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Brief Report

Sensitivity of Yponomeuta padella and Yponomeuta cagnagella (Lepidoptera: Yponomeutidae) to a Native Strain of Steinernema feltiae (Filipjev, 1934)

by
Kornelia Kucharska
1,
Anna Mazurkiewicz
1,
Dorota Tumialis
1,*,
Lidia Florczak
1,
Barbara Zajdel
2 and
Iwona Skrzecz
3
1
Department of Animal Environment Biology, Institute of Animal Sciences, Warsaw University of Life Sciences—SGGW, Ciszewskiego 8 Street, 02-786 Warsaw, Poland
2
Apiculture Division, Institute of Animal Sciences, Warsaw University of Life Sciences—SGGW, Ciszewskiego 8 Street, 02-786 Warsaw, Poland
3
Department of Forest Protection, Forest Research Institute, Braci Leśnej 3 Street, Sękocin Stary, 05-090 Raszyn, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(8), 1582; https://doi.org/10.3390/agriculture13081582
Submission received: 5 July 2023 / Revised: 27 July 2023 / Accepted: 7 August 2023 / Published: 9 August 2023
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
Review Reports Versions Notes

Abstract

:
The larvae of ermine moths from the Yponomeutidae family (Lepidoptera) feed on a range of species and varieties of fruit and ornamental trees. Some species of this family pose a serious threat to the environment, mainly because of the significant defoliation they cause but also due to the widespread use of insecticides used to control them. This study was designed to assess the sensitivity of Yponomeuta padella and Yponomeuta cagnagella larvae and pupae to a native strain of Steinernema feltiae ZAG15 nematodes under laboratory conditions and to test the biological activity of these nematodes against the larvae and pupae of these species in field studies. The following doses were used in the laboratory tests: 50 IJs/insect (Petri dish tests) and 100 IJs/insect (container tests). Petri dish and container tests were performed at 20 °C and 60% humidity. Mortality of two stages (larvae and pupae) was determined 3 days after treatment. In the field trials, the nematodes were applied at the following doses: 4000 IJs/web for the caterpillars of Y. padella and Y. cagnagella and 1000 IJs/web for the pupae of Y. padella and Y. cagnagella (this corresponded to approximately 200 IJs/insect). Nematodes were applied using a 1 L hand sprayer and a lance. The efficacy of the application was assessed after seven days. The results of our study showed that the larvae (81.7%) and pupae (88.3%) of Y. padella had a greater susceptibility to entomopathogenic nematodes (EPNs) than those of Y. cagnagella (50% and 33.3%, respectively). However, our promising laboratory results did not translate into results in field trials, where the application of EPNs proved to be ineffective.

1. Introduction

The ermine moths (Lepidoptera: Yponomeutidae) include about 500 species (28 in Poland), whose larvae feed on a range of species and varieties of fruit and ornamental trees. Ermine moths may be monophagous, oligophagous, or polyphagous insects [1]. Species Yponomeuta are significant pests throughout Europe [2]. The orchard ermine moth, Yponomeuta padella (Linnaeus, 1758), defoliates fruit and ornamental trees, whereas the small ermine moth, Yponomeuta cagnagella, (Hübner, 1813) feeds on the spindle tree. The larvae of ermine moths build characteristic webs at the tips of twigs and join together neighboring leaves, which constitute their feed. In spring, they feed mainly on buds, while in the early summer, they consume massive amounts of leaves, thus markedly limiting the trees’ fruit development [3].
Yponomeuta padella and Y. cagnagella are closely related and have very similar morphology and growth cycle. In summer, ermine moth females secrete pheromones to attract males [4]. Fertilized eggs are then laid on leaves near the tips of twigs or buds. After several days, caterpillars hatch from the eggs but do not start feeding and, instead, overwinter. In spring, the caterpillars begin feeding on leaves and twigs and produce dense, protective webs. After achieving an appropriate body size, they build cocoons, in which they pupate, with the imagines flying out in summer [5,6,7,8,9]. In 1972, Y. padella spread widely across Northern Ireland, destroying about 150,000 km of hawthorn hedges [10,11]. Since then, the species has been considered an environmental threat because of its remarkable ability for defoliation, but also due to the insecticides that are commonly used to control the pest. There is a variety of commercially available pesticides used to control ermine moths in large orchard plantations, which contain various active ingredients: cypermethrin from the pyrethroid group; emamectin benzoate, a compound from the macrocyclic lactones group; chlorantraniliprole, a compound from the anthranilic diamide group; abamectin, a compound from the of macrocyclic lactone group; and azadirachtin A, a compound belonging to the limonoid group [12]. Beyond the chemical means of pest control, there are also biological methods available that contain Bacillus thuringiensis var. aizawai. Ermine moths are resistant to chemical insecticides used on crops, but only for a short time; if the motile larvae do not have webs and feed on young leaves, they can be controlled with preparations containing B. thuringiensis [13]. Hence, environmentally safe methods need to be found to control these pests [14,15]. So far, research on the use of biological methods for combating Yponomeuta has focused mainly on searching for their natural enemies. As a result, dozens of species have been identified, most of which are parasitoids (e.g., Ageniaspis fuscicollis (Dalman)) and predators (e.g., Agria mamillata (Pandellé)). Various viruses and microorganisms (e.g., nuclear polyhedrosis virus, Microsporidum sp.) have also been isolated [11,16,17,18,19,20,21]. At present, however, none of the above-mentioned organisms have found practical application in the control of species of the genus Yponomeuta.
Recently, more attention has been paid to the potential use of entomopathogenic nematodes (EPNs) to control populations of many insect species pests. Entomopathogenic nematodes of the genera Heterorhabditis and Steinernema are insect obligate parasites. These nematodes have a symbiotic relationship with bacteria of the genera Photorhabdus and Xenorhabdus, respectively. Infective juveniles (IJs) enter the host through natural openings such as the mouth, anus, or spiracles, but the IJs of some species can also enter through the cuticle. After penetrating the host’s hemocoel, nematodes release their symbiotic bacteria, which usually kill the host [22,23]. Entomopathogenic nematodes of the genera Steinernema and Heterorhabditis have been extensively used as biological agents against pest insects [24,25,26]. It was found that about 250 insect species representing 10 orders were sensitive to the nematode Steinernema feltiae (Filipjev, 1934) [25]. The native isolate of S. feltiae ZAG15 was tested in our previous studies against various insect species (Lepidoptera, Coleoptera) and always showed high efficacy. Since we assumed that this isolate would also be effective against the species Yponomeuta, we made two hypotheses:
  • The native isolate of S. feltiae shows high activity against Yponomeuta larvae and pupae, whether they are in webs or not;
  • The native isolate of S. feltiae causes mortality of over 50% of the Yponomeuta population during its outbreak under field conditions.
This study was designed to assess the sensitivity of Y. padella and Y. cagnagella larvae and pupae to a native strain of S. feltiae ZAG15 nematodes under laboratory conditions and to test the biological activity of these nematodes against the larvae and pupae of these species in field studies. This present study is the first attempt to evaluate the efficacy of native EPN isolate in controlling Yponomeuta species.

2. Materials and Methods

2.1. Entomopathogenic Nematodes

One native strain of S. feltiae ZAG15 was used for the experiments. The strain was isolated in 2010 from meadows in the valley of the Zagożdżonki river (51°23′10.4820″ N, 21°33′15.54120″ E), which flows through the Kozienicka forest in central Poland. This isolate was one of several collected during studies on the occurrence of EPNs in Poland [27]. Entomopathogenic nematodes were isolated using the soil trap method and live bait (larvae of the greater wax moth Galleria mellonella L.) [28]. Nematodes were identified by species based on morphometric criteria [29] and using genetic methods [27]. The nematodes were maintained in the laboratory on the larvae of G. mellonella (Lepidoptera: Pyralidae), following the technique used by Kaya and Stock [30].

2.2. Insects

The larvae and pupae of Y. padella and Y. cagnagella were used in the laboratory tests. The species were identified based on the morphological features of adults and the larvae’s host plants [31,32,33]. Larvae and pupae were collected in June and July 2019, respectively, during mass appearances on wild plums (Prunus domestica L. subsp. syriaca (Borkh.) Janch. var. cerea) and on the common spindle tree (Euonymus europaeus L.) in Warsaw (central Poland) in the Ursynów district (52°9′52.198″ N, 21°2′38.409″ E and 52°8′35.043″ N, 21°4′7.631″ E). Larvae (length of 10–12 mm) and pupae were used in the experiments two days after their collection.

2.3. Bioassays

The Petri dish and container tests were used to evaluate the susceptibility of the larvae and pupae of Y. padella and Y. cagnagella to the native isolate.

2.3.1. Petri Dish Tests

The experiments were conducted with n = 60 individuals of the larvae and pupae of Y. padella and Y. cagnagella, according to the 4 variants: 2 insect species × 2 developmental stages: (larvae and pupae) × 60 individuals, total 240 insects. All insects were placed in Petri dishes (90 mm in diameter) lined with filter paper, with five larvae or pupae per dish representing one replicate in a given variant (12 replicates × 5 insects in a dish, total of 60 insects/variant). Then, the nematode strain Steinernema feltiae ZAG15 was applied to the filter paper at a dosage of 50 IJs/insect. The number of IJs was determined by counting them in five droplets (5 µL) of previously prepared nematode suspension using water. The selected concentration for the nematode suspension was obtained by diluting the suspension with tap water or concentrating the suspension via centrifugation [34,35].
Thirty larvae and pupae of both species were used in a comparative variant (control) according to the same scheme as for the variants treated with nematodes: 2 insect species × 2 developmental stages: (larvae and pupae) × 30 individuals (6 replicates × 5 insects in a dish), total 120 insects The control insects were exposed to distilled water instead of nematode suspension.

2.3.2. Container Tests

Larvae and pupae of Y. padella and Y. cagnagella in their webs on the twigs of P. domestica and E. europaeus, respectively, were used for these experiments. Each twig (3–4 cm in length) with one web with larvae or pupae was placed separately in a plastic container (120 mL). Similar to the Petri dishes tests, four variants were tested: 2 insect species × 2 developmental stages: (larvae and pupae). In each variant, 10 containers with the insects in webs were replicates of the tests.
Collected webs contained a total of 153 larvae of Y. padella (mean 15 ± 2.5 per web) and 172 larvae of Y. cagnagella (17 ± 2.6). For pupae, the numbers were 59 (6 ± 1.1) and 65 (17 ± 2.6) individuals, respectively.
Insects were sprayed with the nematode suspension using a 0.5 L hand sprayer (100 IJs/insect). A higher dose was used in this test than in the Petri dish tests because the larvae and pupae were in their webs, which made it difficult for the nematodes to reach the host.
Larvae and pupae in 6 containers for each species and sprayed with distilled water served as a comparative control for the test. The following number of control insects was used: Y. padella—88 larvae (14 ± 2.0) and 35 pupae (6 ± 1.1), and Y. cagnagella—96 larvae (16 ± 1.4) and 40 pupae (7 ± 1.2).
The Petri dishes and containers with insects treated with nematodes or water were placed in a Sanyo incubation chamber at a temperature of 20 °C. The average humidity in the incubation chambers was 60%. After three days, dead insects from the Petri dish and containers were sectioned, and the mortality (percentage of infected larvae or pupae in the analyzed samples) was determined using an Olympus SZX9 stereo microscope (magnification × 3–5).

2.3.3. Field Trials and the Application of Nematodes

The field trials were performed in June and July 2020 in the same places where the larvae and pupae had been collected for the laboratory experiments the year before. Both P. domestica and E. europaeus grew in lines of trees along the road, spaced at 3–5 m intervals. On five trees, Y. padella was treated with nematodes, while nematodes were applied to Y. cagnagella on 10 shrubs. The meteorological data for the study area during seven-day experiments are given in Table 1.
The nematodes were applied in the form of point sprinkling, directed onto webs marked earlier with color tape (10 webs for each growth stage of the insect). The application was carried out in the late afternoon.
During earlier laboratory studies, the mean numbers of caterpillars and pupae per web were calculated. In the case of both Y. padella and Y. cagnagella caterpillars, the nematode dose was 4000 IJs/web (in the form of a suspension in 10 mL of water). For the Y. padella and Y. cagnagella pupae, the dose was 1000 IJs/web, which corresponded to about 200 IJs/insect.
EPNs were applied using a 1 L hand sprinkler with a lance. For the control samples, webs containing the larvae or pupae of Y. padella and Y. cagnagella were treated with 10 mL of water (6 webs of each stage and species). The effectiveness of the application was estimated after seven days when the webs were collected and taken to the laboratory and checked for insect survival.

2.4. Statistical Analysis

The results from the laboratory experiments were statistically processed Rusing R Studio, R version 4.1.2 (Bird Hippie) (1 November 2021) (The R Foundation for Statistical Computing). The Student’s t-test was used to compare the mortality of larvae and pupae within species and differences in the mortality of larvae and pupae between species. The same test was used to compare the mortality of larvae and pupae of both Yponomeuta species depending on the type of laboratory test (Petri dish vs. container test).

3. Results

The highest mortality was found in Y. padella pupae (88.3%) in the Petri dish tests, while the lowest was for Y. cagnagella pupae (15.4%) in the container tests. All the results are presented in Table 2.
No significant (p > 0.05) differences were found in the mortality of larvae and pupae of Y. padella three days after application in both Petri dish and container tests (Table 3). In the Petri dish tests, no significant differences (p > 0.001) between the mortality of Y. cagnagella larvae and pupae were noted. The container tests, however, showed statistically significant differences; the mortality of the larvae was higher (44.19%) than that of the pupae (15.38%) (Table 4).
The comparison of Petri dish and container tests for Y. padella showed significant differences in the mortality of both larvae and pupae (p ≤ 0.001). A higher mortality was noted for the Petri dishes. No significant differences were found in Y. cagnagella (Table 5).
Significant differences were also found when comparing the mortality of Y. padella and Y. cagnagella larvae and pupae. Both larvae and pupae (81.7% and 88.3%, respectively) had greater mortality for Y. padella (Table 6).
In the container tests, however, significant differences were noted only for pupae: the mortality of pupae was greater (35.6%) for Y. padella (Table 7).
Regardless of the stage (larva, pupa) and species of Yponomeuta, all insects survived and showed no signs of infection with nematodes. The application of EPNs in field trials appeared ineffective. The survival of both larvae and pupae was 100%.

4. Discussion

Testing alternative pest control means such as EPNs is needed to curb the use of chemical pesticides on fruit, ornamental trees, and shrubs. The results of our study show that both the larvae (81.7%) and pupae (88.3%) of Y. padella had a greater susceptibility to EPNs than that of Y. cagnagella (50% and 33.3%, respectively). Such an effect may result from the fact that the physical structure and immunological resistance of various host species affect their susceptibility to infection by EPNs [36]. There are a few examples in the literature showing that two closely related host species have very different susceptibility to EPNs. A similar observation was made in a study by Mazurkiewicz et al. [37], where the difference in the mortality of three species of Pieris (P. brassicae L. and P. rapae L.) after applying S. feltiae ZAG15 isolate reached 20%. Studies on the use of EPNs to control moths of the genus Yponomeuta were carried out by Kepenekci et al. [38]. The application of S. feltiae to infect two species (Y. padella and Y. malinellus Zell.) resulted in mortality ranging from 33.3 to 49.9%. In our study, the mortality of Y. padella was much greater and amounted to 81.7%. Kepenekci et al. [38] observed similar mortality (88.9%) in the larvae of Y. padella after applying the isolate Heterorhabditis bacteriophora Poinar. The diverse difference in results between Kepenekci et al. [38] and our studies may indicate differences in pathogenicity, both for isolates within one species and also between nematode species. The dosage does not seem to matter; Kepenekci et al. [38] used a double dose of IJs and obtained a much lower mortality rate when using S. feltiae isolates.
Despite the many studies carried out worldwide on the use of EPNs to control plant pests, only Kepenekci et al. [38] analyzed Yponomeutidae from this aspect. Therefore, in the Section 4, we refer to other moth species whose caterpillars build protective silk webs when feeding. Among moth species, most studies pertained to the fall webworm, Hyphantria cunea Drury (Lepidoptera: Erebidae). In laboratory studies by Yüksel et al. [39], an EPN dose of 50 IJs caused high mortality (75–85%) in the larvae of H. cunea 96 h after application. In our study of Y. padella, comparable mortality had already been reached after 48 h. Gözel [40] used four native EPN isolates and obtained high mortality (66–100%) in H. cunea after 48 h. Other studies on the sensitivity of the larvae of brown-tail moths, Euproctis chrysorrhoea (L.) (Lepidoptera: Erebidae), to native EPN isolates, showed them to be highly effective, producing between 51.6 and 81.3% mortality [41], being thus comparable to our findings. To our knowledge, this study is the first attempt to use nematodes to control Yponomeuta in the field. The prospective results of laboratory experiments on the effectiveness of EPNs against insect pests do not often translate to comparable results in field trials [42]. This was the case in our research, where laboratory tests showed that the isolates had a high pathogenicity towards Yponomeuta; however, the field trials did not demonstrate this effect of the S. feltiae isolate on Y. padella and Y. cagnagella. The ineffectiveness of the EPN application in the field may result from the influence of abiotic factors and also the IJs finding it more difficult to penetrate through the silk webs and pupal cocoons [43]. This was confirmed by our results; the higher larvae and pupae mortality in the Petri dish tests (insects without webs) compared to the container tests (insects in webs) proves the protective role of these structures. On the other hand, the higher mortality of larvae compared to pupae in the container tests indicates that pupal cocoons provide an additional protective barrier against nematodes.
According to Lacey and Georgis [44] and Yüksel et al. [39], after the application of the EPNs, the survival rate and tolerance to drying differed markedly across species and EPN isolates. The most critical period for the survival of IJs is often counted in the minutes and hours directly after application. UV radiation and the associated fast drying are responsible for a rapid decline in the number of IJs (40–80%) during this period [45]. Keeping in mind the high potential of EPNs and the results of the laboratory tests presented here, one should search for other solutions that might prove effective in future field trials. One of the ways to improve the effectiveness of nematode applications might be the use of adjuvants and new formulation technology of EPNs. Their use may slow down the rate at which nematodes dry, increase their effectiveness, and enable EPNs to persist longer on the surface of plants and silk webs [46,47]. One example of the application of adjuvants is found in the research of Beck et al. [48], who showed that the use of the Addit adjuvant during nematode spraying increased the amount of EPNs retained on the leaves. In a study by Hoctor et al. [49], the authors evaluated the effect of four surfactants (Revolution, Aqueduct, Cascade Plus, OARS) on the survival and virulence of H. bacteriophora. The results of this study showed that adding these surfactants increased the survival rate of EPN larvae. Increasing the survival rate of IJs using adjuvants was also demonstrated in studies by Platt et al. [50]. In field studies [51] where Atpolan Bio 80 EC adjuvant was used with S. feltiae ZAG15 isolates, a relatively high effectiveness was achieved with foliar application. Searching for new strains and species is also a feasible approach, which might lead to increased effectiveness based on innate differences in nematode virulence, environmental tolerance, and other properties. Using native species is also preferred in order to reduce environmental risk [42]. Much EPN research has focused on the use of indigenous isolates, as they are expected to be better adapted to local conditions and thus more successful in practical applications [52]. Our earlier studies clearly show that while some strains are always effective, the pathogenicity of others is more dependent on the host [53]. Now, the most promising studies seem to be those by Yüksel et al. [39], which have shown, under laboratory conditions, that the bacterial cell-free supernatants isolated from freshly emerged IJs, not the IJs themselves, have a high degree of effectiveness (20–87.5%) against H. cunea.
Despite the failure in field application, new opportunities for the use of EPNs in pest control should continue to be sought because Yponomeuta is very sensitive to EPNs. The development of a biological method to control Yponomeuta based on EPNs could become an element of integrated pest management (IPM) against these pests. This is extremely important because they occur in places where the use of chemicals should be avoided.

5. Conclusions

The results of the laboratory tests using Petri dishes showed that the larvae and pupae of both species of Yponomeuta were highly susceptible to the native S. feltiae ZAG15 isolate. The susceptibility of larvae and pupae in silk webs was much lower (container tests). However, the efficacy of EPN applications in field trials was not demonstrated. The main reasons for the failure are the silk webs, which make it difficult for IJs to reach the insect, as well as the influence of abiotic factors. Efforts to reduce the use of chemicals require further research to increase the efficacy of EPNs in controlling pests such as Yponomeuta, which will make it possible to include nematodes in IPM programs.

Author Contributions

Conceptualization, K.K., A.M. and D.T.; methodology, K.K., L.F. and B.Z.; writing—original draft preparation, K.K., A.M., D.T., L.F. and B.Z.; writing—review and editing, K.K., A.M., D.T. and I.S. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded with the authors’ own sources at Warsaw University of Life Sciences in Poland.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in this study are available upon request from the authors.

Conflicts of Interest

The authors declare no conflict of interest.

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Table 1. Range of daily air temperature (°C), humidity (%), and sum of daily precipitation (mm) for the area of the experimental sites during the seven-day period after the application of EPNs: a. larvae; b. pupae (https://danepubliczne.imgw.pl/data/dane_pomiarowo_obserwacyjne/, accessed on 27 July 2023).
Table 1. Range of daily air temperature (°C), humidity (%), and sum of daily precipitation (mm) for the area of the experimental sites during the seven-day period after the application of EPNs: a. larvae; b. pupae (https://danepubliczne.imgw.pl/data/dane_pomiarowo_obserwacyjne/, accessed on 27 July 2023).
a. larvae
Date6 June 20207 June 20208 June 20209 June 202010 June 202011 June 202012 June 2020
temperature [°C]11–2414–2615–2313–1814–2317–2617–31
humidity [%]50–9761–9782–9783–9781–9762–9748–97
precipitation [mm]0.510.511.5580
b. pupae
date28 June 202029 June 202030 June 20201 July 20202 July 20203 July 20204 July 2020
temperature [°C]18–3019–2715–2414–2717–2719–2614–26
humidity [%]62–9774–9556–9751–9264–9064–835195
precipitation [mm]2140.501.520
Table 2. Mortality [%] of larvae and pupae in the Petri dish and container tests.
Table 2. Mortality [%] of larvae and pupae in the Petri dish and container tests.
TestsDevelopmental StageMortality
[%]
Y. padellaY. cagnagella
Petri disheslarva81.750
Control group00
Containers larva47.744.2
Control group00
Petri dishespupa88.333.3
Control group00
Containerspupa35.615.4
Control group00
Table 3. Comparison of the mortality of Y. padella larvae and pupae in relation to type of test (Petri dish and container tests).
Table 3. Comparison of the mortality of Y. padella larvae and pupae in relation to type of test (Petri dish and container tests).
Teststdfp-Value
Petri dishes−1.0185114.110.3106
Containers1.62041090.108
Table 4. Comparison of the mortality of Y. cagnagella larvae and pupae in relation to type of test (Petri dish and container tests).
Table 4. Comparison of the mortality of Y. cagnagella larvae and pupae in relation to type of test (Petri dish and container tests).
Teststdfp-Value
Petri dishes1.863117.590.06496
Containers4.8849157.332.525 × 10−6 ***
*** statistically significant differences at p ≤ 0.001.
Table 5. Comparison of the mortality of larvae and pupae for both tests in relation to species (Y. padella and Y. cagnagella).
Table 5. Comparison of the mortality of larvae and pupae for both tests in relation to species (Y. padella and Y. cagnagella).
Speciestdfp-Value
Y. padella8.589311.364.283 × 10−16 ***
Y.cagnagella0.9786233.450.3288
*** statistically significant differences at p ≤ 0.001.
Table 6. Comparison of the mortality for both Y. padella and Y. cagnagella in Petri dish samples in relation to stage (larvae and pupae).
Table 6. Comparison of the mortality for both Y. padella and Y. cagnagella in Petri dish samples in relation to stage (larvae and pupae).
Developmental Stagetdfp-Value
larvae3.8472111.010.0001998 ***
pupae7.4073104.043.523 × 10−11 ***
*** statistically significant differences at p ≤ 0.001.
Table 7. Comparison of the mortality for both Y. padella and Y. cagnagella in the container tests in relation to stage (larvae and pupae).
Table 7. Comparison of the mortality for both Y. padella and Y. cagnagella in the container tests in relation to stage (larvae and pupae).
Developmental Stagetdfp-Value
larvae0.63505318.140.5259
pupae2.6119107.30.01029 *
* statistically significant differences at p ≤ 0.05.
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Kucharska, K.; Mazurkiewicz, A.; Tumialis, D.; Florczak, L.; Zajdel, B.; Skrzecz, I. Sensitivity of Yponomeuta padella and Yponomeuta cagnagella (Lepidoptera: Yponomeutidae) to a Native Strain of Steinernema feltiae (Filipjev, 1934). Agriculture 2023, 13, 1582. https://doi.org/10.3390/agriculture13081582

AMA Style

Kucharska K, Mazurkiewicz A, Tumialis D, Florczak L, Zajdel B, Skrzecz I. Sensitivity of Yponomeuta padella and Yponomeuta cagnagella (Lepidoptera: Yponomeutidae) to a Native Strain of Steinernema feltiae (Filipjev, 1934). Agriculture. 2023; 13(8):1582. https://doi.org/10.3390/agriculture13081582

Chicago/Turabian Style

Kucharska, Kornelia, Anna Mazurkiewicz, Dorota Tumialis, Lidia Florczak, Barbara Zajdel, and Iwona Skrzecz. 2023. "Sensitivity of Yponomeuta padella and Yponomeuta cagnagella (Lepidoptera: Yponomeutidae) to a Native Strain of Steinernema feltiae (Filipjev, 1934)" Agriculture 13, no. 8: 1582. https://doi.org/10.3390/agriculture13081582

APA Style

Kucharska, K., Mazurkiewicz, A., Tumialis, D., Florczak, L., Zajdel, B., & Skrzecz, I. (2023). Sensitivity of Yponomeuta padella and Yponomeuta cagnagella (Lepidoptera: Yponomeutidae) to a Native Strain of Steinernema feltiae (Filipjev, 1934). Agriculture, 13(8), 1582. https://doi.org/10.3390/agriculture13081582

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