Abstract
Entomopathogenic fungi (EPF) and essential oils (EOs) can show either positive or negative interactions when used for controlling insect pests. First, the insecticidal efficacy of EPF including Beauveria bassiana isolates Z1 and IRAN1395C, Lecanicillium lecanii, and Paecilomyces lilacinus was tested against adults of Tribolium castaneum using two methods (standard insect dip and wheat diet incorporation). Additionally, the toxicity of EOs from Trachyspermum ammi, Foeniculum vulgare, Eucalyptus globulus, Salvia mirzayanii, Majorana hortensis, and Thymus vulgaris was evaluated against adult T. castaneum. Thereafter, the effect of an LC25 concentration of F. vulgare (86.13 µl L−1), T. ammi (235.2 µl L−1), and E. globulus (111.33 µl L−1) EOs on mycelial growth, spore germination, and sporulation of the EPF was determined. In standard dip bioassay, the lowest LT50 of 10.4 days was induced by L. lecanii, while the wheat diet incorporation method resulted in LT50 values ranging between 13.1 and 15.2 days. The LC50 values for E. globulus, F. vulgare, and T. ammi were 162.3, 140.3, and 310 μl L−1 air against adults, respectively. The EOs examined showed strong inhibition of mycelial growth, conidial germination, and sporulation at sublethal concentrations. EOs of F. vulgare and T. ammi completely inhibited mycelial growth and sporulation of the tested EPF. Germination inhibition ranged from 100% in L. lecanii exposed to EO from F. vulgare to 52.3% in B. bassiana Z1 exposed to EO from T. ammi. Based on the results, although EOs and EPF are successful agents to control adults T. castaneum when used separately, it cannot be applied in combination because of the conflicting effect.
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References
Abou-Jawdah Y, Sobh H, Salameh A (2002) Antimycotic activities of selected plant flora, growing wild in Lebanon, against phytopathogenic fungi. J Agric Food Chem 50:3208–3213
Abou-Taleb HK, Mohamed MIE, Shawir MS, Abdelgaleil SAM (2016) Insecticidal properties of essential oils against Tribolium castaneum (Herbst) and their inhibitory effects on acetylcholinesterase and adenosine triphosphatases. Nat Prod Res 30(6):710–714
Ahmed BI (2010) Potentials of entomopathogenic fungi in controlling the menace of maize weevil Sitophilus zeamais Motsch (Coleoptera: Curculinidae) on stored maize grain. Arch Phytopathol Plant Protect 43(2):107–115
Ambethger V (2009) Potential of entomopathogenic fungi in insecticide resistance management (IRM): a review. J Biopestic 2(2):177–193
Anderson TE, Roberts DW (1983) Compatibility of Beauveria bassiana isolates with insecticide formulations used in Colorado potato beetle (Coleoptera: Chrysomelidae) control. J Econ Entomol 76:1437–1441
Anonymous (1990) EPPO Bull 20: 399–400
Arthur FH, Subramanyam Bh (2012) Chemical control in stored products. In: Hagstrum DW, Phillips TW, Cuperus G (eds) Stored Product Protection. Kansas State University, Manhattan, pp 95–100
Ashraf M, Farooq M, Shakeel M, Din N, Hussain S, Saeed N, Shakeel Q, Rajput NA (2017) Influence of entomopathogenic fungus, Metarhizium anisopliae, alone and in combination with diatomaceous earth and thiamethoxam on mortality, progeny production, mycosis, and sporulation of the stored grain insect pests. Environ Sci Pollut Res 24(36):28165–28174
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils: a review. Food Chem Toxicol 46:446–475
Barra P, Rosso L, Etcheverry M (2013) Isolation and identification of entomopathogenic fungi and their evaluation against Tribolium confusum, Sitophilus zeamais, and Rhyzopertha dominica in stored maize. J Pest Sci 86:217–226
Bedini S, Bougherra HH, Flamini G, Cosci F, Belhamel K, Ascrizzi R, Conti B (2016) Repellency of anethole- and estragole-type fennel essential oils against stored grain pests: the different twins. Bull Insectol 69:149–157
Caballero-Gallardo K, Olivero- Verbel J, Stashenko EE (2012) Repellency and toxicity of essential oils from Cymbopogon martinii, Cymbopogon flexuosus and Lippia origanoides cultivated in Colombia against Tribolium castaneum. J Stored Prod Res 50:62–65
Celar FA, Kos K (2016) Effects of selected herbicides and fungicides on growth, sporulation and conidial germination of entomopathogenic fungus Beauveria bassiana. Pest Manag Sci 72(11):2110-2117
Chaubey MK (2007a) Insecticidal activity of Trachyspermum ammi (Umbelliferae), Anethum graveolens (Umbelliferae) and Nigella sativa (Ranunculaceae) essential oils against stored product beetle Tribolium castaneum Herbst (Coleoptera: Tenebrionidae). Afr J Agric Res 2(11):596–600
Chaubey MK (2007b) Toxicity of essential oils from Cuminum cyminum (Umbelliferae), Piper nigrum (Piperaceae) and Foeniculum vulgare (Umbelliferae) against stored-product beetle Tribolium castaneum Herbst (Coleoptera: Tenebrionidae). Electr J Environ Agric Food Chem 6:1719–1727
Cosimi S, Rossi E, Cioni PL, Canale A (2009) Bioactivity and qualitative analysis of some essential oils from Mediterranean plants against stored-product pests: evaluation of repellency against Sitophilus zeamais Motschulsky, Cryptolestes ferrugineus (Stephens) and Tenebrio molitor L. J Stored Prod Res 45:125–132
Daglish GJ (2008) Impact of resistance on the efficacy of binary combinations of spinosad, chlorpyrifos-methyl and s-methoprene against five stored-grain beetles. J Stored Prod Res 44:71–76
Dal Bello GM, Fuse CB, Pedrini N, Padin SB (2018) Insecticidal efficacy of Beauveria bassiana, diatomaceous earth and fenitrothion against Rhyzopertha dominica and Tribolium castaneum on stored wheat. Int J Pest Manage 64:279–286
Duarte R, Gonçalves K, Espinosa D, Moreira L, De Bortoli S, Humber R, Polanczyk R (2016) Potential of entomopathogenic fungi as biological control agents of diamondback moth (Lepidoptera: Plutellidae) and compatibility with chemical insecticides. J Econ Entomol 109:594–601
Edris AE, Farrag ES (2003) Antifungal activity of peppermint and sweet basil essential oils and their major aroma constituents on some plant pathogenic fungi from the vapour phase. Nahrung 47:117–121
Garcìa M, Donael OJ, Ardanaz CE, Tonn CE, Sosa ME (2005) Toxic and repellent effects of Baccharis salicifolia essential oil on Tribolium castaneum. Pest Manag Sci 61:612–618
Golshan H, Saber M, Majidi-Shilsar F, Karimi F, Ebadi AA (2014) Laboratory evaluation of Beauveria bassiana isolates on red flour beetle Tribolium castaneum and their characterization by random amplified polymorphic DNA. J Agr Sci Tech 16:747–758
Hirose E, Neves PMOJ, Zequi JAC, Martins LH, Peralta CH, Alcides M Jr (2001) Effect of biofertilizers and neem oil on the entomopathogenic fungi Beauveria bassiana (Bals.) vuill. and Metarhizium anisopliae (Metsch.) sorok. Braz Arch Biol Technol 44(4):419–423
Hokkanen HMT, Kotiluoto R (1992) Bioassay of the side effects of pesticides on Beauveria bassiana and Metarhizium anisopliae: standardized sequential testing procedure. IOBC-WPRS Bull 11(3):148–151
Houghton PJ, Ren Y, Howes M-J (2006) Acetylcholinesterase inhibitors from plants and fungi. Nat Prod Rep 23:181–199
Ibrahim MA, Kainulainen P, Aflatuni A, Tiilikkala K, Holopainen JK (2001) Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to limonene and its suitability for control of insect pests. Agr Food Sci Finland 10:243–259
Ilboudo Z, Dabiré LC, Nébié RC, Dicko IO, Dugravot S, Cortesero AM, Sanon A (2010) Biological activity and persistence of four essential oils towards the main pest of stored cowpeas, Callosobruchus maculates (F.) (Coleoptera: Bruchidae). J Stored Prod Res 46:124–128
Immediato D, Figueredo LA, Iatta R, Camarda A, de Luna RLN, Giangaspero A, Brandão-Filho SP, Otranto D, Cafarchia C (2016) Essential oils and Beauveria bassiana against Dermanyssus gallinae (Acari: Dermanyssidae): towards new natural acaricides. Vet Parasitol 229:159–165
Inouye S, Tsuruoka T, Watanabe M, Takeo K, Akao M, Nishiyama Y, Yamaguchi H (2000) Inhibitory effect of essential oils on apical growth of Aspergillus fumigatus by vapour contact. Mycoses 43:17–23
Islam MS, MahbubHasan M, Xiong W, Zhang SC, Lei CL (2009) Fumigant and repellent activities of essential oil from Coriandrum sativum (L.) (Apiaceae) against red flour beetle Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J Pestic Sci 82:171–177
Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66
Jamali F, Kohanmoo MA, Sohrabi F (2017) Lethal effect of Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch.) Sorokinin against larvae and adults of date sap beetle (Carpophilus hemipterus). J Appl Res Plant protect 6(2):93–105 (in Persian)
Karabörklü S, Ayvaz A, Yilmaz S (2010) Bioactivities of different essential oils against the adults of two stored product insects. Pak J Zool 42(6):679–686
Kavallieratos NG, Athanassiou CG, Michalaki MP, Batta YA, Rigatos HA, Pashalidou FG, Balotis GN, Tomanović Ž, Vayias BJ (2006) Effect of the combined use of Metarhizium anisopliae (Metschinkoff) Sorokin and diatomaceous earth for the control of three stored-product beetle species. Crop Prot 25:1087–1094
Kim D-H, Ahn Y-J (2001) Contact and fumigant activities of constituents of Foeniculum vulgare fruit against three coleopteran stored-product insects. Pest Manag Sci 57:301–306
Kim SI, Chae SH, Youn HS, Yeon SH, Ahn YJ (2011) Contact and fumigant toxicity of plant essential oils and efficacy of spray formulations containing the oils against B- and Q-biotypes of Bemisia tabaci. Pest Manag Sci 67:1093–1099
Khorrami F, Valizadegan O, Forouzan M, Soleymanzade A (2018) The antagonistic/synergistic effects of some medicinal plant essential oils, extracts and powders combined with Diatomaceous earth on red flour beetle, Tribolium castaneum Herbst (Coleoptera: Tenebrionidae). Arch Phytopathol Plant Protect 51(13–14):685–695
Kordali S, Cakir A, Ozer H, Cakmakci R, Kesdek M, Mete E (2008) Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresour Technol 99:8788–8795
Lane BS, Humphreys AM, Thompson K, Trinci APJ (1988) ATP content of stored spores of Paecilomyces farinosus and the use of ATP as a criterion of spore viability. Trans Br Mycol Soc 90:109–148
Lee B-H, Annis PC, Tumaalii F, Choi W-C (2004) Fumigant toxicity of essential oils from the Myrtaceae family and 1,8-cineole against 3 major stored-grain insects. J Stored Prod Res 40:553–564
Liska A, Rozman I, Eded A, Mustac S, Perhoc B (2011) Bioactivity of 1,8-cineol against red four beetle, Tribolium castaneum (Herbst), Pupae. Poljoprivreda 17:58–63
Lu H, Zhou J, Xiong S, Zhao S (2010) Effects of low-intensity microwave radiation on Tribolium castaneum physiological and biochemical characteristics and survival. J Insect Physiol 56:1356–1361
Marcuzzo LL, Eli K (2016) Effect of temperature and photoperiod on the in vitro germination of conidia of Botrytis squamosa, the causal agent of Botrytis leaf blight of onion. Summa Phytopathol 42(3):261–263
Michalaki MP, Athanassiou CG, Steenberg T, Buchelos CTh (2007) Effect of Paecilomyces fumosoroseus (Wise) Brown and Smith (Ascomycota: Hypocreales) alone or in combination with diatomaceous earth against Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) and Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Biol Control 40(2):280–286
Mimica-Dukić N, Kujundžić S, Soković M, Couladis M (2003) Essential oil composition and antifungal activity of Foeniculum vulgare Mill. obtained by different distillation conditions. Phytother Res 17:368–371
Moein MR, Zomorodian K, Pakshir K, Yavari F, Motamedi M, Zarshenas MM (2014) Trachyspermum ammi (L.) Sprague: chemical composition of essential oil and antimicrobial activities of respective fractions. Evid. based complement. Alternat Med 20(1):50–56
Mohamed MIE, Abdelgaleil SAM (2008) Chemical composition and insecticidal potential of essential oils from Egyptian plants against Sitophilus oryzae (L.) (Coleoptera: Curculionidae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Appl Entomol Zool 43(4):599–607
Mohamed MIE, Abdelgaleil SAM, Abdel Rasoul MA (2009) Potential of essential oils to control Sitophilus oryzae (L.) and Tribolium castaneum (Herbst) on stored wheat. ASEG 30(4):419–426
Moore D, Lord JC, Smith SM (2000) Pathogens. In: Subramanyam Bh, Hagstrum DW (eds) Alternatives to pesticides in stored-product IPM. Kluwer Academic Publishers, Dordrecht, pp 193–227
Nana P, Ekesi S, Nchu F, Maniania NK (2016) Compatibility of Metarhizium anisopliae with Calpurnia aurea leaf extracts and virulence against Rhipicephalus pulchellus. J Appl Entomol 140(8):590–597
Nardoni S, Ebani VV, D’Ascenzi C, Pistelli L, Mancianti F (2018) Sensitivity of entomopathogenic fungi and bacteria to plants secondary metabolites, for an alternative control of Rhipicephalus (Boophilus) microplus in cattle. Front Pharmacol 9:937
Nattudurai G, Gabriel Paulraj M, Ignacimuthu S (2012) Fumigant toxicity of volatile synthetic compounds and natural oils against red flour beetle Tribolium castaneum (Herbst) (Coleopetera: Tenebrionidae). JKSUS 24:153–159
Negahban M, Moharramipour S (2007) Fumigant toxicity of Eucalyptus intertexta, Eucalyptus sargentii and Eucalyptus camaldulensis against stored-product beetles. J Appl Ent 131:256–261
Nenaah GE, Ibrahim SIA (2011) Chemical composition and the insecticidal activity of certain plants applied as powders and essential oils against two stored-products coleopteran beetles. J Pest Sci 84(3):393–402
Nikooei M, Moharramipour S (2010) Fumigant toxicity and repellency effects of essential oil of Salvia mirzayanii on Callosobruchus maculatus (Col.: Bruchidae) and Tribolium confusum (Col.: Tenebrionidae). J Entomol Soc Iran 30(2):17–30 (in Persian)
Pandey SK, Upadhyay S, Tripathi AK (2009) Insecticidal and repellent activities of thymol from the essential oil of Trachyspermum ammi (Linn) Sprague seeds against Anopheles stephensi. Parasitol Res 105:507–512
Pant M, Dubey S, Patanjali PK, Naik SN, Sharma S (2014) Insecticidal activity of eucalyptus oil nanoemulsion with karanja and jatropha aqueous filtrates. Int Bioiodeterior Biodegrad 91:119–127
Papachristos DP, Stamopoulos DC (2002) Repellent, toxic and reproduction inhibitory effects of essential oil vapours on Acanthoscelides obtectus (Say) Coleoptera: Bruchidae). J Stored Prod Res 38:117–128
Rajendran S, Sriranjini V (2008) Plant products as fumigants for stored-product insect control. J Stored Prod Res 44:126–135
Regnault-Roger C, Hamraoui A (1995) Fumigant toxic activity and reproductive inhibition induced by monoterpenes on Acanthoscelides obtectus (Say) (Coleoptera), a bruchid of kidney bean (Phaseolus vulgaris L). J Stored Prod Res 31:291–299
Safaei-Ghomi J, Ahd AA (2010) Antimicrobial and antifungal properties of the essential oil and methanol extracts of Eucalyptus largiflorens and Eucalyptus intertexta. Parmacogn mag 6(23):172–175
Saroukolai AT, Moharramipour S, Meshkatalsadat MH (2010) Insecticidal properties of Thymus persicus essential oil against Tribolium castaneum and Sitophilus oryzae. J Pest Sci 83:3–8
SAS Institute (2003) The SAS system for windows, Release 9.0. SAS, Institute, Cary, NC
Shafighi Y, Ziaee M, Ghosta Y (2014) Diatomaceous earth used against insect pests, applied alone or in combination with Metarhizium anisopliae and Beauveria bassiana. J Plant Prot Res 54(1):62–66
Siddique S, Parveen Z, Bareen F, Butt A, Chaudhary MN, Akram M (2017) Chemical composition and insecticidal activities of essential oils of Myrtaceae against Tribolium castaneum (Coleoptera: Tenebrionidae). Pol J Environ Stud 26(4):1653–1662
Singh G, Maurya S, Catalan C, De Lampasona MP (2004) Chemical constituents, antifungal and antioxidative effects of ajwain essential oil and its acetone extract. J Agric Food Chem 52:3292–3296
Sohrabi F, Jamali F, Morammazi S, Saber M, Kamita SG (2019) Evaluation of the compatibility of entomopathogenic fungi and two botanical insecticides tondexir and palizin for controlling Galleria mellonella L. (Lepidoptera: Pyralidae). Crop Prot 117:20–25
Sohrabi F, Kohanmoo MA (2017) Fumigant Toxicity of plant essential oils against Oligonychus afrasiaticus (MCG) (Acari: Tetranychidae) and identification of their chemical composition. J Essent Oil Bear Pl 20(11):1–7
Sohrabi F, Kohanmoo MA, Jamali F (2015) Fumigant toxicity of five medicinal plant essential oils against the date sap beetle, Carpophilus hemipterus (Linnaeus) and identification of their chemical composition. Plant Prot 39(3):13–26 (in Persian)
Soylu EM, Soylu S, Kurt Ş (2006) Antimicrobial activities of the essential oils of various plants against tomato late blight disease agent Phytophthora infestans. Mycopathologia 161:119–128
Soylu EM, Tok FM, Soylu S, Kaya AD, Evrendilek GA (2005) Antifungal activities of the essential oils on post-harvest disease agent Penicillium digitatum. Pak J Biol Sci 8:25–29
Soylu S, Yigitbas H, Kurt Ş (2007) Antifungal effects of essential oils from oregano and fennel on Sclerotinia sclerotiorum. J Appl Microbiol 103:1021–1030
Stefanazzi N, Stadler T, Ferrero A (2011) Composition and toxic, repellent and feeding deterrent activity of essential oils against the stored-grain pests Tribolium castaneum (Coleoptera: Tenebrionidae) and Sitophilus oryzae (Coleoptera: Curculionidae). Pest Manag Sci 67:639–646
Storm C, Scoates F, Nunn A, Potin O, Dillon A (2016) Improving efficacy of Beauveria bassiana against stored grain beetles with a synergistic co- formulant. Insects 7(3):42
Taghizadeh-Saroukolai A, Moharramipour S, Meshkatalsadat MH (2010) Insecticidal properties of Thymus persicus essential oil against Tribolium castaneum and Sitophilus oryzae. J Pest Sci 83:3–8
Wakil W, Ghazanfar MU, Yasin M (2014) Naturally occurring entomopathogenic fungi infecting stored grain insect species in Punjab. Pakistan J Insect Sci 14:182
Watts M, Williamson S (2015) Replacing chemicals with biology: phasing out highly hazardous pesticides with agroecology. PAN International, Fremont
Acknowledgements
The authors gratefully acknowledge Dr. Shizuo George Kamita for help with scientific editing and the college of Agriculture and Natural resources, Persian Gulf University, Bushehr, Iran, for the support in conducting the current study. The authors also acknowledge Dr. Youbert Ghosta (University of Urmia, Iran) for supplying fungal isolates.
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Jamali, F., Sohrabi, F. & Kohanmoo, M.A. Entomopathogenic fungi and plant essential oils are not compatible in controlling Tribolium castaneum (Herbst). J Plant Dis Prot 128, 799–808 (2021). https://doi.org/10.1007/s41348-021-00430-5
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DOI: https://doi.org/10.1007/s41348-021-00430-5