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Beauveria Bassiana, Metarhizium Anisopliae</I>, and <I>Isaria Fumo

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Beauveria Bassiana, Metarhizium Anisopliae</I>, and <I>Isaria Fumo 87 Journal of Food Protection, Vol. 77, No. 1, 2014, Pages 87–93 doi:10.4315/0362-028X.JFP-13-196 Copyright G, International Association for Food Protection Evaluation of the Entomopathogenic Fungi Beauveria bassiana, Metarhizium anisopliae, and Isaria fumosorosea for Control of Sitophilus oryzae NICKOLAS G. KAVALLIERATOS,1* CHRISTOS G. ATHANASSIOU,2 MARIA M. AOUNTALA,1 AND DEMETRIUS C. KONTODIMAS1 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/77/1/87/1683291/0362-028x_jfp-13-196.pdf by guest on 01 October 2021 1Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute, 8 Stefanou Delta Street, 14561, Kifissia, Attica, Greece; and 2Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, Phytokou Street, Nea Ionia, 38446, Magnissia, Greece MS 13-196: Received 11 May 2013/Accepted 1 July 2013 ABSTRACT The entomopathogenic fungi Beauveria bassiana, Metarhizium anisopliae, and Isaria fumosorosea were tested against the stored-grain pest Sitophilus oryzae. The fungi were isolated from the soil (from three locations in Attica, Greece: B. bassiana from Tatoion, M. anisopliae from Marathon, and I. fumosorosea from Aghios Stefanos) using larvae of Galleria mellonella as bait. Suspensions of 2.11 | 107 and 2.11 | 108, 1.77 | 107 and 1.77 | 108, and 1.81 | 107 and 1.81 | 108 conidia per ml of B. bassiana, M. anisopliae, and I. fumosorosea, respectively, were applied by three treatments: (i) sprayed on food and set in petri dishes with adults of S. oryzae, (ii) sprayed on adults of S. oryzae and set in petri dishes without food, and (iii) sprayed on adults of S. oryzae and set in petri dishes with food. The observed mortality of S. oryzae adults during the overall exposure period for the lowest, as well as for the highest, concentrations of B. bassiana, M. anisopliae, and I. fumosorosea ranged from 0 to 100%. Concentration was, in most of the cases tested, a critical parameter that determined the ‘‘speed of kill’’ of the exposed insect species for B. bassiana and M. anisopliae. Conversely, concentration was not that critical for I. fumosorosea, and survival was high in some of the combinations tested, even after 14 days of exposure. Both in the highest and the lowest concentrations of fungi, the mortality of S. oryzae adults was higher when the fungi were applied on adults than when they were applied on food. Higher mortality was observed when food was absent than when food was present, in most of the cases tested. The high efficacy levels recorded in the current study indicate that the tested fungi could be effective biocontrol agents against S. oryzae. Alternatives to synthetic insecticides have been sought are environmentally safe, and they infect the insects by in response to the development of insecticide resistance and contact. Entomopathogenic fungi penetrate the cuticle, the concerns about consumer health and environmental safety; insect dies, and then the fungi are recycled in the cadavers, biological control is one of the methods that have been thus returning more inoculum to the stored-product system developed. Agents for biological control of stored-product (10, 24, 29, 30). Previous studies have examined the insect pests include hymenopterous parasitoids, predaceous potential of entomopathogenic fungi against stored-product insects or mites, and insect pathogens, such as entomo- insects, with promising results. Searle and Doberski (27) pathogenic fungi, bacteria, viruses, protozoa, and nematodes reported complete mortality of Oryzaephilus surinamensis (13, 24). The use of natural enemies and insect pathogens is (L.) (Coleoptera: Silvanidae) adults exposed to Beauveria considered compatible when biological control strategies in bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) stored facilities are followed. Yet insect pathogens can be conidiospores at concentrations from 104 to 106 spores per stored for a longer time than can the beneficial insects, and ml after 26 days of exposure in wheat. Rice and Cogburn they infest a wide range of insect pest species in contrast to (25) investigated B. bassiana against adults of Sitophilus beneficial insects, which are host-specific. Generally, the oryzae (L.) (Coleoptera: Curculionidae), Rhyzopertha do- presence of insects in cereals, even if they are there as minica (F.) (Coleoptera: Bostrychidae), and Tribolium biological control agents, is considered contamination, castaneum (Herbst) (Coleoptera: Tenebrionidae) on three making the products unacceptable for consumption (13, types of substrates and recorded 80 to 100% mortality at the 24). Among insect pathogens, entomopathogenic fungi are highest concentrations. Ekesi et al. (12) found that B. promising alternatives to chemical insecticides (17, 24): bassiana, Metarhizium anisopliae (Metschnikoff) Sorokin they have low mammalian toxicity, they exist naturally and (Ascomycota: Hypocreales), and Nomuraea rileyi (Farlow) Sampson (Ascomycota: Hypocreales) caused 48 to 96%,89 * Author for correspondence. Tel: z30-2108180215; Fax: z30-2108077506; to 100%, and 33 to 95% mortality, respectively, of E-mail: [email protected]. Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae) 88 KAVALLIERATOS ET AL. J. Food Prot., Vol. 77, No. 1 adults in sorghum 7 days after exposure. Lord (20) found 95 tested commodity was 11.3% (mini GAC plus moisture tester, to 97% reduction in progeny of R. dominica adults in wheat Dickey-John Europe S.A.S., Colombes, France) at the beginning of treated with 200 mg of conidia of B. bassiana per kg at 43% the tests. relative humidity. Insects. The S. oryzae adults used in the tests were taken from a Various application methods have been used to test the culture that was kept in the Laboratory of Agricultural Entomology effectiveness of entomopathogenic fungi as grain protec- (Benaki Phytopathological Institute, Attica, Greece) under continuous tants. For example, Searle and Doberski (27) mixed B. darkness on whole hard wheat at 27uCand65% relative humidity. All bassiana conidiospores with food that had been infected by individuals used in the experiments were ,2 weeks old. O. surinamensis. Hluchy´ and Samsˇinˇa´kova´ (15) sprayed Sitophilus granarius (L.) (Coleoptera: Curculionidae) adults Fungal isolates. The B. bassiana, M. anisopliae, and I. with 1 ml of conidial suspensions of B. bassiana in dishes, fumosorosea isolates used in the tests were obtained from the left them for 2 h, and then added food to the dishes. Adane collection of entomopathogenic fungi of Benaki Phytopathological et al. (1) sprayed Sitophilus zeamais Motschulsky (Coleop- Institute and were first isolated from soil samples from Tatoion, tera: Curculionidae) adults with 1 ml of conidial suspension Marathon, and Aghios Stefanos (Attica, Greece), respectively, using Downloaded from http://meridian.allenpress.com/jfp/article-pdf/77/1/87/1683291/0362-028x_jfp-13-196.pdf by guest on 01 October 2021 of B. bassiana, left them without food for 1 day, and then larvae of Galleria mellonella (L.) (Lepidoptera: Pyralidae) as bait gave them access to a food source. Moino et al. (23) (34). Fungi were initially grown on half-strength Sabouraud dextrose agar at 25 C for 15 days. Then the plates were removed exposed adults of R. dominica, S. oryzae, and S. zeamais for u and preserved at 4uC. Before each test, the isolates were subcultured 1 min to the surface of sporulating B. bassiana culture. on Sabouraud dextrose agar (10 petri dishes each) and were placed in Then, either they transferred them to food, or they placed incubators at 25uC for 12 days in continuous darkness. the adults inside tubes that contained conidia of the fungus, shook them all together, and then transferred them to food. Conidial suspensions. Conidia were harvested by scraping Dal Bello et al. (11) sprayed S. oryzae adults with 1 ml of the surface of the petri dishes with a sterilized scalpel and flooding conidial suspension of B. bassiana, M. anisopliae, Isaria the dishes with a sterile liquid solution of 0.1% Tween 80 (20 ml farinosa (Holmskjold) Fries (~Paecilomyces farinosus per plate). The conidial suspensions were stirred using a magnetic (Holmskjold) Brown and Smith), and Lecanicillium lecanii stirrer (Heidolph MR 3001, Heidolph Instruments GmbH and Co. Zare and Gams (Ascomycota: Eurotiales) (~Verticillium KG, Schwabach, Germany) and filtered twice using a sterile nylon lecanii (Zimmermann)), left them for 1 day without food, and membrane. The concentration of fungal conidia in the conidial then transferred them to food. Kassa et al. (16) dipped S. suspension was determined using a hemocytometer (Precicolor, HBG, Giessen-Luetzellinden, Germany). Standard first concentra- zeamais and Prostephanus truncatus (Horn) (Coleoptera: tions of B. bassiana, M. anisopliae, and I. fumosorosea of 2.11 | Bostrychidae) adults for 5 s in 1 ml of B. bassiana, M. 8 8 8 10 , 1.77 | 10 , and 1.81 | 10 conidia per ml were prepared, anisopliae, and Isaria sp. conidial suspensions, left them respectively. Then, dilutions were prepared by adding 5 ml of the without food for 1 day, and then transferred the individuals to suspensions to 45 ml of sterile water, providing final concentra- food. Batta (7) estimated the efficacy of M. anisopliae against tions of 2.11 | 107, 1.77 | 107, and 1.81 | 107 conidia per ml adults of R. dominica by applying the fungus as dry (conidia for B. bassiana, M. anisopliae, and I. fumosorosea, respectively. powder) or liquid (conidial suspension in sterile water, Conidia viability was 98.4, 97.1, and 97.5% for B. bassiana, M. conidia in invert emulsion) formulations on the bottom of anisopliae, and I. fumosorosea, respectively. plastic boxes: food was included inside the boxes and adults were added later, or adults were given access to food and Bioassays. The conidial suspensions of fungi were applied by fungus was applied later. Wakefield et al. (32) tested oil-, three treatments: (i) they were sprayed on food (wheat), which was powder-, and water-based formulations of B. bassiana then placed in petri dishes with adults of S. oryzae; (ii) they were sprayed on adults of S.
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