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Article

Limited Influence of Abiotic and Biotic Factors on the Efficacy of Soil Insecticides and Entomopathogenic Nematodes when Managing the Maize Pest Diabrotica v. virgifera (Coleoptera: Chrysomelidae)

by
Szabolcs Toth
1,
Stefan Toepfer
1,2,
Mark Szalai
3 and
Jozsef Kiss
1,*
1
Department of Integrated Plant Protection, Institute of Plant Protection, Hungarian University of Agriculture and Life Sciences (MATE), Pater K. Street 1, H 2100 Godollo, Hungary
2
CABI, Rue des Grillons 1, CH 2800 Delemont, Switzerland
3
Institute of Agricultural Economics, Zsil Str. 3, H 1093 Budapest, Hungary
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(11), 2697; https://doi.org/10.3390/agronomy12112697
Submission received: 30 August 2022 / Revised: 19 October 2022 / Accepted: 27 October 2022 / Published: 30 October 2022
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Abstract

:
Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) is a serious pest that infects maize. Insecticides or entomopathogenic nematodes are used to control the root-damaging larvae. However, such treatments are reportedly inconsistent in terms of efficacy under farming conditions. To better understand the reasons behind these inconsistencies, we studied the control efficacy of seed coatings, such as clothianidin; granular soil insecticides, such as cypermethrin and tefluthrin; and fluid-applied entomopathogenic nematodes, such as Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae). We assessed the influence of 12 biotic and 20 abiotic factors on the reduction of Diabrotica v. virgifera populations and on the prevention of root damage in 20 field-scale experiments in Hungary between 2010 and 2020. Results confirmed that all treatment types are able to control pest populations and prevent root damage, but with high variability. Our analyses showed that most investigated factors, for example, air temperature, most soil parameters, and pest infestation levels, did not influence the efficacy of the treatments. The efficacy of clothianidin in preventing root damage decreased slightly with increasing soil bulk density but improved with late maize sowing, and therefore late treatment, as well as with increasing soil moisture in July. The efficacy of cypermethrin in preventing damage improved slightly with increasing clay content in the soil. Tefluthrin was slightly less effective in reducing D. v. virgifera with increasing soil moisture in June. However, all these factorial influences were minor in their absolute effects. Surprisingly, none of the investigated factors seemed to influence the efficacy of H. bacteriophora. In conclusion, the efficacy of chemical and biological treatments against this soil pest remains difficult to predict under farming conditions.

1. Introduction

Rice, wheat, and maize are the top three food providers for humans, accounting for an estimated 42% of the food calories consumed across the world [1]. In the latest FAO survey, the sowing area of maize worldwide is estimated to be 197 million ha, producing 1.14 million tons of maize per year [1]. In the developed economies, maize yield is mainly used for feeding livestock (~75%). In sub-Saharan Africa, Latin America, and some of the Asian countries, about 20% of the harvest is consumed by humans directly [2,3]. However, numerous threats endanger the optimal level of maize cultivation all around the globe, including climate change [4], for example, in the form of drought or heat stress [5], and new invasive species [6]. One such problematic invasive maize pest is Diabrotica v. virgifera LeConte (Coleoptera: Chrysomelidae) or western corn rootworm. It has spread through large parts of the north American continent and successfully invaded maize growing regions of Europe since the late 1980s [7].
Diabrotica virgifera ssp. virgifera probably originated from Central America, likely around Mexico. From there, it had invaded North America by the early 19th century [8,9,10]. D. v. virgifera was accidentally introduced from North America into Europe on at least five separate occasions [11]. The first of these successful introductions was probably in Serbia in the 1980s, but it took until 1992 when the damage it caused (and, thus, the species) was detected [12]. Over the last three decades, D. v. virgifera has invaded most maize growing areas of Central Europe, parts of Eastern Europe, parts of the Balkans, as well as Italy [7]. Altogether, it has invaded 32 European countries until now [13].
The pest is an univoltine species with eggs overwintering in the soil [8]. After maize germination, eggs hatch and larvae appear on the maize roots [12]. After pupation, adult beetles emerge from the soil during late vegetative and flowering stages of maize [14]. The larvae exclusively feed on maize roots, lowering nutrient and water intake of the plants and causing plant lodging [14,15]. Adult beetles can also cause some damage in maize by feeding on pollen and silk, hindering fertilization [16]. In areas with high pest densities, yield loss can be significant [17] and become particularly serious when combined with adverse weather conditions [18,19,20]. To manage this pest and to prevent damage and yield losses, several control options are available to farmers.
In short, the most important control methods are the following: (a) crop rotation, (b) chemical insecticides such as granular formulations, fluids, or seed treatments against the larvae, (c) foliar insecticides against the adults, (d) transgenic hybrids against the larvae, and (e) biological control agents against the larvae. Historically, four groups of insecticides have been used widely and abundantly against the rootworms: pyrethroids (e.g., tefluthrin, bifenthrin, cypermethrin, and deltamethrin), organophosphates (e.g., terbufos, chlorpyriphos, and methyl parathion), carbamates (e.g., carbofuran, carbaryl), and neonicotinoids (e.g., clothianidin, thiamethoxam, and imidacloprid). All these can be formulated as granules or liquids and applied into the furrow, usually at sowing time; and some of these are also formulated as seed coating [21,22,23]. However, there is a lot of variability in the efficacy of the soil insecticides or seed coatings, probably due to technical failures such as incorrect calibration of machines or other human errors, On the other hand, two other important causes can be considered, one is the probability of insecticide resistance, or the influence of abiotic and biotic factors of the environment [24].
The first confirmed instance of insecticide resistance shown by D. v. virgifera was against two organochlorine substances, aldrin and heptachlor, by field-collected beetles (in 1960–1961) in Nebraska, where the LD50 was about 80-fold greater for heptachlor and 50-fold greater for aldrin compared to a susceptible population [25]. Later, in the 1990s, bioassays with field-collected populations confirmed carbamate (e.g., carbaryl) and organophosphate (e.g., methyl parathion) resistance [26]. Moreover, pyrethroids are not untouched by this phenomenon, as recently reported [27].
In addition to insecticide resistance, biotic factors such as the degradation of an insecticide by microbials can hinder effective rootworm control. For example, Felsot et al. [28,29] have investigated why repeated carbofuran treatments started to fail to control rootworms after some years. Different Pseudomonas and Actinomycetes bacteria started to use the chemical themselves, and the insecticide rapidly disappeared from the soil. Similar observations were made for the organophosphate isofenphos [30]. Different abiotic factors also explain the insufficient performance of some soil insecticides [31], such as the type, texture, and organic content of the soil; soil moisture; and soil temperature. For example, organochlorines and organophosphates are believed to be more effective in soils with a high organic matter content [32]. Moreover, increasing soil moisture may elevate their toxicity [31]. With some exceptions, it seems that increasing soil temperatures increases the toxicity of soil insecticides [33,34,35]. Cultural control practices, for example, late sowing of maize or late treatments closer to the hatching of the larvae, may increase insecticide efficacy [36,37].
Despite some insecticide resistance [20,38], bans on active ingredients and sometimes entire chemical groups [39] under new agri-policies have reduced the diversity of modes of actions of chemical pesticides [40]. Nevertheless, soil insecticides still seem an essential element in the toolkit of farmers for soil insect control. For example, in Hungary, an EU member state, 5000 tons of the granular soil insecticide tefluthrin was sold in 2019, which was 46% of all insecticides sold [41]. However, alternatives are needed due to environmental concerns and because more ingredients will likely be taken off the market sooner or later.
One such alternative option is the use of entomopathogenic nematodes, tiny soil-living worms living together with symbiont bacteria in their gut, jointly killing insects and using their resources for reproducing inside them [42]. One of its representatives, the Heterorhabditis bacteriophora has been proven effective against D. v. virgifera larvae and commercial products have been developed [43,44,45,46]. H. bacteriophora can persist in the soil of maize fields for up to 6 weeks after treatment [47]. However, its efficacy against larvae can, as for insecticides, be variable under field conditions [48]. Similar to soil insecticides, several studies aimed at understanding which environmental factors may influence the performance of entomopathogenic nematodes [49]. For example, infectivity and persistence of Heterorhabditis bacteriophora and Steinernema carpocapsae modestly increased with increasing loam and organic matter content of soils compared with sandy soils [49,50]. Less soil moisture of soils is occasionally reported to negatively affect nematode infectivity, survival, and pathogenicity [51,52], but other studies could not find such effects [53]. However, soil characteristics and moisture are likely not the only factors influencing nematode efficacy.
Our work was aimed at better understanding the effects of abiotic and biotic factors on the efficacy of control agents under farming conditions. We built our analyses on a larger set of field trials from Hungary, i.e., on 20 field experiments on farmer fields over 10 years. We attempted to detect relationships between various abiotic and biotic factors and the efficacy of insecticides as well as entomopathogenic nematodes in managing the larval populations of and preventing root damage by D. v. virgifera. We hypothesized that some of the abiotic and/or biotic factors may negatively or positively affect treatment efficacy and thus may explain their variability under field conditions. The findings are expected to contribute to a better understanding of why certain treatments may sometimes fail or may not be satisfactory. This, in turn, could lead to new developments and actions for improving plant protection products or strategies against soil insect pests, such as the invasive alien D. v. virgifera.

2. Materials and Methods

2.1. Study Fields

Experiments were carried out on 20 grain maize fields in Hungary between 2010 and 2020 (Supplementary data, Table S1). Experimental fields were ploughed at the end of each season and then tilled and harrowed before maize was sowed. Maize was sowed between mid-April and early May (Table S1). Individual maize seeds were sowed every 16 to 18 cm in rows 75 cm apart, using a 4-row or a 6-row planter, leading to 72,000–87,000 plants per ha. Except for the seeds treated with insecticide clothianidin, the rest had been coated with standard fungicides only.

2.2. Target Pest

The subject of the study was the western corn rootworm, Diabrotica virgifera ssp. virgifera LeConte (Coleoptera: Chrysomelidae). The majority of the study fields had no natural pest population because the pre-crop had not been maize (Table S1). Only in a few study fields (Fields T, S, P, O, and H) had maize been sown for the second year in a row, and in one (Field L), maize had been sown for the third year in a row. Maize plants were artificially infested with eggs of D. v. virgifera to simulate homogenously distributed pest populations. Eggs were obtained from laboratory-reared beetles that had been collected from fields in southern Hungary the previous year. For rearing and overwintering procedures, see [54,55]. In April, the eggs were transferred to a 24-degree-Celsius environment to stop diapause. Parallel with the artificial infestation in the field, some eggs were transferred onto moistened filter paper to check their overwintering survival and hatching success. The average hatching ratio was always between 50 and 80%, with a relatively high variability, and hatching patterns were comparable to reports from the literature [55].
In the laboratory, D. v. virgifera larvae started to hatch around 1 week after the egg application date (more than 2 weeks after diapause stopped), and hatching lasted until late May. In the field, larvae likely emerged slightly later [56].
Two series of six or seven maize plants in each plot were infested with ready-to-hatch eggs at the 1st to 4th leaf stage (Table S1 presents the dates and egg densities). The eggs in 1 to 2 mL aqueous agar were applied using a 5 mL pipette into two to four holes at both sides of a maize plant [54].

2.3. Experimental Design and Treatments

Experiments were implemented following the EPPO standards PP 1/212 and PP 1/152 [57,58]. Four or five plots of four to six rows of maize were systematically arranged per treatment and control (Table S1).
Soil insecticides, insecticide-coated seeds, and entomopathogenic nematodes were applied into the sowing row. The entire plots were treated. Treatment and maize sowing were carried out about 1 to 3 weeks prior to the expected hatching of eggs. About a week later, two to three series of six to seven maize plants were randomly chosen from among the middle rows of each plot to check for infestation with D. v. virgifera eggs as described above and, therefore, also to assess the data from June to August (described below).

2.3.1. Heterorhabditis Bacteriophora Fluid

About 0.1 to 0.15 million infective juveniles (ij) of the entomopathogenic nematode H. bacteriophora (Rhabditida: Heterorhabditidae) were applied per row meter (hybrid of European and US strains, DianemTM, e-nema GmbH, Schwentinental, Germany), which equals 1.5 to 2 billion ij per hectare. The formulation was a water-soluble inert powder (SP GIFAP code). Prior to application, the quality of nematodes had been checked under a stereomicroscope to ensure a survival rate of at least 70%. The formulated nematodes were then diluted in water and injected into the seeding row behind seed placement (200 up to 550 L of water per hectare). Different applicators were used as described in [55].

2.3.2. Clothianidin Seed Coating

We used maize seeds coated with clothianidin, i.e., the nicotinoid of the active substance (E)-1-(2-chloro-1,3-thiazol-5-ylmethyl)-3-methyl-2-nitroguanidin (Poncho™ FS 600, Bayer Crop Science Hungaria KFT, Budapest, Hungary; formulation type: Solution for seed treatment LS according to GIFAP code). About 0.006 mL of clothianidin was coated on a seed.

2.3.3. Cypermethrin Microgranules

About 12 kg of the soil insecticide cypermethrin, equaling 0.9 per row meter, was applied per hectare with seeder-mounted micro-granule applicators (Belem™ 0.8 MG, 0.8% a.i., Spiess-Urania, Hamburg, Germany). Cypermethrin is a pyrethroid of the chemical compound [Cyano-(3-phenoxyphenyl) methyl] 3-(2,2-dichloro-ethenyl)-2,2-dimethyl-cyclopropane-1-carboxylate (IRAC 3A).

2.3.4. Tefluthrin Fine Granules

About 13.3 kg of the soil insecticide tefluthrin, equaling 1 g per row meter, was applied per hectare (Force™ 1.5 G, Syngenta, Hungary). Tefluthrin is a pyrethroid of the chemical compound 2,3,5,6-tetrafluoro-4-methylbenzyl(Z)-(1RS,3RS)-3-(2-chloro- 3,3,3-trifluoro-1-propenyl-2,2-dimethyl-cyclopropanecarboxylate.

2.3.5. Untreated Control

Infested but untreated plots served as negative control.

2.4. Assessment of Abiotic and Biotic Factors

The characteristics of the assessed abiotic and biotic factors are presented in Table S1 and Table 1.
The quality of entomopathogenic nematodes and their application was assessed by counting surviving nematodes before and after the application of the following [44]. Virulence of the nematodes was assessed with subsamples from the delivered product as well as with subsamples post-application using quality control bioassays with Tenebrio molitor larvae (Coleoptera: Tenebrionidae) [44].
From each experimental site, from an area of 5 to 30 cm, 1 L of five to six mixed soil samples was taken. These samples were sent to the Soil Conservation Service, Szolnok, Hungary, to analyze for clay, loam, sand, CaCO3, and humus content, as well as the pH of the soils. Soil moisture and soil bulk density were measured according to [57] on a monthly basis from April to August. Temperature and rainfall data were recorded hourly through a weather station (Davis Instruments).

2.5. Assessment of Pest Populations and Root Damage

Four to five series of six to seven infested maize plants were assessed per treatment and control per field. Plants were covered with gauze cages (0.125 × 0.4 × 1.5 m high). They were placed prior to the expected start of adult emergence, which was usually in mid-June [44]. The adult beetles of D. v. virgifera that emerged were counted on a weekly basis and removed from cages at each assessment [48]. Weekly emergence data of adults were standardized to 100 eggs per plant. The efficacy of each treatment was calculated as the reduced emergence of beetles relative to the emergence of beetles from untreated control (corrected efficacy % = 100 × (beetles in control plots—beetles in treated plots)/maximum (beetles in the control or treated plots) [calculation according to [58]].
To assess the root damage, the roots of 24 to 30 maize plants per treatment were dug out from each field every year from early July to the beginning of August. Firstly, the soil was removed by shaking the roots. We were careful not to break off any of the primary roots. Secondly, the remaining soil was removed from the root system using a high-pressure water sprayer after soaking the roots for a few hours. Damage was rated using two scales: (i) the 1.0 to 6.0 Iowa scale for the general root damage [59], which is the most commonly used scale despite the fact that it may overestimate the importance of minor damage (such as feeding scars) and (ii) the 0.00–3.00 node-injury scale for heavy root damage [60], which is a linear and decimal scale that measures only totally destroyed roots or nodes. The corrected efficacy of root damage was calculated as 100 × (damage in control plots − damage in treated plots)/maximum (damage in control or treated plots) [calculation according to 99].

2.6. Data Analysis

We used ordinary least squares linear models to detect the overall effect of the treatments on adult emergence and root damage. This was followed by ANOVA tests with a post hoc Tukey test to detect the differences between the treatments.
Due to the high multicollinearity between the factors, which otherwise would not be allowed in regression modeling, we preselected the most relevant factors by calculating Pearson’s correlation coefficients (r coefficient) between the different factors and between the efficacies of treatments in controlling adult emergence as well as in preventing general and heavy root damage. Factors appearing to have r coefficients of at least −0.4 ≤ r coefficient ≥+0.4 with a p-value < 0.05 were chosen for developing regression models. This means that factors with small r coefficients were dropped from further analysis.
Simple or multiple linear regressions were performed for correlated factors to identify relationships between factors and control efficacies (Table 1). To avoid any misinterpretation of the models, non-linearity of the response–predictor pairs, correlation of the error terms, non-constant variance of error terms, outliers, high-leverage points, and multicollinearity were investigated before model execution [61]. R v.4.0.2 (R Core Team, 2020) was used for data visualization and statistical analysis.

3. Results

3.1. Treatment Efficacies

All four studied treatment types applied at the sowing of maize, i.e., clothianidin seed coating, cypermethrin granular soil insecticide, tefluthrin granular soil insecticide, and the biocontrol agent H. bacteriophora, were able to control D. v. virgifera larvae (reduced adult emergence: LM, R2 = 0.3, p < 0.001). Achieved control efficacies were comparable among the treatments (ANOVA, R2 = 0.08, p = 0.11).
In detail, across fields and years, clothianidin reduced the pest population by 69% ± 8% (SD) on average (median 71%, LM, padj < 0.001, 95% CI (41, 98); Figure 1), cypermethrin reduced the pest population by 31% ± 34% (median 30%, LM, padj < 0.001, 95% CI (12, 50)), tefluthrin reduced the pest population by 44% ± 41% (median 63%, LM, padj < 0.001, 95% CI (21, 47)), and the entomopathogenic H. bacteriophora reduced the pest population by 34% ± 34% (median 46%, LM, padj < 0.001, 95% CI (27, 60)). Achieved efficacies of treatments in pest reduction were highly variable, as reflected in the large SDs (numbers after ± above the boxplots) and the wide spread of the data points in Figure 1. Most treatment types occasionally failed. Although clothianidin reached control efficacies in all experiments and years, cypermethrin was successful in only 70% of the experiments, tefluthrin in 79% of the experiments, and H. bacteriophora in 80% of the experiments (data points at or below 0 in Figure 1).
All four treatment types, i.e., the clothianidin seed coating, cypermethrin and the tefluthrin granular soil insecticide as well as the H. bacteriophora were able to prevent general root damage from D. v. virgifera larvae (1.0 to 6.0 modified Iowa scale: LM, R2 = 0.3, p < 0.001). Control efficacies were different between the treatments (ANOVA, R2 = 0.4, p < 0.001), the efficacy of clothianidin and tefluthrin were more than 4x higher compared to cypermethrin and H. bacteriophora.
Clothianidin prevented 19% ± 13% (median 20%, LM, padj < 0.05, 95% CI (14, 23)) of general root damage. The cypermethrin prevented 4% ± 16% (median 5%, LM, padj < 0.05, 95% CI (0.1, 8)) of the root damage. Tefluthrin prevented 20% ± 16% (median 20%, LM, padj < 0.05, 95% CI (17.1, 23]) of the root damage. The entomopathogenic H. bacteriophora prevented 3% ± 16% (median 3%, LM, padj < 0.05, 95% CI (0.07, 5)) general root damage. Achieved efficacies of treatments in prevention of the general root damage were highly variable, as reflected in the large SDs (numbers after ± above the boxplots) and the wide spread of the data points in Figure 1. All treatment types occasionally failed. In other words, clothianidin prevented general root damage in 94% of the experiments and years, whereas cypermethrin was successful in 65% of the experiments, tefluthrin in 81% of the experiments, and H. bacteriophora in 59% of the experiments.
All treatments were also able to prevent heavy root damage by D. v. virgifera larvae (1.00 to 3.00 node-injury scale: LM, R2 = 0.3, p < 0.001), but to different levels (ANOVA, R2 = 0.62, p < 0.001). The efficacy of clothianidin and tefluthrin was about double that of cypermethrin and H. bacteriophora.
Here, clothianidin prevented 83% ± 17% (median 84%, LM, padj < 0.05, 95% CI (67, 98)) of heavy root damage. Cypermethrin prevented 50% ± 65% (median 100%, LM, padj < 0.05, 95% CI (37, 63)) of the root damage. Tefluthrin prevented 83% ± 31% (median 100%, LM, padj < 0.05, 95% CI (73, 92)) of the root damage. H. bacteriophora prevented 47% ± 62% (median 72%, LM, padj < 0.05, 95% CI (38, 92)). Although clothianidin was able to prevent heavy root damage across all experiments and years, cypermethrin was successful only in 75% of the experiments, tefluthrin in 95% of the experiments, and H. bacteriophora in 79% of the experiments.

3.2. Abiotic and Biotic Factors Influencing Treatment Efficacies

The efficacy of Heterorhabditis bacteriophora in controlling D. v. virgifera and preventing root damage was hardly influenced by any of the 12 assessed biotic and 20 assessed abiotic factors. In fact, none of the factors had a notable impact on efficacies (see the narrow distributions of Pearson’s r values around 0 in Figure 2 and the lack of influencing factors in models, presented in Table 2).
The efficacy of clothianidin in controlling D. v. virgifera and preventing root damage was hardly influenced by any of the 6 assessed biotic and 20 assessed abiotic factors.
Only two soil components appeared negatively correlated with the efficacy of clothianidin seed coatings in suppressing the pest population: CaCO3 soil content (Pearson’s r coefficient = −0.82, p = 0.04) and humus content (Pearson’s r coefficient = −0.85, p = 0.02). Regression model for both factors explained ~60% of the variance of efficacies, which was not enough to allow a reliable prediction (LM: R2adj = 0.63, df = 3, p = 0.1). This was also true when separately analyzing CaCO3 (β = −0.8, 95% CI (−4.5, 2.8), p = 0.5) and humus content (β = −8.8, 95% CI (−33.2, 15.5), p = 0.3) (Table 2).
Only one soil component appeared to be negatively correlated with the efficacy of clothianidin in preventing general root damage as assessed by the 1.0 to 6.0 Iowa scale, namely the soil bulk density (Pearson’s r = −0.51, p < 0.001). The fitted regression model was able to predict a slight decrease in efficacy general root damage prevention with increasing soil bulk density and explained ~30 of the variance (R2adj = 0.28, df = 40, p < 0.001).
Prevention of heavy root damage (assessed through the 1.00 to 3.00 node-injury scale) increased with late sowing and late treatment dates (Pearson’s r = 0.71, p < 0.001; LM: β = 1.9, 95% CI (1.1, 2.8), p < 0.001) as well as with increasing soil moisture in July (Pearson’s r = 0.57, p < 0.001; LM: β = 1.2, 95% CI (0.2, 2.2), p = 0.02). The fitted linear model with these two factors explained about half of the variance (R2adj = 0.55, df = 39, p < 0.001).
Cypermethrin’s efficacy in controlling D. v. virgifera was not influenced by any of the 6 assessed biotic and the 20 assessed abiotic factors. As for its efficacy in preventing root damage, we identified a few factors that influenced it.
Four factors correlated to the efficacy of cypermethrin in preventing general root damage according to the 1.0 to 6.0 Iowa scale. Two were correlated to it positively and moderately: the clay content of the soil (Pearson’s r = 0.51, p < 0.001) and the air temperature in July (Pearson’s r = 0.54, p < 0.001). The other two factors were negatively and moderately correlated with it, namely the pH of the soil (Pearson’s r = −0.51, p < 0.001) and the eggs applied per plant number (Pearson’s r = −0.43, p < 0.001). The regression model with all factors explained less than half of the variance in efficacies, but its predictive values were reliable (R2adj = 0.39, df = 35, p < 0.001). However, within the model, separate factor effects were non-significant.
The prevention of heavy root damage (assessed with the 1.00 to 3.00 node-injury scale) increased with increasing clay content of the soil (Pearson’s r = 0.41, p < 0.001; LM: β = 4, 95% CI (0.6, 7.5), p = 0.02). The fitted linear model that contains this factor had explained about 1/3 of the variance in the efficacies (R2adj = 0.36, df = 44, p < 0.001).
The efficacy of tefluthrin in controlling D. v. virgifera and preventing root damage was hardly influenced by any of the 6 assessed biotic and 20 assessed abiotic factors.
Two factors were moderately and positively correlated with the efficacy of the tefluthrin granules in suppressing the pest population, the air temperature in June (Pearson’s r = 0.46, p = 0.04) and the cumulative rainfall in July (Pearson’s r = 0.52, p = 0.02), but one factor was highly and negatively correlated with it, namely the soil moisture in June (Pearson’s r = −0.82, p < 0.001). The regression model with these factors has a high predictive value, explaining almost 80% of the variance in tefluthrin’s efficacies (R2adj = 0.77, df = 9, p < 0.001). Tefluthrin’s efficacy slightly decreased with increasing soil moisture in June (β = −2.3, 95% CI (−4.6, −0.04), p = 0.047) but increased with higher rainfall in July (β = 0.4, 95% CI (0.1, 0.8), p = 0.02).
We were not able to detect any factors that are correlated with tefluthrin’s efficacy in preventing general root damage.
Prevention of heavy root damage slightly decreased with increased sand content of the soil (Pearson’s r = −0.4, p < 0.001; LM: β = −1.4, 95% CI (−2, −0.8), p < 0.001). The regression model explained only a small fraction, of around 1/10, of the variance (R2adj = 0.15, df = 109, p < 0.001).

4. Discussion

In general, the applied soil insecticides, the insecticide seed coating, and the entomopathogenic nematodes reduced the D. v. virgifera population by 31 to 69% across the fields and years of this study, and this at comparable levels. The found efficacies of the chemical insecticides were comparable with results from others studies, as was the observation that efficacies recorded from different fields trials or years can vary considerably [22,62,63,64]. Such variability in pest reduction seems also true for entomopathogenic nematodes [60,65]. Moreover, there was high variability among the treatments in our study in terms of root damage, such as a 3 to 20% efficacy in preventing general root damage as assessed by the 1.0 to 6.0 Iowa damage rating scale. This also holds true for the prevention of heavy root damage as assessed by the 0.00 to 3.00 node-injury scale, where we found variable efficacies of 46 to 82%. This issue had been also been observed by [66] and other authors over a long period. Therefore, we wanted to find out how abiotic and biotic factors may influence the efficacies of chemical insecticides or entomopathogenic nematodes in reducing D. v. virgifera populations and preventing root damage in maize. We analyzed relationships between the efficacies of the above-mentioned control methods and a large number of abiotic and biotic factors (32) across 10 years in 20 fields in Hungary. However, we found only a few indications that some of the studied factors may influence the efficacy of the agents in our study. Neonicotinoids seed coatings, such as clothianidin, have been widely used for the control of rootworms and other soil pests. In our study, clothianidin reduced D. v. virgifera populations by 69% ± 8% and prevented general root damage by 19% ± 13% and heavy root damage by 83% ± 17% in maize (Figure 1). However, variability in efficacy was relatively high. Schwarz et al. [67], who tested clothianidin seed treatment effects on four Diabrotica species, found that it reduced root damage to a similar extent as chlorpyriphos, tefluthrin, and fipronil. However, clothianidin sometimes failed to prevent heavy root damage (i.e., in 26% of cases). In another study, clothianidin reduced larvae in four out of five different locations and protected the roots from heavy damage in only two locations [68]. In a 2-year study in Austria, Rauch et al. [46] reported the failure of clothianidin in pest reduction. Others too have reported occasional inconsistent results of D. v. virgifera larval control when clothianidin is used over several years [23,69,70]. Some argue that clothianidin seed treatment is recommended only when the population is low to moderate and it is more a protective tool than a control solution against root damage under high Diabrotica pressure [71]. On the contrary, in our experiments, the performance of clothianidin in controlling the pest population and in protecting the roots slightly exceeded that of all other tested treatments and it failed in only a few cases.
There is not much published information on factors that directly affect clothianidin toxicity in the soil or may cause its degradation. We know that clothianidin and another neonicotinoid thiamethoxam are both considered hydrolytically stable, but with high solubility properties: 0.327 g/L at 20 °C and 4.1 g/L at 25 °C [72]. More knowledge has been accumulated over the years about other neonicotinoids. Mahapatra et al. [73] studied the effects of abiotic factors on the degradation of imidacloprid. They found that the rate of dissipation of imidacloprid from the soil samples was faster under submerged conditions compared to when the soil was left in its field capacity and soil samples were air-dried. Imidacloprid dissipated non-significantly between sterile and non-sterile soils. Similarly, under submergence, the dissipation of imidacloprid was up to 66% and 80% of the initial concentration in sterile and non-sterile soils, respectively. Imidacloprid was more stable in acidic and neutral water than in alkalic conditions. Similar results were found for thiamethoxam persistence [74]. Longer persistence was observed under dryer conditions than under submerged conditions. In a leaching experiment in a soil column with water equivalent to 65 cm rainfall, 66–79% of the applied thiamethoxam was recovered from leachate and no residues remained in the soil. Some studies have addressed the biodegradation of neonicotinoids [75]. For example, Parte and Kharat [76] showed that Pseudomonas stutzeri can degrade 62% of clothianidin within 2 weeks at 30 °C under aerobic conditions.
In our study, there were few indications of possible slight factorial effects on clothianidin. For example, clothianidin was slightly less effective in preventing damage at a high soil bulk density; but late maize sowing and therefore late treatment as well as high soil moisture in July slightly improved the prevention of heavy root damage. Others also achieved similar results, for example, organochloride dieldrin volatilization is highest at low soil bulk density (here 0.75 g/cm3) but lowest at high density (1.25 g/cm3) [77]. This is comparable to the results of our studied fields, with a bulk density from 0.89 to 1.3 g/cm3. Therefore, in all probability, clothianidin volatilization, i.e., free movement in the soil, may have been hindered around the root system of the maize plants by the high bulk density of the soil. As mentioned above, elevated soil moisture in July, i.e., during the flowering stage of maize in Europe, seems to slightly aid clothianidin’s efficacy in protecting maize against heavy root damage. A handful of studies have shown this result, that is, that higher soil moisture elevates the toxicity of different soil insecticides [78,79,80]. However, in our case, this is something hard to explain because many larvae are already either pupae or have emerged from the soil as adults by mid-July in Hungary. One reason might be that high soil moisture in July helps roots to recover from damage, and damage then becomes less obvious and more difficult to assess. In our study, late sowing seemed to lead to a slightly better protective role of clothianidin seed treatment against D. v. virgifera damage than early sowing. A smaller time window between the treatment and hatching of the first larvae may have favored the treatment efficacy. Alford and Krupke [81] detected that after sowing maize, there is only a low amount of clothianidin in the plants (maximum 1.34% from the plant tissues and 0.26% from root tissues). This is surprising because in treated seeds, clothianidin is considered a highly translocatable substance. They also found the amounts of plant-bound active ingredients to rapidly decrease after 20 days, putting a question mark on its long-term protective role throughout the cropping seasons. We found something similar in the case of the protective role of clothianidin against heavy root damage.
Pyrethroid insecticides such as tefluthrin have been used against a number of soil-dwelling insect pests since the 1980s [26]. A number of studies have demonstrated that tefluthrin (usually put as granules into furrows) can reduce D. v. virgifera larvae infestation, leading to less root damage, fewer lodged plants, and increased yield [68,82,83,84]. This is confirmed in our study, wherein tefluthrin reduced the pest population by 44% ± 41%, prevented the general root damage by 20% ± 16%, and heavy root damage by 83% ± 31%. However, inconsistent results, especially in controlling D. v. virgifera populations, have been reported [48] and are confirmed here. Insect resistance could be one of the explanations for the observed inconsistencies. Pyrethroid resistance has been reported in the D. v. virgifera populations found in some maize fields in the USA [27]. However, in Europe, resistance of D. v. virgifera against pyrethroids has not been reported or maybe not even studied. Therefore, the inconsistent performance of tefluthrin could be caused by environmental factors.
In our analysis, soil moisture in June, i.e., during the vegetative stages of maize in Hungary, had a slight negatively effect on the efficacy of tefluthrin against D. v. virgifera populations. This is hard to explain, considering that dry soils are known to absorb insecticides whereas soil moisture favors their release from the formulation [85]. An explanation could be that moisture accelerates chemical [86] or biological degradation of the insecticide [87] and therefore the majority of the molecules are not in the soil fraction anymore [88]. On the contrary, higher cumulative rainfall in July seemed to have a positive influence on tefluthrin’s efficacy against D. v. virgifera population in our study. This too is somewhat unusual to see because, normally, many larvae in the soil have emerged by mid-July in Hungary. However, in years when larvae hatching and development are extended due to cool weather, it might be possible that bigger rain quantities wash the tefluthrin into lower or wider layers of soil, allowing the tefluthrin to better reach late instars that have moved due to competition or for pupation [89]. According to Sutter et al. [66], a low density of larvae around roots caused less competition; thus, larvae could live outside of the treated band and avoid contact with soil insecticides. We have also found that soil with a higher sand content may negatively influence tefluthrin’s efficacy in preventing heavy root damage. Higher sand or quartz content of the soil is known to absorb some insecticides and may, therefore, reduce their effects on insect pests [31,85].
In our study, another pyrethroid, cypermethrin, reduced D. v. virgifera by 31% ± 34%, prevented the general root damage by 4% ± 16, and heavy root damage by 50% ± 65%. Although these values are lower than those found for tefluthrin or clothianidin, we could not detect any major influence of the studied biotic and abiotic factors. The only thing we found was that elevated clay content of the soil may slightly aid cypermethrin’s efficacy in protecting maize against heavy root damage. This is contrary to the above-discussed role of sandy soils and to the observation that a higher clay content may lower the toxicity of insecticides in the soil [31]. The pH of the soil may have also played an additional role. For example, Bhat et al. [90] showed that biological degradation of pyrethroid molecules is mediated by different hydrolases. These hydrolases remove ester groups from the molecules and thus they will be inactive. However, the activity of these hydrolases depends on the changes in the pH of the environment. In general, it remains unclear which factors cause a high variability in cypermethrin efficacy and may lead to the occasional low efficacy or even failure.
For biological control agents, such as the entomopathogenic nematodes in our study, variability in efficacies is a well-known phenomenon. There are also numerous indications from both laboratory and field studies that abiotic factors can influence the mortality and infectivity of entomopathogenic nematodes. For example, H. bacteriophora infectivity against Popillia japonica was the highest in potting mix soils, did not differ between loamy sand and other types of loamy soils, and was the lowest in acidic sand [91]. Toepfer et al. [92] investigated the influence of soil types on the efficacy of H. bacteriophora, H. megidis, and S. feltiae against D. v. virgifera larvae under field conditions. They found that all nematodes were able to control D. v. virgifera larvae in most soils. However, their efficacy was slightly higher in heavy clay or silty soils than in sandy soils. At high soil moistures, the rehydration effect favors many nematode species [51,52,93], and this can also be true for elevated temperatures (5 °C vs. 15–30 °C) [52]. Soil salinity seems to play a role. For example, elevated levels of CaCl2 and KCl had no effect on H. bacteriophora survival, penetration efficiency, or movement through a soil column, but moderate concentrations of these salts enhanced H. bacteriophora virulence [94]. Survival of infective juveniles of Steinernema carpocapsae and S. glaseri gradually declined over 16 weeks when pH decreased from pH 8 to pH 4 [95]. However, despite the findings of others on the importance of soil moisture in the pathogenicity of entomopathogenic nematodes [49,50,51,52], we found no such relationship in our study under field conditions.
In our study, we detected a high variability in the efficacy of the applied H. bacteriophora in controlling the pest population and preventing root damage. Therefore, it came as a surprise that we found no relationship between nematode efficacy and the more than 30 tested abiotic or biotic factors. This means that factors other than those studied here may influence the performance of entomopathogenic nematodes in the control of soil insect pests. An increasing number of studies are highlighting the importance of the below-ground interactions between the entomopathogenic nematodes and the fauna and microbiological communities of the soil. For example, predation or infection of the nematodes [96,97] or competition with other organisms [98,99] may play a role. This interaction could influence nematode efficacy, but these were not examined in our study. What is clear is that nematode product quality (measured as virulence and mortality before and after field application) had no influence on their efficacy, indicating that is easy to handle and apply nematodes. This could be crucial in view of farmers who are often less experienced in working with living organism than with pesticides. Another positive aspect is that regardless of the nematodes being applied into the furrow with 100 L of water or more than 500 L, there efficacy remained comparable. Voros et al. [54] made similar observations and argued that the amount of water used for application has little importance when nematodes are applied into the seeding furrow, which is usually already moist and provides a protected environment to nematodes. So, farmers have to carry less water to the fields for application.

5. Conclusions

In conclusion, our work clearly showed that only a few factors may influence the efficacy of the chemical and biological control options used against D. v. virgifera in maize fields. The efficacy of chemical and biological treatments against this serious soil insect pest remains difficult to predict under real-time farming conditions. Other biological factors could influence their performance, such as the degradation of the insecticide by the microbiota and the effect of the microfauna and microbiological communities on the entomopathogenic nematodes, something that merits more investigation. Nevertheless, it is positive that many types of treatments help manage D. v. virgifera in most cases under diverse conditions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12112697/s1, Table S1: Properties of the experimental maize fields and treatments against D. v. virgifera larvae in Hungary between 2010 and 2020.

Author Contributions

S.T. (Stefan Toepfer) and J.K. organized the projects. S.T. (Stefan Toepfer) designed and implemented most experiments. S.T. (Szabolcs Toth) and M.S. conducted the statistical analyses with the large set of data from the numerous experiments. S.T. (Szabolcs Toth) wrote the manuscript with support from co-authors. All authors have read and agreed to the published version of the manuscript.

Funding

The field studies were funded through public funds, such as the Ministry for Rural Areas & Consumer Protection of the State of Baden-Wuerttemberg via the LTZ agricultural technology centre; the Swiss CTI Innovation Promotion Agency of the Federal Office for Professional Education & Technology; and the State Ministry of Food, Agriculture and Forestry StMELF of Bavaria via the Research Centre for Agriculture LfL. A few field experiments were funded by e-nema GmbH, Germany. Data analyses, modeling, and manuscript writing were funded by a Hungarian PhD scholarship at the Hungarian University of Agriculture and Life Sciences (MATE) as well as by the ARRS Science Foundation of Slovenia (J4-2543) and the National Research, Development and Innovation Office NKFIH of Hungary (SNN 134356). CABI is grateful for the core funding from respective tax payers behind the European Commission, Department for International Development of the UK, the Swiss Agency for Development and Cooperation, the Directorate General for International Cooperation of the Netherlands, Irish Aid International Fund for Agricultural Development, and the Australian Centre for International Agricultural Research (https://www.cabi.org/about-cabi/who-we-work-with/key-donors/, accessed on 19 October 2022).

Data Availability Statement

The analysis, with the data alongside, is openly available in Github at https://github.com/DiabroticaHULab/EnvFactInfluDvv, accessed on 19 October 2022.

Acknowledgments

We would like to thank the Government Office of Plant Protection and Soil Conservation in Hodmezovasarhely in Hungary for their continuous support. The farmers Jancso Pal and Gyorgy Szrnka and the Cereal Research Station of Szeged kindly provided the maize fields for our study. We are grateful to Michael Glas and Peter Knuth (LTZ, Germany), Michael Zellner (LfL, Germany), as well as Ralf-Udo Ehlers (e-nema, Germany) for the scientific exchanges related to the experiments. We would also like to thank our summer students Ferenc Koncz, Rajmond Stuber, Andor Kiss, and Ferenc Kiraly for their help in field work.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02697 g001 550
Figure 1. Efficacy of different treatments in controlling Diabrotica v. virgifera larvae and in preventing root damage in maize fields compared to the untreated, infested control. General root damage assessed via the 1.0 to 6.0 modified Iowa scale, and heavy root damage assessed via 0.00 to 3.00 Oleson’s node-injury scale. Pest population assessed by counting adults emerging from the soil in gauze cages. The spread of the data points represents the mean number of adults per field and the means of the general and heavy root damage per plot. The median is presented as a full line inside box plots; the mean ± the SD is presented as numbers above the boxes. Different letters on box plots indicate the significant difference as per post hoc Tukey HSD test at p < 0.05 following ANOVA; untreated, infested control significance letter is a, n = 20 sites, and the study was conducted across 10 years in southern Hungary.
Figure 1. Efficacy of different treatments in controlling Diabrotica v. virgifera larvae and in preventing root damage in maize fields compared to the untreated, infested control. General root damage assessed via the 1.0 to 6.0 modified Iowa scale, and heavy root damage assessed via 0.00 to 3.00 Oleson’s node-injury scale. Pest population assessed by counting adults emerging from the soil in gauze cages. The spread of the data points represents the mean number of adults per field and the means of the general and heavy root damage per plot. The median is presented as a full line inside box plots; the mean ± the SD is presented as numbers above the boxes. Different letters on box plots indicate the significant difference as per post hoc Tukey HSD test at p < 0.05 following ANOVA; untreated, infested control significance letter is a, n = 20 sites, and the study was conducted across 10 years in southern Hungary.
Agronomy 12 02697 g001
Agronomy 12 02697 g002 550
Figure 2. Histogram of the distribution of Pearson’s correlation coefficients between the 32 investigated abiotic and biotic factors and the efficacies of the entomopathogenic nematode Heterorhabditis bacteriophora in reducing Diabrotica v. virgifera population and protecting against heavy and general root damage in maize at 20 sites across 10 years in southern Hungary. Dashed lines represent the border of −0.4 and 0.4 for the r coefficient values that were set to be the threshold for factor selection for regression modeling.
Figure 2. Histogram of the distribution of Pearson’s correlation coefficients between the 32 investigated abiotic and biotic factors and the efficacies of the entomopathogenic nematode Heterorhabditis bacteriophora in reducing Diabrotica v. virgifera population and protecting against heavy and general root damage in maize at 20 sites across 10 years in southern Hungary. Dashed lines represent the border of −0.4 and 0.4 for the r coefficient values that were set to be the threshold for factor selection for regression modeling.
Agronomy 12 02697 g002
Table
Table 1. Characteristics of abiotic and biotic factors analyzed for their influence on the efficacy of soil insecticides and entomopathogenic nematodes in reducing Diabrotica v. virgifera larvae and protecting the roots against damage in maize (at 20 sites over 10 years in Hungary).
Table 1. Characteristics of abiotic and biotic factors analyzed for their influence on the efficacy of soil insecticides and entomopathogenic nematodes in reducing Diabrotica v. virgifera larvae and protecting the roots against damage in maize (at 20 sites over 10 years in Hungary).
FactorUnitMeanStandard DeviationMinimumMaximumRangeShapiro–Wilk Normality Test Sample SizeLevels of a Factor
WpnUnique Values
Biotic factors
Eggs per plant 40622120011009000.7<0.0014826
Billion nematodes per ha injected 1.70.21.51.90.40.7<0.0012823
Water per ha injected with nematodesLiters328.7158.41335584250.6<0.0014998
Nematode mortality before application%1582.92522.10.9<0.0011079
Nematode mortality after application%2315457530.8<0.0019114
Nematode virulence before application (1-week bioassay)%4127890820.9<0.00113614
Nematode virulence after application (1-week bioassay)%38181076660.9<0.0011059
Maize sowing dateJulian days1123108122140.8<0.0015309
Egg infection dateJulian days1253122134120.8<0.0014518
Maize densityPlants per ha78,00053,76072,00087,00015,0000.8<0.0015305
Elevationm901580150700.6<0.00153011
Natural mortality of adult D. v. virgifera%98.61.196.299.83.60.8<0.0018325
Abiotic factors
Clay content% m/m3472254320.9<0.00150916
Loam content% m/m296939300.8<0.00150916
Sand content% m/m3782451270.8<0.00150916
Soil bulk densityg/cm310.10.91.340.450.9<0.00152211
CaCO3% m/m53112110.9<0.00150916
Soil pH 7.90.27.48.20.80.8<0.00150913
Humus content% m/m2.70.71.633.92.270.9<0.00150917
Soil moisture in Aprilw% = grav.%16311.1219.90.9<0.00147617
Soil moisture in Mayw% = grav.%21.379.93222.10.9<0.00152219
Soil moisture in Junew% = grav.%16.26.8829.521.50.8<0.00142016
Soil moisture in Julyw% = grav.%12.14.1722.915.90.9<0.00152218
Air temperature in April°C13.31.51116.85.80.9<0.0015229
Air temperature in May°C16.81.713.820.26.40.9<0.0015229
Air temperature in June°C21.30.7202330.9<0.0015229
Air temperature in July°C23.31.121.6253.40.9<0.00149010
Cumulative rainfall in Aprilmm17.617.61.45654.60.8<0.00152211
Cumulative rainfall in Maymm6631.420.3134113.70.9<0.00152211
Cumulative rainfall in Junemm36.4303.39389.70.8<0.0015229
Cumulative rainfall in Julymm45.532.8141271130.8<0.00149010
Rain around sowing and treatment (±1 day)mm10.901.91.90.7<0.0013936
Table
Table 2. Correlations and regressions between abiotic or biotic factors and the efficacy of soil insecticides and entomopathogenic nematodes in reducing Diabrotcia v. virgifera larvae and protecting against root damage in maize; only factors that had an influence are presented; n = 20 sites or fields in southern Hungary.
Table 2. Correlations and regressions between abiotic or biotic factors and the efficacy of soil insecticides and entomopathogenic nematodes in reducing Diabrotcia v. virgifera larvae and protecting against root damage in maize; only factors that had an influence are presented; n = 20 sites or fields in southern Hungary.
Pearson CorrelationOrdinary Least Squares Regression Model
TreatmentFactorsrpModel No.Adjusted R2Dfpβ Coefficientp95% CI
Pest infestation (Adults that emerged per plant)
ClothianidinCaCO3 soil content−0.820.0410.6330.1−0.80.5−4.5, 2.8
Humus content−0.850.02−8.80.3−33.2, 15.5
TefluthrinSoil moisture in June−0.82<0.00120.779<0.001−2.30.047−4.6, 0.04
Air temperature in June0.460.0415.20.13−5.2, 35.7
Rainfall in July0.520.020.40.020.1, 0.8
CypermethrinNo factor foundNANANANANANANANANA
H. bacteriophoraNo factor foundNANANANANANANANANA
General root damage (1.0 to 6.0 modified Iowa root damage scale)
ClothianidinSoil bulk density−0.51<0.00130.2840<0.001−47.2<0.001−70.2, −24.3
TefluthrinNo factor foundNANANANANANANANANA
CypermethrinClay content0.51<0.00140.3935<0.0011.20.2−0.8, 3.3
Soil pH−0.51<0.001−15.60.2−39, 8
Air temperature in July0.54<0.0014.70.4−5.9, 15.3
Pest eggs per plant−0.430.0010.020.5−0.03, 0.06
H. bacteriophoraNo factor foundNANANANANANANANANA
Heavy root damage (0.00 to 3.00 Oleson node-injury scale)
ClothianidinMaize sowing date0.71<0.00150.5539<0.0011.9<0.0011.1, 2.8
Soil moisture in July0.57<0.0011.10.020.2, 2.2
TefluthrinSand content−0.4<0.00160.15109<0.001−1.4<0.001−2, −0.8
CypermethrinClay content0.410.00170.3644<0.00140.020.6, 7.5
Soil pH−0.5<0.001−66.70.2−173, 40
Air temperature in June0.47<0.00114.70.6−41, 70.6
H. bacteriophoraNo factor foundNANANANANANANANANA
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Toth, S.; Toepfer, S.; Szalai, M.; Kiss, J. Limited Influence of Abiotic and Biotic Factors on the Efficacy of Soil Insecticides and Entomopathogenic Nematodes when Managing the Maize Pest Diabrotica v. virgifera (Coleoptera: Chrysomelidae). Agronomy 2022, 12, 2697. https://doi.org/10.3390/agronomy12112697

AMA Style

Toth S, Toepfer S, Szalai M, Kiss J. Limited Influence of Abiotic and Biotic Factors on the Efficacy of Soil Insecticides and Entomopathogenic Nematodes when Managing the Maize Pest Diabrotica v. virgifera (Coleoptera: Chrysomelidae). Agronomy. 2022; 12(11):2697. https://doi.org/10.3390/agronomy12112697

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Toth, Szabolcs, Stefan Toepfer, Mark Szalai, and Jozsef Kiss. 2022. "Limited Influence of Abiotic and Biotic Factors on the Efficacy of Soil Insecticides and Entomopathogenic Nematodes when Managing the Maize Pest Diabrotica v. virgifera (Coleoptera: Chrysomelidae)" Agronomy 12, no. 11: 2697. https://doi.org/10.3390/agronomy12112697

APA Style

Toth, S., Toepfer, S., Szalai, M., & Kiss, J. (2022). Limited Influence of Abiotic and Biotic Factors on the Efficacy of Soil Insecticides and Entomopathogenic Nematodes when Managing the Maize Pest Diabrotica v. virgifera (Coleoptera: Chrysomelidae). Agronomy, 12(11), 2697. https://doi.org/10.3390/agronomy12112697

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