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Article

Effect of Synthetic Fungicides Used in Conventional Strawberry Growing System on Hirsutella sp., an Entomopathogenic Fungus of Cyclamen Mite

by
Andréa Duclos
1,
Maxime Delisle-Houde
1,
Joseph Moisan-De Serres
2,
Stéphanie Tellier
3,
Valérie Fournier
1 and
Russell J. Tweddell
1,*
1
Département de Phytologie, Université Laval, Québec, QC G1V 0A6, Canada
2
Laboratoire d’Expertise et de Diagnostic en Phytoprotection du MAPAQ, Québec, QC G1P 3W8, Canada
3
Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec, Direction Territoriale de la Capitale-Nationale, de la Chaudière-Appalaches et de la Côte-Nord, Québec, QC G1N 3Y7, Canada
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(7), 715; https://doi.org/10.3390/agriculture15070715
Submission received: 23 January 2025 / Revised: 7 March 2025 / Accepted: 25 March 2025 / Published: 27 March 2025
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
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Abstract

:
The study investigated the effect of 17 synthetic fungicides used in strawberry fields in Québec (Canada) on the in vitro growth of Hirsutella sp., an entomopathogenic fungus. Isolates collected from cyclamen mites from farms with a conventional growing system (Hirsutella sp. H94 and Hirsutella nodulosa H98) and from a farm with an organic growing system (H. nodulosa H0) were selected for the study. All the fungicides tested strongly inhibited the mycelial growth of the three isolates, although slight differences in sensitivity were observed. Fullback® 125 SC (A.I.: flutriafol), Mettle® 125 ME (A.I.: tetraconazole), NovaTM (A.I.: myclobutanil), and Quadris top® (A.I.: azoxystrobin and difenoconazole) were the most effective at inhibiting the growth of the three isolates. Property® 300SC (A.I.: pyriofenone) was the fungicide with the lowest inhibiting effect on the growth of the three isolates. Isolates H94 and H98 obtained from farms with a conventional growing system, and thus frequently exposed to synthetic fungicides, did not show resistance to the fungicides tested. The study suggests that fungicides might negatively impact the natural populations of the entomopathogenic fungi of the genus Hirsutella on strawberry plants.

1. Introduction

Management of horticultural crops has changed significantly in the last 2 decades, with growing awareness of the damage caused by extensive use of chemical fertilizers and synthetic pesticides [1,2]. Recent research has highlighted the importance of beneficial microorganisms as plant growth promoters and biocontrol agents, in order to decrease the negative impact of conventional approaches on the environment and human health [3,4]. Among beneficial microorganisms, entomopathogenic fungi represent a very interesting yet little-studied group [5,6,7,8]. Some entomopathogenic fungi, such as Beauveria bassiana and Metarhizium anisopliae, have the ability to infect agricultural pests and therefore have potential for use in biocontrol strategies [9,10,11]. In Canada, Metarhizium brunneum (strain F52) and B. bassiana (strains ANT-03, GHA, PPRI 5339, and R444) are the active ingredients of different phytosanitary products registered to control different pests of horticultural crops [12]. Metarhizium brunneum is registered for use against the western flower thrips (Frankliniella occidentalis) and the strawberry root weevil (Otiorhynchus ovatus). Beauveria bassiana is registered for use against several pests, including the greenhouse whitefly (Trialeurodes vaporariorum), aphids, and thrips. According to Maina et al. [13], phytosanitary products containing microbial agents as active ingredients account for 1.3% of the global pesticide market. Among these products, over one-third feature B. bassiana as the active ingredient [13].
The cyclamen mite (Phytonemus pallidus Banks; Acari: Tarsonemidae) is a major pest of strawberries (Fragaria × ananassa) worldwide causing important economic losses [14,15,16,17]. Historical records show that P. pallidus can cause up to 50% yield reduction in strawberry fields [18]. Recent observations have shown that this mite can cause damage resulting in complete yield loss if left unchecked [19]. Since the highly effective acaricide endosulfan was banned, chemical control of the cyclamen mite has been extremely difficult to achieve, given that few active ingredients are registered in Canada for use in strawberry production [20,21]. In this context, new effective long-term management strategies need to be developed [17,22,23,24].
Recently, some cyclamen mites parasitized by Hirsutella sp. were observed in strawberry fields in Québec (Canada), suggesting that this entomopathogenic fungus, which is naturally present in strawberry fields, could eventually help to control cyclamen mite populations. However, cultivated strawberry plants are affected by several diseases caused by fungi and oomycetes, requiring the application of fungicides [25,26,27]. Studies have shown that field application of pesticides, especially fungicides, can have a negative impact on entomopathogenic fungal communities [28,29,30,31,32,33,34].
As part of ongoing research aimed to enhance the presence of Hirsutella spp. in Québec strawberry fields and explore potential conservation of biological control strategies, this study evaluated the impact of 17 synthetic fungicides commonly used in these fields on the in vitro growth of three Hirsutella isolates.

2. Materials and Methods

Fungicides. The fungicides tested in the study are listed in Table 1. The range of concentrations tested for each fungicide was determined according to the manufacturer’s recommendations.
Isolation of Hirsutella sp. strains. Mites covered with a white layer of fungal hyphae were collected between May and October 2022 from young leaves of cultivated strawberry plants growing in fields of different regions (Capitale-Nationale, Montérégie, and Chaudière-Appalaches) of Québec. Dead mites were placed on potato dextrose agar (PDA; Becton, Dickinson and Company, Sparks, MD, USA) supplemented with 50 µg/mL of chloramphenicol (Sigma-Aldrich Inc., St. Louis, MO, USA), penicillin G (Sigma-Aldrich Inc.), and streptomycin sulfate (Thermo Fisher Scientific Inc., Waltham, MA, USA) in Petri dishes (one mite per Petri dish; 60 mm × 15 mm) and incubated at 26 °C in darkness. White dense mycelium surrounding the mite in each Petri dish was isolated. Each isolate was then cultivated in pure culture on PDA.
Hirsutella strain identity. DNA of Hirsutella sp. strains H0, H94, and H98 was extracted using a DNeasy® Plant Mini Kit (Qiagen, Hilden, Germany) according to the manufacturer’s protocol. Internal transcribed spacer region (ITS), 28 S large ribosomal subunit (nrLSU) region, and tef1 genes were targeted using ITS1f/ITS4, LR0R-LR5, and tef1-983F/tef1-2218R as primers, respectively. The identity of the three isolates was determined through Sanger sequencing, followed by a BLAST search (https://blast.ncbi.nlm.nih.gov/Blast.cgi; accessed on 25 February 2025) on the NCBI database (https://www.ncbi.nlm.nih.gov/; accessed on 25 February 2025).
Effect of fungicides on mycelial growth of Hirsutella isolates. PDA agar discs (3 mm diameter) covered with 20-day-old actively growing mycelium of Hirsutella sp. (isolates H0, H94, or H98) were deposited on PDA containing different concentrations of each tested fungicide (Table 1) in Petri dishes. Fungicides were first suspended in sterile distilled water and then incorporated into warm (45–50 °C) PDA. Sterile distilled water was used as control. Petri dishes were incubated at 26 °C in darkness. After different incubation periods (5, 10, 15, 20, and 25 days), the mycelial radial growth of each isolate was measured using a ruler. The percent of inhibition of radial growth (PIRG) was calculated according to the following equation:
PIRG = {[Mycelial radial growth (control) − Mycelial radial growth (fungicide)]/(Mycelial radial growth (control)} × 100
Each combination isolate/fungicide/concentration was tested in six replicates.
Statistical analysis. Analysis of variance (ANOVA) and the Kruskal–Wallis test, a non-parametric alternative, were performed using R (version 4.1.1, R Core Team, 2021, Vienna, Austria). When significant differences were found (p ≤ 0.05), post-hoc comparisons of treatment means were made using the Tukey test.

3. Results

Numerous isolates were obtained from dead mites. Three isolates (H0, H94, and H98; Table 2; Supplementary Table S1) were selected to evaluate the effect of fungicides. The three isolates were first identified as Hirsutella sp. by sequence comparison of ITS [similarity > 99% with GenBank accession no. KJ524680.1 (isolate H0), KJ524690.1 (isolate H94), and KM652172.1 (isolate H98)]. The identity of the entomopathogenic fungus Hirsutella nodulosa associated with P. pallidus was determined based on sequencing of the nrLSU and tef1 regions for isolate H0 and isolate H98. Indeed, these isolates showed a similarity > 99.9% with H. nodulosa [GenBank accession no. KM652117.1 (H0, nrLSU), OQ979221.1 (H0, tef1), KM652117.1 (H98, nrLSU), and KM652000.1 (H98, tef1)] and H. satumaensis [GenBank accession no. KJ524711.1 (H0, nrLSU), KM652008.1 (H0, tef1), KJ524711.1 (H98, nrLSU), and KM652008.1 (H98, tef1)], a species belonging to the H. nodulosa clade. Isolate H94 was not identified at the species level.
All the fungicides tested strongly inhibited the mycelial growth of Hirsutella isolates (Table 3). Fullback® 125 SC (A.I.: flutriafol), Mettle® 125 ME (A.I.: tetraconazole), and NovaTM (A.I.: myclobutanil) completely inhibited the mycelial growth of the three isolates at the minimum concentration tested (0.5 µL/mL, 0.25 µL/mL, and 0.25 mg/mL, respectively) (Table 3). Quadris top® (A.I.: azoxystrobin and difenoconazole) was similarly effective, except against isolate H94 (PIRG = 97%). The other fungicides inhibited mycelial radial growth to varying degrees, ranging from 46% (Property® 300SC; A.I.: pyriofenone) to 97% (Miravis® Prime; A.I.: fludioxonil and pydiflumetofen) at the minimum concentration tested, and from 58% (Property® 300SC) to 100% (Evito® 480 SC; A.I.: fluoxastrobin, Miravis® Prime) at the maximum concentration tested (Table 3). Property® 300SC was the fungicide with the lowest inhibiting effect against all isolates at both minimum and maximum concentrations (Table 3). The growth inhibition caused by Property® 300SC was significantly lower as compared to the growth inhibition caused by the other fungicides tested.
The growth of isolates H0, H94, and H98 over a period of 25 days in the presence of different concentrations of Evito® 480 SC, ScalaMD SC, Property® 300SC, Kenja® 400SC, and Elevate® 50 WDG are presented in Figure 1, Figure 2, Figure 3, Figure 4 and Figure 5. The growth curves of the three isolates are quite similar whatever the concentrations tested for Kenja® 400SC (Figure 4) and Elevate® 50 WDG (Figure 5). The growth curves of isolates H0, H98, and H94 are also quite similar whatever the concentrations tested for Evito® 480 SC (Figure 1A), ScalaMD SC (Figure 2C), and Property® 300SC (Figure 3B), respectively. However, the growth of isolates H98 and H0 is clearly further delayed by the highest concentration of Evito® 480 SC (Figure 1C) and ScalaMD SC (Figure 2A).

4. Discussion

Different species of entomopathogenic fungi from Beauveria, Metarhizium, Hirsutella, and Lecanicillium genera have been widely studied in recent decades for their potential as environmentally safe alternatives to chemical pesticides [8,11,35,36,37]. Hirsutella nodulosa, the species identified in this study, was previously reported to infect P. pallidus [38]. As observed in the identification of the isolates tested in this study, H. nodulosa shows little phylogenetic variation compared to some other Hirsutella species as H. satumaensis, a species belonging to the H. nodulosa clade [39,40]. Conventional management of pathogens/pests in strawberry production requires the use of several synthetic pesticides including numerous fungicides that might threaten the survival of entomopathogenic fungi such as Hirsutella sp. [29,41,42,43,44]. In this context, the study investigated the effect of 17 fungicides used in Québec strawberry fields on the in vitro growth of Hirsutella sp. to determine which ones would least affect the natural occurrence of the fungus.
Active ingredients of the fungicides tested belong to fungicide resistance action committee (FRAC) codes 3 (demethylation inhibitors; difenoconazole, flutriafol, tetraconazole, myclobutanil), 11 (quinone outside inhibitors; azoxystrobin, mandestrobin, fluoxastrobin, trifloxystrobin, pyraclostrobin), 7 (succinate dehydrogenase inhibitors; boscalid, fluxapyroxad, penthiopyrad, pydiflumetofen, isofetamid), 12 (phenylpyrroles; fludioxonil), 9 (anilinopyrimidines; cyprodinil, pyrimethanil), M 04 (phthalimides; captan), 17 (ketoreductase inhibitors; fenhexamid), and 50 (aryl-phenyl-ketones; pyriofenone) [12]. Regardless of the isolate tested, the results showed that fungicides belonging to FRAC chemical group code 3 (demethylation inhibitors) have the strongest PIRG (∼100%). To a lesser extent, fungicides belonging to FRAC chemical group codes M 04, 7, 9, 11, 12, and 17 strongly inhibited Hirsutella mycelial growth. Property® 300SC (A.I.: pyriofenone) (FRAC group code 50) was the only fungicide to show a PIRG lower than 70% for the three isolates tested. Several studies reported the strong inhibiting effect of fungicides from several FRAC chemical group codes including M 01, M 03, 3, 9, 11, and 12 on the growth of different species of Hirsutella [43,45,46]. There are few exceptions such as sulfur (FRAC group code M 02), an active ingredient often used in organic crop production, which has been shown to have a weak effect on the fungus [43].
Fungicides belonging to different chemical families do not target the same metabolic pathways, and fungal growth can be affected differently depending on exposure [47]. In most cases, the growth of isolates H0, H94, and H98 was strongly affected by the tested fungicides, therefore showing comparable sensitivity. Isolate H0 was found to be slightly more sensitive to Intuity® (A.I.: mandestrobin), Evito® 480 SC (A.I.: fluoxastrobin), and Flint (A.I.: trifloxystrobin) which are quinone outside inhibitors. Isolate H94 was found to be slightly more sensitive to Property® 300SC, which is an aryl-phenyl-ketone, at the minimum concentration tested. Isolate H98 was found to be slightly more sensitive to Elevate® 50 WDG (A.I.: fenhexamid), which is a ketoreductase inhibitor.
Entomopathogenic fungi of different genera such as Hirsutella, Beauveria, Conidiobolus, Metarhizium, Paecilomyces, Scopulariopsis, and Lecanicillium were shown to be sensitive to fungicides [33,34,43,48,49]. It has previously been demonstrated that B. bassiana strains can develop resistance to fungicides following exposure in the field [50]. Isolates H94 and H98 obtained from farms with a conventional growing system, and consequently exposed frequently to synthetic fungicides did not show resistance to the fungicides tested.
Conservation biological control is a very complex strategy to apply in crop production [51,52,53]. This strategy showed encouraging results, promoting predator or parasitoid longevity in strawberry fields [54,55,56]. Conservation biological control can be implemented by creating beneficial habitats for predators or by reducing the use of pesticides [51]. In light of the results obtained in this study, it is difficult to recommend a specific strategy to limit the non-targeted effects of fungicides commonly used in strawberries on the entomopathogenic fungi of the genus Hirsutella. However, the in vitro tests described here evaluate the effect of fungicides in direct contact with the fungi and do not always reflect field conditions [57]. Future research should evaluate the effect of these fungicides under field conditions to determine in planta their impact on Hirsutella sp.

5. Conclusions

This study reveals the strong in vitro inhibiting effect of 17 fungicides commonly used in Québec strawberry fields even at the lowest concentrations tested. This suggests that fungicides might negatively impact the natural populations of the entomopathogenic fungi of the genus Hirsutella on strawberry plants. Future work will be undertaken in planta to further investigate the effect of fungicides on the populations of these entomopathogenic fungi.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture15070715/s1, Supplementary Table S1. ITS, nrLSU, and tef1 sequences of Hirsutella isolates.

Author Contributions

Conceptualization, V.F. and R.J.T.; methodology, A.D., M.D.-H. and J.M.-D.S.; writing—original draft preparation, A.D.; writing—review and editing, A.D., M.D.-H., J.M.-D.S., V.F., R.J.T. and S.T.; supervision, V.F. and R.J.T.; funding acquisition, V.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Innov’Action Agroalimentaire program, grant number IA121708, under the Canadian Agricultural Partnership, an agreement between the governments of Canada and Québec.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors would like to thank all the companies that supplied fungicide samples: UPL Limited, BASF Canada, Syngenta Canada, Valent Canada Inc., and Belchim Crop Protection.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 15 00715 g001
Figure 1. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 0.25 µL/mL (▲), 1.5 µL/mL (■), and 3 µL/mL (⬧) of Evito® 480 SC (A.I.: fluoxastrobin). Each value represents the mean of six replicates ± standard deviation.
Figure 1. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 0.25 µL/mL (▲), 1.5 µL/mL (■), and 3 µL/mL (⬧) of Evito® 480 SC (A.I.: fluoxastrobin). Each value represents the mean of six replicates ± standard deviation.
Agriculture 15 00715 g001
Agriculture 15 00715 g002
Figure 2. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 1 µL/mL (▲), 2 µL/mL (■), and 4 µL/mL (⬧) of ScalaMD SC (A.I.: pyrimethanil). Each value represents the mean of six replicates ± standard deviation.
Figure 2. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 1 µL/mL (▲), 2 µL/mL (■), and 4 µL/mL (⬧) of ScalaMD SC (A.I.: pyrimethanil). Each value represents the mean of six replicates ± standard deviation.
Agriculture 15 00715 g002
Agriculture 15 00715 g003
Figure 3. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 0.25 µL/mL (▲), 1 µL/mL (■), and 2 µL/mL (⬧) of Property® 300SC (A.I.: pyriofenone). Each value represents the mean of six replicates ± standard deviation.
Figure 3. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 0.25 µL/mL (▲), 1 µL/mL (■), and 2 µL/mL (⬧) of Property® 300SC (A.I.: pyriofenone). Each value represents the mean of six replicates ± standard deviation.
Agriculture 15 00715 g003
Agriculture 15 00715 g004
Figure 4. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 1 µL/mL (▲), 2 µL/mL (■), and 3 µL/mL (⬧) of Kenja® 400SC (A.I.: isofetamid). Each value represents the mean of six replicates ± standard deviation.
Figure 4. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 1 µL/mL (▲), 2 µL/mL (■), and 3 µL/mL (⬧) of Kenja® 400SC (A.I.: isofetamid). Each value represents the mean of six replicates ± standard deviation.
Agriculture 15 00715 g004
Agriculture 15 00715 g005
Figure 5. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 1.5 µL/mL (▲), 2.5 µL/mL (■), and 3.5 µL/mL (⬧) of Elevate® 50 WDG (A.I.: fenhexamid). Each value represents the mean of six replicates ± standard deviation.
Figure 5. Radial growth of Hirsutella nodulosa H0 (A), Hirsutella sp. H94 (B), and H. nodulosa H98 (C) in the absence (control, ●) and in the presence of 1.5 µL/mL (▲), 2.5 µL/mL (■), and 3.5 µL/mL (⬧) of Elevate® 50 WDG (A.I.: fenhexamid). Each value represents the mean of six replicates ± standard deviation.
Agriculture 15 00715 g005
Table 1. Fungicides and concentrations tested.
Table 1. Fungicides and concentrations tested.
FRAC Code aProductManufacturerActive
Ingredient(s)		Concentrations Tested
3Fullback® 125 SCFMC of Canada Limited (Calgary, AB, Canada)Flutriafol0.5 and 2 µL/mL
3Mettle ® 125 MEGowan Company LLC
(Yuma, AZ, USA)		Tetraconazole0.25 and 2 µL/mL
3NovaTMCorteva Agriscience Canada Company
(Calgary, AB, Canada)		Myclobutanil0.25 and 1 mg/mL
3/11Quadris top®Syngenta Canada Inc.
(Guelph, ON, Canada)		Difenoconazole/Azoxystrobin1 and 7 µL/mL
7FontelisTMCorteva Agriscience Canada CompanyPenthiopyrad2 and 16 µL/mL
7Kenja® 400SCISK Bioscience Corporation
(Painesville, OH, USA)		Isofetamid1, 2, and 3 µL/mL
9ScalaMD SCBayer CropScience
(Calgary, AB, Canada)		Pyrimethanil1, 2, and 4 µL/mL
11Evito® 480 SCUPL AgroSolutions Canada Inc.
(Guelph, ON, Canada)		Fluoxastrobin0.25, 1.25, and 3 µL/mL
11FlintBayer CropScienceTrifloxystrobin0.25 and 1.5 mg/mL
11Intuity®Valent Canada, Inc.
(Guelph, ON, Canada)		Mandestrobin0.5 and 9 µL/mL
7/11MerivonMDBASF Canada Inc.
(Mississauga, ON, Canada)		Fluxapyroxad/Pyraclostrobin0.5 and 9 µL/mL
7/11PristineMD WGBASF Canada Inc.Boscalid/
Pyraclostrobin		1 and 4 mg/mL
7/12Miravis® PrimeSyngenta Canada Inc.Pydiflumetofen/Fludioxonil1 and 5 µL/mL
9/12Switch® 62.5 WGSyngenta Canada Inc.Cyprodinil/
Fludioxonil		1 and 5 mg/mL
17Elevate® 50 WDGUPL AgroSolutions Canada Inc.Fenhexamid1.5, 2.5, and 3.5 mg/mL
50Property® 300SCISK Bioscience CorporationPyriofenone0.25, 1, and 2 µL/mL
M 04Maestro® 80 WSPUPL AgroSolutions
Canada Inc.		Captan1.5 and 3.5 mg/mL
a FRAC Code: number and/or letter combination assigned by the fungicide resistance action committee (FRAC) to group together active ingredients which demonstrate potential for cross resistance.
Table 2. Hirsutella sp. isolates used in the present study.
Table 2. Hirsutella sp. isolates used in the present study.
H. nodulosa H0Hirsutella sp. H94H. nodulosa H98
LocationCapitale-Nationale MontérégieChaudière-Appalaches
Growing systemOrganicConventional Conventional
Sequence comparisonGenBank accession no.Query coverPer. identityGenBank accession no.Query coverPer. identityGenBank accession no.Query coverPer. identity
ITSKJ524680.1100%100%KJ524690.1100%99.64%KM652172.1100%99.83%
nrLSUKM652117.1100%99.9%–––KM652117.1100%99.9%
KJ524711.1100%100%–––KJ524711.1100%100%
tef1OQ979221.1100%100%–––KM652000.1100%100%
KM652008.1100%100%–––KM652008.1100%100%
Table 3. Effects of minimum (min) and maximum (max) concentrations of the fungicides tested on mycelial growth of Hirsutella nodulosa isolates H0 and H98 and Hirsutella sp. isolate H94.
Table 3. Effects of minimum (min) and maximum (max) concentrations of the fungicides tested on mycelial growth of Hirsutella nodulosa isolates H0 and H98 and Hirsutella sp. isolate H94.
Percent Inhibition of Radial Growth (%)
FungicideH. nodulosa H0Hirsutella sp. H94H. nodulosa H98
MinMaxMinMaxMinMax
Fullback® 125 SC100 ± 0 a a100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a
Mettle® 125 ME100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a
NovaTM100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a100 ± 0 a
Quadris top®100 ± 0 a100 ± 0 a97 ± 3 ab100 ± 0 a100 ± 0 a100 ± 0 a
Intuity®95 ± 3 ab99 ± 3 ab84 ± 5 cdef85 ± 3 cd89 ± 3 bcde90 ± 3 bcd
Miravis® Prime 95 ± 3 ab98 ± 3 ab94 ± 6 abc94 ± 7 abc97 ± 2 ab100 ± 0 a
Evito® 480 SC 92 ± 2 abc100 ± 1 a73 ± 11 fg88 ± 3 bcd74 ± 14 g89 ± 3 cde
Switch® 62.5 WG 89 ± 4 bcd96 ± 5 abcd91 ± 3 abcd97 ± 3 ab95 ± 5 abc99 ± 2 a
Flint87 ± 2 bcd88 ± 7 bcdef73 ± 9 fg84 ± 1 d79 ± 5 efg91 ± 3 bcd
Maestro® 80 WSP82 ± 8 de86 ± 3 cdef83 ± 6 cdef85 ± 5 cd85 ± 3 cdef91 ± 3 bcd
PristineMD WG 83 ± 4 de90 ± 6 abcde88 ± 1 abcd91 ± 5 abcd90 ± 1 abcd97 ± 3 ab
ScalaMD SC81 ± 7 de89 ± 3 abcde75 ± 8 efg88 ± 2 bcd76 ± 7 fg82 ± 2 e
MerivonMD81 ± 9 de84 ± 14 ef87 ± 7 bcde89 ± 8 bcd90 ± 5 abcd96 ± 5 abc
FontelisTM83 ± 3 cde84 ± 4 def79 ± 4 defg85 ± 4 cd84 ± 5 defg90 ± 2 bcd
Kenja® 400SC 82 ± 4 de81 ± 7 ef81 ± 4 defg83 ± 3 de85 ± 9 cdef86 ± 9 de
Elevate® 50 WDG 74 ± 4 e77 ± 7 f70 ± 10 g73 ± 11 e82 ± 5 defg83 ± 4 e
Property® 300SC 47 ± 3 f65 ± 6 g58 ± 7 h63 ± 6 f46 ± 7 h58 ± 4 f
a Each value represents the mean of six replicates ± standard deviation. Within the same column, means with the same letter are not significantly different according to the Tukey test (p < 0.05).
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Duclos, A.; Delisle-Houde, M.; Moisan-De Serres, J.; Tellier, S.; Fournier, V.; Tweddell, R.J. Effect of Synthetic Fungicides Used in Conventional Strawberry Growing System on Hirsutella sp., an Entomopathogenic Fungus of Cyclamen Mite. Agriculture 2025, 15, 715. https://doi.org/10.3390/agriculture15070715

AMA Style

Duclos A, Delisle-Houde M, Moisan-De Serres J, Tellier S, Fournier V, Tweddell RJ. Effect of Synthetic Fungicides Used in Conventional Strawberry Growing System on Hirsutella sp., an Entomopathogenic Fungus of Cyclamen Mite. Agriculture. 2025; 15(7):715. https://doi.org/10.3390/agriculture15070715

Chicago/Turabian Style

Duclos, Andréa, Maxime Delisle-Houde, Joseph Moisan-De Serres, Stéphanie Tellier, Valérie Fournier, and Russell J. Tweddell. 2025. "Effect of Synthetic Fungicides Used in Conventional Strawberry Growing System on Hirsutella sp., an Entomopathogenic Fungus of Cyclamen Mite" Agriculture 15, no. 7: 715. https://doi.org/10.3390/agriculture15070715

APA Style

Duclos, A., Delisle-Houde, M., Moisan-De Serres, J., Tellier, S., Fournier, V., & Tweddell, R. J. (2025). Effect of Synthetic Fungicides Used in Conventional Strawberry Growing System on Hirsutella sp., an Entomopathogenic Fungus of Cyclamen Mite. Agriculture, 15(7), 715. https://doi.org/10.3390/agriculture15070715

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