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Are Entomopathogenic Fungal-based Insecticides and Insect Growth Regulator Mixtures Effective Against the Citrus Mealybug, Planococcus citri (Hemiptera: Pseudococcidae), Feeding on Coleus, Solenostemon scutellarioides, Plants under Greenhouse Conditions?

Authors:
Raymond A. Cloyd Department of Entomology, Kansas State University, 123 Waters Hall, Manhattan, KS 66506, USA

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Nathan J. Herrick Department of Entomology, Kansas State University, 123 Waters Hall, Manhattan, KS 66506, USA

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Article Category:
Research Article
Online Publication Date:
15 Sep 2023
Page(s):
1225–1229
Volume/Issue:
Volume 58: Issue 10
Copyright:
© American Society for Horticultural Science 2023
DOI:
https://doi.org/10.21273/HORTSCI17291-23
Open Access
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Abstract

The citrus mealybug, Planococcus citri, is an insect pest of greenhouse-grown horticultural crops. Citrus mealybug causes plant damage when feeding on plant leaves, stems, flowers, and fruits, resulting in a substantial economic loss. Insecticides are applied to manage citrus mealybug populations in greenhouse production systems. Anecdotal information suggests that mixing entomopathogenic fungal-based insecticides with insect growth regulators may be effective for managing citrus mealybug populations under greenhouse conditions. Consequently, we conducted two experiments in a research greenhouse at Kansas State University (Manhattan, KS, USA) in 2023. The experiments were designed to determine the efficacy of three commercially available entomopathogenic fungal-based insecticides [Beauveria bassiana Strain GHA (BotaniGard®), B. bassiana strain PPRI 5339 (Velifer™) and Isaria fumosorosea Apopka Strain 97 (Ancora®)] when mixed with three insect growth regulators [azadirachtin (Azatin® O), novaluron (Pedestal®), and pyriproxyfen (Distance®)] on citrus mealybug feeding on coleus, Solenostemon scutellarioides, plants. The entomopathogenic fungal-based insecticides alone or when mixed with the insect growth regulators were not effective in managing citrus mealybug populations, with <20% mortality during each experiment. In addition, all coleus plants treated with the entomopathogenic fungal-based insecticides had a white, powdery residue on the leaves. Our study demonstrates that entomopathogenic fungal-based insecticides, even when mixed with insect growth regulators, are not effective in managing citrus mealybug populations in greenhouses, which is likely because the environmental conditions (temperature and relative humidity) are not optimal for conidial germination and hyphal infection to occur. Therefore, entomopathogenic fungal-based insecticides have limited use for managing insect pests in greenhouse production systems.

Keywords: azadirachtin; Beauveria bassiana; Isaria fumosorosea; novaluron; pyriproxyfen

Citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), is an insect pest of greenhouse-grown horticultural crops, including the following: coleus, Solenostemon scutellarioides (L.) Codd; grape ivy, Cissus rhombifolia Vahl; croton, Codiaeum variegatum (L.); and Transvaal daisy, Gerbera jamesonii H. Bolus ex Hook.f. (Cloyd 2011; McKenzie 1967; Pillai 2016). Citrus mealybug causes direct plant damage when feeding on plant leaves, stems, flowers, and fruits (Franco et al. 2009; Godfrey et al. 2002; McKenzie 1967). In addition, citrus mealybug excretes honeydew when feeding, which serves as a substrate for black sooty mold (Mani and Shivaraju 2016). Black sooty mold inhibits plant photosynthesis and reduces the aesthetic quality of plants (Charles 1982; Mani and Shivaraju 2016).

One female citrus mealybug adult can produce more than 400 eggs during her lifetime (Copeland et al. 1985). Consequently, killing the nymphs (crawlers) before they develop into adults is important for managing citrus mealybug populations (Pillai 2016). Insecticides are used to manage citrus mealybug populations in greenhouse production systems; however, management can be difficult when using insecticides (Franco et al. 2009; Parrella 1999; Pillai 2016). Citrus mealybug populations are difficult to manage with insecticides because the later instars and adults possess a hydrophobic waxy covering that protects citrus mealybugs from insecticide sprays, and citrus mealybugs reside in protected areas on plants that reduce exposure to insecticide spray applications (Charles 1982; Franco et al. 2009; Herrick and Cloyd 2017; Venkatesan et al. 2016).

Entomopathogenic fungi are the active ingredient in commercially available entomopathogenic fungal-based insecticides registered for use against aphids, whiteflies, and the citrus mealybug. Entomopathogenic fungal-based insecticides include Beauveria bassiana Strain GHA (BotaniGard®; Laverlam International Corp., Butte, MT, USA), Isaria fumosorosea Apopka Strain 97 (Ancora®; OHP, Inc., Bluffton, SC, USA), and B. bassiana strain PPRI 5339 (Velifer™; BASF Corp., Research Triangle Park, NC, USA).

Commercial formulations of entomopathogenic fungi are contact microbial insecticides composed of fungal conidia. Conidia germinate on the insect cuticle (exoskeleton), and then hyphae penetrate the cuticle by releasing enzymes such as proteases and chitinases. Hyphae enter the insect body and grow in the hemocoel (body cavity). Death of the insect usually occurs because of mechanical damage, release of fungal toxins, or both (Clarkson and Charnley 1996; Ortiz-Urquiza and Keyhani 2013). Infection and mortality of insects by entomopathogenic fungal-based insecticides takes longer (in days) than commonly used contact insecticides (Zhang et al. 2021).

Herrick and Cloyd (2023) found that entomopathogenic fungal-based insecticides alone are not effective in managing citrus mealybug populations under greenhouse conditions. However, anecdotal information suggests that mixing entomopathogenic fungal-based insecticides with insect growth regulators may enhance efficacy by increasing hyphal penetration through the insect cuticle (Akbar et al. 2005; Hernandez et al. 2012; Kivett et al. 2016). Insect growth regulators are compounds that disrupt growth and development by inhibiting chitin formation, mimicking juvenile hormones, or interrupting the molting process (Tunaz and Uygun 2004; Yu 2008).

The objective of our study was to determine the effects of spray applications of entomopathogenic fungal-based insecticides and insect growth regulator mixtures on citrus mealybug populations feeding on coleus, S. scutellarioides, plants under greenhouse conditions.

Materials and Methods

Two replicated experiments were conducted in a research greenhouse at Kansas State University (Manhattan, KS, USA) in 2023. A laboratory colony of the citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), used in the experiments was maintained on butternut squash, Cucurbita maxima Duchesne, at 22 to 27 °C, 50% to 60% relative humidity, and under constant light in a laboratory located in the Department of Entomology at Kansas State University (Manhattan, KS, USA). Voucher specimens (number 254) are deposited in the Kansas State University Museum of Entomological and Prairie Arthropod Research (Manhattan, KS, USA).

Expt. 1.

Seventy coleus, Solenostemon scutellarioides (cultivar Campfire), plugs (young plants—either seedlings or cuttings grown as single units in modular trays) were ordered from Ball Horticultural Company (West Chicago, IL, USA), with the source being Dickman Farms and Greenhouses (Auburn, NY, USA). Upon receipt, plugs were transplanted into 15.2-cm-diameter containers with a growing medium (Berger® BM1; Saint-Modeste, Quebec, Canada) composed of 75% to 85% course sphagnum peatmoss, perlite, vermiculite, and a wetting agent. Plants were grown for 73 d before use in the experiment and were irrigated with 400 to 500 mL of tap water as needed.

The experiment was had a completely randomized design. The plants were artificially infested with ∼10 second to early-third instar citrus mealybug nymphs from the laboratory colony on 6 Jan 2023. Coleus plants were spaced 0.30 m apart on a bench. Spray applications of the treatments were performed for all the coleus plants [22.2 ± 0.5 cm (mean ± SEM) in height with 19.3 ± 1.1 leaves] on 9 Jan 2023. There were 14 treatments, including a water control, and a treatment using a standard insecticide, flupyradifurone (Altus™), with five replications per treatment (Table 1). The treatments were prepared in 946 mL of tap water, with ∼60 mL applied to the upper and lower leaf surfaces and stems of each coleus plant. The spray solution volume was sufficient to thoroughly cover the leaves and stems.

Table 1.

Active ingredient, trade name, rate used (per 946 mL), and manufacturer information associated with treatments used in the two experiments. The entomopathogenic fungal-based insecticides were BotaniGard®, Velifer™, and Ancora®. The insect growth regulators were Distance®, Azatin® O, and Pedestal®.
Table 1.

The environmental conditions (temperature and relative humidity) in the greenhouse were measured using a Digital Humidity/Temperature Meter (Fisherbrand Traceable®; Fisher Science Education, Hanover Park, IL, USA). Plants were grown under natural daylight conditions. Whole plants were destructively sampled 10 d after applying the treatments, and the numbers of live and dead citrus mealybugs were recorded. Citrus mealybugs that did not move after prodding with a dissecting probe were considered dead. The presence of male pupae, which indicated that citrus mealybug nymphs were able to complete development, or females that produced egg masses were counted as alive.

Expt. 2.

The second experiment was conducted in a manner similar to that of the first experiment. However, plants were grown for 131 d before use in the experiment. The coleus plants were artificially infested with ∼10 second to early-third instar citrus mealybug nymphs from the laboratory colony on 7 Mar 2023. Spray applications of the treatments were performed for all the coleus plants (22.6 ± 0.6 cm in height with 9.2 ± 0.5 leaves) on 8 Mar 2023. The treatments were the same as those of Expt. 1 (Table 1). Treatments were prepared in 946 mL of tap water, with ∼40 mL applied to the upper and lower leaf surfaces and stems of each coleus plant. The coleus plants had fewer leaves than the plants in the first experiment; therefore, less spray solution was needed. Regardless, the spray solution volume was sufficient to thoroughly cover the leaves and stems.

The environmental conditions (temperature and relative humidity) in the greenhouse were measured in the same manner as that during the first experiment. As in the first experiment, plants were grown under natural daylight conditions. Whole plants were destructively sampled 10 d after applying the treatments, and the numbers of live and dead citrus mealybugs were recorded. Citrus mealybugs that did not move after prodding with a dissecting probe were considered dead. The presence of male pupae, which indicated that citrus mealybug nymphs were able to complete development, or females that produced egg masses were counted as alive.

Statistical analysis.

The citrus mealybug mortality rate was calculated by dividing the number of dead citrus mealybugs on each coleus plant by the total number associated with each coleus plant, and then multiplying by 100. Data were analyzed using an analysis of variance (ANOVA) (PROC GLIMMIX, α = 0.05) with treatment as the main effect. Individual treatment means were separated using Tukey’s honestly significant difference test when the ANOVA indicated a significant treatment effect (SAS/STAT® 14.2 user’s guide 2016).

Results

During the first experiment, there was a significant treatment effect associated with the citrus mealybug mortality rate (F = 13.08; df = 13, 52; P < 0.0001). The flupyradifurone (Altus™) treatment at 1.03 mL/946 mL resulted in significantly higher citrus mealybug mortality (between 60% and 70%) than all the other treatments and the water control, which had citrus mealybug mortality rates <20% (Fig. 1). None of the treatments exhibited phytotoxic effects on the coleus plants. However, all of the coleus plants treated with entomopathogenic fungal-based insecticides had a white, powdery residue on the leaves. The temperature in the greenhouse during the experiment ranged from 8.9 to 40.0 °C, with relative humidity of 0% to 66%.

Fig. 1.
Fig. 1.

Mean (± SEM) mortality rates of citrus mealybug (CMB), Planococcus citri, in Expt. 1 after exposure to spray applications of the following treatments: (1) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL, (2) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL, (3) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL, (4) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (5) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (6) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (7) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (8) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (9) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (10) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (11) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (12) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (13) flupyradifurone (Altus™) at 1.03 mL/946 mL, and (14) water control. Means followed by the same letter are not significantly different (P > 0.05; n = 645). The vertical bar within each mean represents the SEM.

Citation: HortScience 58, 10; 10.21273/HORTSCI17291-23

During the second experiment, there was also a significant treatment effect affiliated with the citrus mealybug mortality rate (F = 6.13; df = 13, 52; P < 0.0001). Again, the flupyradifurone (Altus™) treatment at 1.03 mL/946 mL resulted in significantly higher citrus mealybug mortality (between 60% and 70%) than the other treatments and the water control, which had citrus mealybug mortality rates <20% (Fig. 2). No treatment was phytotoxic to the coleus plants. However, all of the coleus plants treated with entomopathogenic fungal-based insecticides had a white, powdery residue on the leaves. The temperature in the greenhouse during the experiment ranged from 18.9 to 45.0 °C, with relative humidity of 0% to 38%.

Fig. 2.
Fig. 2.

Mean (± SEM) mortality rates of citrus mealybug (CMB), Planococcus citri, in Expt. 2 after exposure to spray applications of the following treatments: (1) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL, (2) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL, (3) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL, (4) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (5) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (6) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (7) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (8) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (9) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (10) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (11) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (12) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (13) flupyradifurone (Altus™) at 1.03 mL/946 mL, and (14) water control. Means followed by the same letter are not significantly different (P > 0.05; n = 553). The vertical bar within each mean represents the SEM.

Citation: HortScience 58, 10; 10.21273/HORTSCI17291-23

Discussion

We found that the entomopathogenic fungal-based insecticides alone and in mixtures with the insect growth regulators tested were not effective in managing citrus mealybug populations on coleus plants under greenhouse conditions. The lack of efficacy may be attributed to the waxy covering protecting citrus mealybugs, which prevents the conidia of the entomopathogenic fungi from attaching to the cuticle (Herrick and Cloyd 2023).

It has been suggested, although anecdotally, that adding an insect growth regulator to a spray solution may increase the efficacy of entomopathogenic fungal-based insecticides against the citrus mealybug (Herrick and Cloyd 2023). However, the mechanisms responsible for increasing efficacy are unclear. Nevertheless, in our study, we found that none of the three insect growth regulators increased the efficacy of the three entomopathogenic fungal-based insecticides.

The three insect growth regulators tested in our study have different modes of action. Pyriproxyfen (Distance®) is a juvenile hormone mimic that affects the hormonal balance of insects, resulting in suppression of embryogenesis, metamorphosis, and adult formation (Ishaaya et al. 1994; Ishaaya and Horowitz 1995; Ware and Whitacre 2004). Novaluron (Pedestal®) is a chitin synthesis inhibitor that interrupts the synthesis and/or transport of specific proteins involved in chitin assemblage in the cuticle (Oberlander and Silhacek 1998; Ware and Whitacre 2004). Azadirachtin (Azatin® O) is an ecdysone antagonist that delays the molting process by inhibiting the molting hormone, ecdysone (Islam et al. 2010; James 2003; Schmutterer 1990). A delay in the molting process may allow more time for the hyphae of the entomopathogenic fungi to penetrate the insect cuticle (Akbar et al. 2005; Hernandez et al. 2012; Schmutterer 1990). However, Kivett et al. (2016) found that azadirachtin did not enhance the efficacy of the entomopathogenic fungi Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae) or Isaria fumosoroseus Wie Brown and Smith (Hypocreales: Cordycipitaceae) against the western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). During a greenhouse study in which azadirachtin (Ornazin® 3% EC; SePRO, Carmel, IN, USA) was added to two formulations of B. bassiana (BotaniGard® ES and BotaniGard® WP), there was no evidence of increased efficacy against western flower thrips larvae, with or without azadirachtin (Cloyd RA, unpublished data).

The main factor responsible for the failure of entomopathogenic fungal-based insecticides to manage citrus mealybug populations in greenhouses is unfavorable environmental conditions, such as temperature and relative humidity. Temperature and relative humidity can substantially affect the ability of entomopathogenic fungi to manage insect pest populations (Demirci et al. 2011; Tanada and Kaya 1993). Temperature can influence the effectiveness of entomopathogenic fungal-based insecticides by affecting conidia survival, conidia germination, hyphal growth, and insect mortality rate (Qayyum et al. 2021; Walstad et al. 1970). The optimal temperature range for germination and infection of B. bassiana is 25 to 30 °C (Ekesi et al. 1999; Fargues and Luz 2000; Tang and Hou 2001).

High relative humidity is important for conidia survival, conidia germination, and hyphal penetration in the hemocoel (Daoust and Roberts 1983; Hajek et al. 1990; Tang and Hou 2001). The germination of entomopathogenic fungal conidia only occurs when relative humidity is 90% (Ramoska 1984). For example, B. bassiana conidia will not germinate at relative humidity <92% (Ferron 1977). The temperature and relative humidity associated with the two greenhouse experiments ranged from 8.9 to 45 °C and from 0% to 66%, respectively. Consequently, these fluctuating environmental parameters are probably not conducive for entomopathogenic fungal infection, which likely was responsible for the <20% mortality rate of the citrus mealybug populations on the coleus plants treated with the entomopathogenic fungal-based insecticides alone or when mixed with insect growth regulators. The environmental parameters in the research greenhouse where we conducted our study are representative of commercial production greenhouses.

In addition to the issues associated with the environmental conditions described, we also observed that all coleus plants treated with the entomopathogenic fungal-based insecticides had white, powdery residues on the leaves after the spray applications. Residues on plants are concerning because any residue can affect plant salability (Ahmed et al. 2001).

The nonfungal-based insecticide, flupyradifurone (Altus™) provided between 60% and 70% mortality of the citrus mealybugs in each experiment. Flupyradifurone is active on sucking insect pests of horticultural crops, including aphids and whiteflies, and binds to the nicotinic acetylcholine receptors in the central nervous system (Nauen et al. 2014). We have found, in previous studies, that flupyradifurone is an effective insecticide for managing citrus mealybug populations on coleus plants (Herrick NJ and Cloyd RA, unpublished data).

In conclusion, based on the findings of Herrick and Cloyd (2023) and the findings of the current study, entomopathogenic fungal-based insecticides alone or in mixtures with insect growth regulators are not effective in managing citrus mealybug populations on coleus plants. The temperature and relative humidity must be optimal for germination and infection to occur. Otherwise, entomopathogenic fungal-based insecticides have limited use in the management of insect pests in greenhouse production systems.

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    • Export Citation

  • Oberlander H, Silhacek DL. 1998. New perspectives on the mode of action of benzoylphenyl urea insecticides, p 92–105. In: Ishaaya I, Degheele D (eds). Insecticides with novel modes of action. Springer-Verlag, Berlin, Germany.

  • Ortiz-Urquiza A, Keyhani NO. 2013. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects. 4:357–374. https://doi.org/10.3390/insects4030357.

    • Search Google Scholar
    • Export Citation

  • Parrella MP. 1999. Arthropod fauna, p 213–250. In: Stanhill G, Zvi Enoch H (eds). Ecosystems of the world 20. Greenhouse Ecosystems. Elsevier, New York, NY, USA.

  • Pillai KG. 2016. Glasshouse, greenhouse and polyhouse crops, p 621–628. In: Mani M, Shivaraju C (eds). Mealybugs and their management in agricultural and horticultural crops. Springer (India) Pvt. Ltd, New Delhi, India.

  • Qayyum MB, Bilal H, Ullah UN, Ali H, Raza H, Wajid M. 2021. Factors affecting the epidzootics of entomopathogenic fungi-a review. J. Biores. Manag. 8:78–85. https://doi.org/10.35691/JBM.1202.0204.

    • Search Google Scholar
    • Export Citation

  • Ramoska WA. 1984. The influence of relative humidity on Beauveria bassiana infectivity and replication in the chinch bug, Blissus leucopterus. J Invertebr Pathol. 43:389–394. https://doi.org/10.1016/0022-2011(84)90085-5.

    • Search Google Scholar
    • Export Citation

  • SAS/STAT® 14.2 user’s guide. 2016. SAS Institute Inc, Cary, NC, USA.

  • Schmutterer H. 1990. Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annu Rev Entomol. 35:271–297. https://doi.org/10.1146/annurev.en.35.010190.001415.

    • Search Google Scholar
    • Export Citation

  • Tanada Y, Kaya HK. 1993. Insect pathology. Academic Press, San Diego, CA, USA.

  • Tang LC, Hou RF. 2001. Effects of environmental factors on virulence of the entomopathogenic fungus, Nomuraea rileyi, against the corn earworm, Helicoverpa armigera (Lep., Noctuidae). J Appl Entomol. 125:243–248. https://doi.org/10.1046/j.1439-0418.2001.00544.x.

    • Search Google Scholar
    • Export Citation

  • Tunaz H, Uygun N. 2004. Insect growth regulators for insect pest control. Turk J Agric For. 28:377–387. https://www.researchgate.net/publication/279704506.

    • Search Google Scholar
    • Export Citation

  • Venkatesan T, Jalali SK, Ramya SL, Prathibha M. 2016. Insecticide resistance and its management in mealybugs, p 223–229. In: Mani M, Shivaraju C (eds). Mealybugs and their management in agricultural and horticultural crops. Springer (India) Pvt. Ltd, New Delhi, India.

  • Walstad JD, Anderson RF, Stambauch WJ. 1970. Effects of environmental conditions on two species of muscardine fungi (Beauveria bassiana and Metarhizium anisopliae). J Invertebr Pathol. 16:221–226. https://doi.org/10.1016/0022-2011(70)90063-7.

    • Search Google Scholar
    • Export Citation

  • Ware GW, Whitacre DM. 2004. The pesticide book (6th ed). MeisterPro Information Resources, Willoughby, OH, USA.

  • Yu SJ. 2008. The toxicology and biochemistry of insecticides. Taylor & Francis Group, LCC, Boca Raton, FL, USA.

  • Zhang Z, Zheng C, Keyhani NO, Gao Y, Wang J. 2021. Infection of the western flower thrips, Frankliniella occidentalis, by the insect pathogenic fungus Beauveria bassiana. Agron. 11:1910. https://doi.org/10.3390/agronomy11101910.

    • Search Google Scholar
    • Export Citation
Received:
07 Jun 2023
|
Accepted:
28 Jul 2023
|
Published online:
15 Sep 2023
|
Published-print:
01 Oct 2023
Received:
07 Jun 2023
|
Accepted:
28 Jul 2023
|
Published online:
15 Sep 2023
|
Published-print:
01 Oct 2023
  • Fig. 1.
    View in gallery
    Fig. 1.

    Mean (± SEM) mortality rates of citrus mealybug (CMB), Planococcus citri, in Expt. 1 after exposure to spray applications of the following treatments: (1) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL, (2) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL, (3) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL, (4) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (5) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (6) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (7) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (8) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (9) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (10) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (11) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (12) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (13) flupyradifurone (Altus™) at 1.03 mL/946 mL, and (14) water control. Means followed by the same letter are not significantly different (P > 0.05; n = 645). The vertical bar within each mean represents the SEM.

  • Fig. 2.
    View in gallery
    Fig. 2.

    Mean (± SEM) mortality rates of citrus mealybug (CMB), Planococcus citri, in Expt. 2 after exposure to spray applications of the following treatments: (1) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL, (2) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL, (3) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL, (4) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (5) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (6) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (7) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (8) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (9) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (10) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (11) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (12) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (13) flupyradifurone (Altus™) at 1.03 mL/946 mL, and (14) water control. Means followed by the same letter are not significantly different (P > 0.05; n = 553). The vertical bar within each mean represents the SEM.

Fig. 1.

Mean (± SEM) mortality rates of citrus mealybug (CMB), Planococcus citri, in Expt. 1 after exposure to spray applications of the following treatments: (1) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL, (2) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL, (3) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL, (4) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (5) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (6) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (7) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (8) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (9) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (10) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (11) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (12) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (13) flupyradifurone (Altus™) at 1.03 mL/946 mL, and (14) water control. Means followed by the same letter are not significantly different (P > 0.05; n = 645). The vertical bar within each mean represents the SEM.
Fig. 2.

Mean (± SEM) mortality rates of citrus mealybug (CMB), Planococcus citri, in Expt. 2 after exposure to spray applications of the following treatments: (1) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL, (2) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL, (3) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL, (4) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (5) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (6) Beauveria bassiana Strain GHA (BotaniGard®) at 2.26 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (7) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (8) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (9) Isaria fumosorosea Apopka Strain 97 (Ancora®) at 1.98 g/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (10) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + pyriproxyfen (Distance®) at 0.88 mL/946 mL, (11) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + azadirachtin (Azatin® O) at 1.18 mL/946 mL, (12) Beauveria bassiana strain PPRI 5339 (Velifer™) at 0.96 mL/946 mL + novaluron (Pedestal®) at 0.59 mL/946 mL, (13) flupyradifurone (Altus™) at 1.03 mL/946 mL, and (14) water control. Means followed by the same letter are not significantly different (P > 0.05; n = 553). The vertical bar within each mean represents the SEM.

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  • Oberlander H, Silhacek DL. 1998. New perspectives on the mode of action of benzoylphenyl urea insecticides, p 92–105. In: Ishaaya I, Degheele D (eds). Insecticides with novel modes of action. Springer-Verlag, Berlin, Germany.

  • Ortiz-Urquiza A, Keyhani NO. 2013. Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects. 4:357–374. https://doi.org/10.3390/insects4030357.

    • Search Google Scholar
    • Export Citation

  • Parrella MP. 1999. Arthropod fauna, p 213–250. In: Stanhill G, Zvi Enoch H (eds). Ecosystems of the world 20. Greenhouse Ecosystems. Elsevier, New York, NY, USA.

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  • Qayyum MB, Bilal H, Ullah UN, Ali H, Raza H, Wajid M. 2021. Factors affecting the epidzootics of entomopathogenic fungi-a review. J. Biores. Manag. 8:78–85. https://doi.org/10.35691/JBM.1202.0204.

    • Search Google Scholar
    • Export Citation

  • Ramoska WA. 1984. The influence of relative humidity on Beauveria bassiana infectivity and replication in the chinch bug, Blissus leucopterus. J Invertebr Pathol. 43:389–394. https://doi.org/10.1016/0022-2011(84)90085-5.

    • Search Google Scholar
    • Export Citation

  • SAS/STAT® 14.2 user’s guide. 2016. SAS Institute Inc, Cary, NC, USA.

  • Schmutterer H. 1990. Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annu Rev Entomol. 35:271–297. https://doi.org/10.1146/annurev.en.35.010190.001415.

    • Search Google Scholar
    • Export Citation

  • Tanada Y, Kaya HK. 1993. Insect pathology. Academic Press, San Diego, CA, USA.

  • Tang LC, Hou RF. 2001. Effects of environmental factors on virulence of the entomopathogenic fungus, Nomuraea rileyi, against the corn earworm, Helicoverpa armigera (Lep., Noctuidae). J Appl Entomol. 125:243–248. https://doi.org/10.1046/j.1439-0418.2001.00544.x.

    • Search Google Scholar
    • Export Citation

  • Tunaz H, Uygun N. 2004. Insect growth regulators for insect pest control. Turk J Agric For. 28:377–387. https://www.researchgate.net/publication/279704506.

    • Search Google Scholar
    • Export Citation

  • Venkatesan T, Jalali SK, Ramya SL, Prathibha M. 2016. Insecticide resistance and its management in mealybugs, p 223–229. In: Mani M, Shivaraju C (eds). Mealybugs and their management in agricultural and horticultural crops. Springer (India) Pvt. Ltd, New Delhi, India.

  • Walstad JD, Anderson RF, Stambauch WJ. 1970. Effects of environmental conditions on two species of muscardine fungi (Beauveria bassiana and Metarhizium anisopliae). J Invertebr Pathol. 16:221–226. https://doi.org/10.1016/0022-2011(70)90063-7.

    • Search Google Scholar
    • Export Citation

  • Ware GW, Whitacre DM. 2004. The pesticide book (6th ed). MeisterPro Information Resources, Willoughby, OH, USA.

  • Yu SJ. 2008. The toxicology and biochemistry of insecticides. Taylor & Francis Group, LCC, Boca Raton, FL, USA.

  • Zhang Z, Zheng C, Keyhani NO, Gao Y, Wang J. 2021. Infection of the western flower thrips, Frankliniella occidentalis, by the insect pathogenic fungus Beauveria bassiana. Agron. 11:1910. https://doi.org/10.3390/agronomy11101910.

    • Search Google Scholar
    • Export Citation
Raymond A. Cloyd Department of Entomology, Kansas State University, 123 Waters Hall, Manhattan, KS 66506, USA

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Nathan J. Herrick Department of Entomology, Kansas State University, 123 Waters Hall, Manhattan, KS 66506, USA

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Contributor Notes

We thank Dr. Mary Beth Kirkham from the Department of Agronomy and Dr. Kun Yan Zhu from the Department of Entomology at Kansas State University (Manhattan, KS, USA) for reviewing an initial draft of the manuscript.

R.A.C. is the corresponding author. E-mail: rcloyd@ksu.edu.

Received:
07 Jun 2023
|
Accepted:
28 Jul 2023
|
Published online:
15 Sep 2023
|
Published-print:
01 Oct 2023
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