy Ltd., Rwanda 48–520.000321 50 0.516.5 18001.818,000594,000
Nature-based ingredients
PyrethrinPyrethrin 5%AgroPy Ltd., Rwanda 50.1112 7.350.072.4 0000
SpinosadSpinosad 12% SCHenan Jiahe Agriculture Ltd.., China 120.0112 30.031.0 0000
Negative control
Untreated control
Field 2 and 3 in 2024
Surfactant and UV protectant + EPN
Alkyl polyglycoside APG surfactantGlucopon 425BASF by AgroPy Ltd., Rwanda 48–520.000321 1001.542 1000115,000420,000
+ Canola seed oilRape seed oilAgroPy Ltd., Rwanda 10001.542,000 1001.542
Surfactant + EPN
Alkyl polyglycoside APG surfactantGlucopon 425BASF by AgroPy Ltd., Rwanda 48–520.000321 1001.542 1000115,000420,000
Nature-based ingredients
PyrethrinPyrethrin 5%AgroPy Ltd., Rwanda 50.1716 7.50.113.2 0000
Positive control
Lambda cyhalothrinLambdex 50ECEGT, Hemen Industries, Rwanda 500.000321 10.020.4 0000
Negative control
Untreated control
Table 2. Factors influencing the efficacy of treatments in reducing larvae of Phthorimaea (syn. Tuta) absoluta in leaf mines of tomatoes, preventing damage and improving yields. Results shown for differently formulated entomopathogenic nematodes (EPN), two other nature-based products, and a standard insecticide. Data were corrected to the data of the negative control. Yield quality gain is presented as the % prevention of fruits with punctures. Three open-field tomato experiments in Rwanda in 2023 and 2024 with four plots per treatment per field. Multivariate analyses of variance and significance presented in bold at p < 0.05.
Table 2. Factors influencing the efficacy of treatments in reducing larvae of Phthorimaea (syn. Tuta) absoluta in leaf mines of tomatoes, preventing damage and improving yields. Results shown for differently formulated entomopathogenic nematodes (EPN), two other nature-based products, and a standard insecticide. Data were corrected to the data of the negative control. Yield quality gain is presented as the % prevention of fruits with punctures. Three open-field tomato experiments in Rwanda in 2023 and 2024 with four plots per treatment per field. Multivariate analyses of variance and significance presented in bold at p < 0.05.
Factors % Prevention of Leaflet Damage% Prevention of Leaf Damage% Reduction in Larvae% Larval Mortality % Yield Quality Gain % Yield Weight Gain
dfFp Fp Fp Fp Fp Fp
Treatments 5; 9341.30.26 2.30.16 3.20.002 1.10.3433.90.02 0.60.584
Formulation of EPNs 2; 11490.90.34 2.20.12 2.40.068 0.80.48310.37 1.30.344
Frequency of treatments 2; 9342<0.0001 9.3<0.0001 3.70.024 0.30.723NANA NANA4
Weeks after treatment12; 221332<0.0001 0.40.55 6.50.020 7.7<0.0001 NANA NANA4
Field site 2; 93440.018 110.001 1.70.190 6.40.002 4.80.03 0.040.954
Pest population levels 7; 11518.5<0.0001 0.70.572260<0.0001 119<0.0001 0.60.56 0.080.784
1 Effect of time since treatments within 1 to 3 weeks shown; 2 pest population levels had no influence on damaged leaves as most leaves were damaged; 3 larvae difficult to reliably assess in the field, and mortality data are therefore to be considered with caution; 4 no detectable effects of pests and treatments on the total weight of the yield, but many tomato fruits could not be sold because of pest damage.
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Kajuga, J.N.; Waweru, B.W.; Bazagwira, D.; Ishimwe, P.M.; Ndacyayisaba, S.; Mukundiyabo, G.C.; Mutumwinka, M.; Uwimana, J.d.; Toepfer, S. Efficacy of Foliar Applications of Entomopathogenic Nematodes in the Management of the Invasive Tomato Leaf Miner Phthorimaea absoluta Compared to Local Practices Under Open-Field Conditions. Agronomy 2025, 15, 1417. https://doi.org/10.3390/agronomy15061417

AMA Style

Kajuga JN, Waweru BW, Bazagwira D, Ishimwe PM, Ndacyayisaba S, Mukundiyabo GC, Mutumwinka M, Uwimana Jd, Toepfer S. Efficacy of Foliar Applications of Entomopathogenic Nematodes in the Management of the Invasive Tomato Leaf Miner Phthorimaea absoluta Compared to Local Practices Under Open-Field Conditions. Agronomy. 2025; 15(6):1417. https://doi.org/10.3390/agronomy15061417

Chicago/Turabian Style

Kajuga, Joelle N., Bancy W. Waweru, Didace Bazagwira, Primitive M. Ishimwe, Stephano Ndacyayisaba, Grace C. Mukundiyabo, Marie Mutumwinka, Jeanne d’Arc Uwimana, and Stefan Toepfer. 2025. "Efficacy of Foliar Applications of Entomopathogenic Nematodes in the Management of the Invasive Tomato Leaf Miner Phthorimaea absoluta Compared to Local Practices Under Open-Field Conditions" Agronomy 15, no. 6: 1417. https://doi.org/10.3390/agronomy15061417

APA Style

Kajuga, J. N., Waweru, B. W., Bazagwira, D., Ishimwe, P. M., Ndacyayisaba, S., Mukundiyabo, G. C., Mutumwinka, M., Uwimana, J. d., & Toepfer, S. (2025). Efficacy of Foliar Applications of Entomopathogenic Nematodes in the Management of the Invasive Tomato Leaf Miner Phthorimaea absoluta Compared to Local Practices Under Open-Field Conditions. Agronomy, 15(6), 1417. https://doi.org/10.3390/agronomy15061417

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