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Effects of Combining an Entomopathogenic Fungi Or Bacterium with Entomopathogenic Nematodes on Mortality of Curculio Caryae

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Effects of Combining an Entomopathogenic Fungi Or Bacterium with Entomopathogenic Nematodes on Mortality of Curculio Caryae Biological Control 30 (2004) 119–126 www.elsevier.com/locate/ybcon Effects of combining an entomopathogenic fungi or bacterium with entomopathogenic nematodes on mortality of Curculio caryae (Coleoptera: Curculionidae) David I. Shapiro-Ilan,a,* Mark Jackson,b Charles C. Reilly,a and Michael W. Hotchkissa a USDA-ARS, SE Fruit and Tree Nut Research Lab, 21 Dunbar Road, Byron, GA 31008, USA b USDA-ARS-NCAUR 1815 N. University St. Peoria, IL 61604, USA Received 10 July 2003; accepted 25 September 2003 Abstract Our objective was to determine the effects of combining entomopathogenic nematodes with other entomopathogens on their ability to suppress larvae of the pecan weevil, Curculio caryae. In laboratory assays, we simultaneously applied the nematodes Heterorhabditis indica or Steinernema carpocapsae with the fungus Beauveria bassiana, Metarhizium anisopliae,orPaecilomyces fumosoroseus, or the bacterium Serratia marcescens. Mortality of C. caryae was determined 14 days after application. We observed antagonism in all pathogen combinations, except H. indica combined with M. anisopliae, for which additive effects were observed. The combination of H. indica and M. anisopliae may merit further study in other systems. Depending on application rate, S. carpocapsae combined with B. bassiana or S. marcescens also resulted in additivity. S. carpocapsae (applied alone) generally caused greater C. caryae mortality than other pathogens applied alone. P. fumosoroseus and S. marcescens were not pathogenic to C. caryae when applied alone. We conclude that the pathogen combinations we investigated are not likely to improve suppression of C. caryae larvae beyond what is expected from single application of the pathogen with greatest virulence. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Additivity; Antagonism; Beauveria bassiana; Heterorhabditis indica; Paecilomyces fumosoroseus; Pathogen combinations; Serratia marcescens; Steinernema carpocapsae 1. Introduction additional year in the soil as larvae and emerge as adults in the third year (Harris, 1985). The pecan weevil, Curculio caryae (Horn), is a key Control recommendations for C. caryae currently pest of pecan throughout the Southeastern US as well as consist of foliar applications of chemical insecticides in portions of Texas and Oklahoma (Payne and Dut- (e.g., carbaryl) to kill the adults (Harris, 1999). Due to cher, 1985). This insect has a 2- or 3-year life cycle the problems associated with aphid resurgence (Dutcher (Harris, 1985). Adults emerge from soil in late July- and Payne, 1985), as well as other environmental and August and feed on and oviposit in nuts (Harris, 1985). regulatory concerns, research toward developing alter- Larvae develop within the nut and fourth instars drop to native control strategies is warranted. Entomopatho- the ground where they burrow to a depth of 8–25 cm, genic nematodes, which occur naturally as pathogens of form a soil cell, and overwinter. The following year, C. caryae (Nyczepir et al., 1992), are one of the potential approximately 90% of the larvae pupate and spend the alternatives (Shapiro-Ilan, 2003). next 9 months in the soil cell as adults (Harris, 1985). Entomopathogenic nematodes are obligate parasites The remaining 10% of the larval population spend an in the families Steinernematidae and Heterorhabditidae. Entomopathogenic nematodes kill insects with the aid of a mutualistic bacterium, which is carried in their intes- * Corresponding author. Fax: 1-478-956-2929. tine (Xenorhabdus spp. and Photorhabdus spp. are as- E-mail address: [email protected] (D.I. Shapiro-Ilan). sociated with Steinernema spp. and Heterorhabditis spp., 1049-9644/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2003.09.014 120 D.I. Shapiro-Ilan et al. / Biological Control 30 (2004) 119–126 respectively) (Poinar, 1990). The nematodes complete 2– microbial control agents for C. caryae suppression 3 generations within the host, after which free-living (Shapiro-Ilan, 2003). infective juveniles emerge to seek new hosts (Poinar, The primary objective of this study was to determine 1990). Entomopathogenic nematodes are effective at whether applications of entomopathogenic fungi or a controlling a variety of economically important pests bacterium combined with entomopathogenic nematodes including the larvae of several weevil species (Coleop- results in a synergistic, additive, or antagonistic effect on tera: Curculionidae) such as the black vine weevil, Oti- C. caryae larvae. It was also of interest to compare the orhynchus sulcatus (F.), and the Diaprepes root weevil, relative virulence of each of the entomopathogens acting Diaprepes abbreviatus (L.) (Shapiro-Ilan et al., 2002). alone and determine which treatments caused greater One approach to controlling C. caryae with ento- mortality than a non-treated control. The entomopath- mopathogenic nematodes would be to target the larvae ogens tested were B. bassiana, M. anisopliae, Paecilo- when they drop to the ground or after burrowing into myces fumosoroseus (Wize), and S. marcescens combined the soil. Prior research, however, does not indicate great with Heterorhabditis indica Poinar, Karunakar, & David potential for entomopathogenic nematodes to control or S. carpocapsae. the larval stage of C. caryae (Nyczepir et al., 1992; Shapiro-Ilan, 2001a; Smith et al., 1993). Field trials to suppress C. caryae larvae with H. bacteriophora (Po- 2. Materials and methods inar), Steinernema carpocapsae (Weiser), or Steinernema feltiae (Filipjev) resulted in less than 35% control (Ny- 2.1. Insects and pathogens czepir et al., 1992; Smith et al., 1993). Furthermore, in a laboratory study, Shapiro-Ilan (2001a) found the viru- Nematodes, H. indica (Hom1 strain) and S. carpo- lence of 15 strains from nine species of entomopatho- capsae (All strain), originally obtained from Integrated genic nematodes to be relatively poor to C. caryae larvae Biocontrol Systems (Aurora, IN) and K. Nguyen (none of the nematodes produced greater than 60% (University of Florida), respectively, were cultured in mortality when applied at ca. 40 infective juveniles/cm2). the last instar of Galleria mellonella (L.) according to Conceivably, combining entomopathogenic nema- procedures described by Kaya and Stock (1997). The todes with other entomopathogens would result in syn- two nematode species were chosen because each has ergistic interactions that would enhance the potential for shown at least some promise for C. caryae control rel- biological control of C. caryae. In studies targeting ative to other species (Shapiro-Ilan, 2001a,b; Shapiro- other insect pests, synergistic interactions have been Ilan et al., 2003). Entomopathogenic fungi, B. bassiana observed from certain combinations of entomopatho- (BbGA2) and M. anisopliae (MaLA4), were collected genic nematodes with other pathogens. For example, from soil in pecan orchards in Byron, Georgia and synergistic virulence to Cyclocephala spp. was observed Dixie, Louisiana, respectively (Shapiro-Ilan et al., 2003), in combinations of entomopathogenic nematodes with and reproduced on SabouraudÕs dextrose agar (Becton Paenibacillus popilliae (Dutky) (Thurston et al., 1993, Dickson, Sparks, MD, USA) with yeast extract (Sigma 1994) or with Bacillus thuringiensis Berliner subspecies Chemical, St. Louis, MO, USA) according to Goettel japonensis (Koppenhofer€ and Kaya, 1997; Koppenhofer€ and Inglis (1997); these strains were chosen because they et al., 1999). However, interactions between entomo- previously exhibited relatively high virulence to C. car- pathogenic nematodes and other entomopathogens can yae larvae compared with other strains in laboratory also be antagonistic (Baur et al., 1998; Brinkman and assays (Shapiro-Ilan et al., 2003). P. fumosoroseus Gardner, 2000; Koppenhofer€ and Kaya, 1997). (ARSEF 3581), was originally isolated from an infected In addition to entomopathogenic nematodes, several silverleaf whitefly (Bemisia argentifolii Bellows and other entomopathogens have been reported to occur Perring); blastospores were produced through deep-tank naturally in C. caryae including the entomopathogenic fermentation in a basal salts medium containing 2.5% fungi Beauveria bassiana (Balsamo) Vuillemin and acid hydrolyzed casein and 5% glucose and subsequent Metarhizium anisopliae (Metschnikoff) Sorokin (Sri- air-drying (Jackson et al., 2003). The S. marcescens Arunotai et al., 1975; Swingle and Seal, 1931), and isolate was obtained on potato dextrose agar from the Paecilomyces sp. (Sikorowski, 1985), and the bacterium surface of an adult pecan weevil (captured on a pecan Serratia marcescens Bizio (Sri-Arunotai et al., 1975). tree trunk in Byron, GA, identified by Bacterial Strain- Field trials with B. bassiana and M. anisopliae caused Identification and Mutant Analysis Service (BSI-MSA, significant reductions in C. caryae larval populations, Auburn University, AL) and cultured in nutrient broth but the levels of control were generally low (e.g., <35%) (Becton Dickson) (Klein, 1997). Nematodes were stored (Gottwald and Tedders, 1983; Harrison et al., 1993; at 13 °C (Kaya and Stock, 1997) and the other patho- Shapiro-Ilan, 2003). Beyond entomopathogenic nema- gens at 4 °C (Goettel and Inglis, 1997; Klein, 1997) prior todes, B. bassiana and M. anisopliae, no other pathogens to use in experiments; pathogens were not sub-cultured that naturally occur in C. caryae have been tested as more than once during the study. D.I. Shapiro-Ilan et al. / Biological Control 30 (2004)
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