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Biological Activity of Bacillus Spp. Evaluated on Eggs and Larvae of Red Palm Weevil Rhynchophorus Ferrugineus

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Biological Activity of Bacillus Spp. Evaluated on Eggs and Larvae of Red Palm Weevil Rhynchophorus Ferrugineus View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Archivio istituzionale della ricerca - Università di Palermo Ann Microbiol (2015) 65:477–485 DOI 10.1007/s13213-014-0881-4 ORIGINAL ARTICLE Biological activity of Bacillus spp. evaluated on eggs and larvae of red palm weevil Rhynchophorus ferrugineus Nicola Francesca & Antonio Alfonzo & Gabriella Lo Verde & Luca Settanni & Milko Sinacori & Paolo Lucido & Giancarlo Moschetti Received: 4 November 2013 /Accepted: 18 March 2014 /Published online: 5 April 2014 # Springer-Verlag Berlin Heidelberg and the University of Milan 2014 Abstract This study was conducted to characterize the Introduction Bacillus populations associated with dead Rhynchophorus ferrugineus, to develop a biological control for the red palm The red palm weevil Rhynchophorus ferrugineus (Coleoptera: weevil. Dead adult beetles, collected throughout Sicily, were Curculionidae), which is native to Asia and Melanesia, feeds used for isolating internal and external spore forming bacteria on many species of palm trees and represents the most com- (SFB) microbiota. The isolates, preliminarily allotted to the mon insect on this host. R. ferrugineus lives in regions with Bacillaceae family, were tested at four concentrations (103 to temperate climates (Murphy and Briscoe 1999) where palm 106 CFU/mL) for their ability to inhibit hatching of eggs of trees are common. Since the end of the second millennium, the R. ferrugineus and were used at 106 CFU/mL to monitor their presence of red palm weevil has been also documented in insecticidal activity against 10-day-old larvae. Total amounts Egypt, Israel, Jordan and Palestine (Kehat 1999). The red of SFB measured outside the skeleton and in the inners part of palm weevil was first found in Europe in 1993, when the the beetles were 5.59–6.94 and 5.17–7.05 Log CFU/g, respec- weevil was detected in Spain in the palms of the genus tively. Hatching was markedly inhibited by nine isolates, Phoenix from Egypt (Barranco et al. 1996). Currently, the representing nine distinct strains of seven species (Bacillus weevil has, colonized the entire Mediterranean Basin, from amyloliquefaciens, Bacillus cereus, Bacillus licheniformis, Morocco to Turkey (EPPO 2007a, 2009). In Italy, the red Bacillus megaterium, Bacillus pumilus, Bacillus subtilis,and palm weevil was found for the first time in a nursery in Lysinibacillus sphaericus), especially by the strains Pistoia (Tuscany) in 2004 (Sacchetti et al. 2005, 2006), B. pumilus GC43 and GC51, which exhibited lethal concen- after which, the weevil has also been detected in Sicily trations 50 (LC50) values of 1.60×103 and 9.84×103 CFU/ (Longo and Tamburino 2005), Campania (Anonimo 2005), mL, respectively. Among all the strains tested, only Latium, Apulia and Sardinia (EPPO 2007b). Over the past B. licheniformis CG62 exhibited significant insecticidal activ- 5 years, several palms belonging to the species Phoenix ity against red palm weevil larvae. The Bacillus isolates char- canariensis, which is spread across the Canary Islands and acterized and tested in this study inhibited the hatching of red many regions of southern Italy (especially Sicily), were palm weevils in a contact-dependent manner. Thus, these infested by the weevil and were destroyed to limit the isolates can be used as a preventive rather than as a curative disproportionate spread of the insect. From 1995 to 2010, treatment. infestation by the weevil destroyed almost 40,000 palms in Italy (Lo Verde et al. 2011). The weevil has spread rapidly throughout Sicily because of the numerous nurseries pres- Keywords Bacillus . Rhynchophorus ferrugineus . Hatching ent in the region, and, especially because of the inade- assays . Larvae . Palm quate phytosanitary inspections preformed on imported plants. Furthermore, control measures applied on infested : : : : : plants were poorly timed, which led to a massive increase N. Francesca A. Alfonzo G. Lo Verde L. Settanni M. Sinacori in red palm weevil populations and made managing their : * P. Lucido G. Moschetti ( ) infestation challenging. Department of Agricultural and Forest Science, Università degli Studi di Palermo, Viale delle Scienze 4, 90128 Palermo, Italy Palms are an integral part of the Mediterranean landscape e-mail: [email protected] and they are key components of the nurseries. Insects that 478 Ann Microbiol (2015) 65:477–485 infect palms in nurseries are controlled mainly by the Table 1 Description of the samples of red palm weevil and spore- application of systemic insecticides. The red palm weevil forming bacteria concentration can be monitored using pheromone-containing lure buckets Site (Sicily, Italy) Samples Spore-forming bacteria or pitfall traps, and the weevil can be controlled using concentration* field sanitation and mass trapping methods with traps Exogenous Log Endogenous Log baited with pheromone and plant-derived semiochemicals (CFU/g) (CFU/g) ((4S, 5S)-4-methyl-5-nonanol) (El-Shafie et al. 2011). Several research programs have also been initiated for Agrigento 1 to 10 6.78±1.45 aB 7.05±1.56aB studying the biological control of R. ferrugineus. Catania 11 to 20 6.49±0.88 aB 6.60±0.91aB Specifically, two entomopathogenic fungi Metarhizium Cinisi (PA) 21 to 30 6.34±0.46 aB 6.43±0.51aB anisopliae and Beauveria bassiana, have been detected Marsala (TP) 31 to 40 6.37±0.57 aB 6.20±0.68aB on the red palm weevil and tested under laboratory and Mazara del Vallo (TP) 41 to 50 6.94±0.78 aB 6.59±0.38aB field conditions (Deadman et al. 2001;Gindinetal.2006; Messina 51 to 60 6.71±0.82 aB 6.81±0.63aB El Sufti et al. 2007; 2009; 2011;Sewifyetal.2009; Torta Palermo 61 to 70 5.59±1.21 aA 5.17±1.20aA et al. 2009; Vitale et al. 2009; Dembilio et al. 2010; Ragusa 71 to 80 6.79±0.32 aB 6.63±0.37aB Güerri-Aguilló et al. 2010; 2011; Merghem 2011; Terrasini (PA) 81 to 90 6.49±0.58 aB 6.19±0.80aB Francardi et al. 2012). Red weevil infestation is also Villagrazia di Carini (PA) 91 to 100 6.50±0.53 aB 6.61±0.42aB tackled using microbiological approaches. Members of * the Bacillus genus are key antagonistic agents of phytoph- Mean values are shown ± SD (standard deviation) agous insects (Salama et al. 2004), and several species of The statistical significances at P values of <0.05 are indicated by lower- this genus are routinely used in the biological control of case (a, b) and uppercase (A, B) letters between the lines and the columns, respectively beetles; the species are remarkably specific in targeting dis- tinct stages of the insect’slifecycle.Bacillus thuringiensis, B. popilliae, B. lentimorbus and B. sphaericus synthesize were used: the insects were removed from flasks and proteins with insecticidal activity (Bulla et al. 1975). immersed in ethanol (100 % w/v) and then their sur- Based on these findings, we isolated and character- faces were sterilized using a Bunsen burner (Khiyami ized bacteria of the Bacillaceae family from dead adults and Alyamani 2008). Thereafter, the samples were trans- red palm weevils and conducted preliminary tests to ferred to sterile bags containing sterile Ringer’ssolution measure the capacity of these bacteria to inhibit the and homogenized using a stomacher (BagMixer® 400, hatching of R. ferrugineus eggs and to kill weevil Interscience, Saint Nom, France) at the highest speed larvae. setting until the exoskeleton dissolved completely. All cell suspensions were heated at 85 °C for 15 min and then diluted serially (1:10) in Ringer’s solution; 0.1 mL Materials and methods aliquots of the cell suspensions were spread on plates of Nutrient Agar (NA) (Oxoid, Basingstoke, UK) and in- Sampling cubated at 32 °C for 48 h. The analysis was performed in duplicate. Furthermore, isolation tests were performed From each sampling area (Table 1), ten dead adult weevils on PDA (Potato dextrose agar, Oxoid) at 27 °C for with no detectable signs of fungal infection were collected 2 weeks to confirm the absence of entomopathogenic from palms growing in urban green areas of Sicily affected by fungi. R. ferrugineus. The sampling period lasted from 21 November 2007 to 4 March 2008. The beetles were stored individually in sterile plastic containers (100 mL) at 18 °C until being used Isolation and identification of spore-forming bacteria (SFB) for isolating bacteria. Based on the different appearance (shape, color, edge and Microbiological analysis elevation), colonies were picked randomly from count plates, transferred to the corresponding broth media and purified by From the collected beetles, exogenous and endogenous repeated sub-culturing. Gram staining was performed as re- spore-forming bacteria (SFB) were isolated. Exogenous ported by Gregersen (1978), and catalase test was determined SFB were obtained by placing the insects in sterile flasks by transferring fresh colonies from a Petri dish to a glass slide containing sterile Ringer’s solution (Sigma-Aldrich, Milan, and adding 5 % H2O2 (v/v). The SFB were identified accord- Italy) at a final ratio of 1:10 (w/v) and shaking for 10 min ing to the method of Gordon (1974) and stored in glycerol at 150 rpm. To isolate endogenous SFB, the same beetles stocks at −80 °C until analysis. Ann Microbiol (2015) 65:477–485 479 Bioassays on eggs and larvae Sinacori et al. (2014). DNA was extracted using InstaGeneTM Matrix (Bio-Rad Laboratories, Hercules, CA) Eggs of R. ferrugineus were obtained from adults reared in the according to the supplier’s recommendations. All isolates laboratory of the Department Agricultural and Forest Science, were also analyzed using repetitive DNA element-PCR (rep- University of Palermo. Newly hatched adults (5–10), both PCR) with the (GTG)5 and BOXA1R primer sets (Versalovic females and males, were placed in rearing boxes and provided et al.
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