STORED-PRODUCT Survival of Stored-Product Insect Natural Enemies in Spinosad-Treated Wheat 1 MICHAEL D. TOEWS AND BHADRIRAJU SUBRAMANYAM Department of Grain Science and Industry, Kansas State University, Manhattan, KS 66506 J. Econ. Entomol. 97(3): 1174Ð1180 (2004) ABSTRACT The survival of stored product insect natural enemies in wheat treated with spinosad was investigated in laboratory and pilot scale experiments. The predator Xylocoris flavipes (Reuter), the warehouse pirate bug, and the parasitoids Habrobracon hebetor (Say), Theocolax elegans (West- wood), and Anisopteromalus calandrae (Howard) were exposed to wheat treated with aliquots of water or spinosad at 0.05Ð1 mg ([AI])/kg. X. flavipes was the only species that survived (92% survival) in spinosad-treated wheat at 1 mg/kg. X. flavipes suppressed populations of immature Tribolium casta- neum (Herbst), the red ßour beetle, by nearly 90% compared with a water-treated control, but 100% suppression of immatures was achieved in wheat receiving spinosad or spinosad ϩ X. flavipes treatments. A 3-mo pilot scale experiment to evaluate T. castaneum suppression in drums holding 163.3 kg of wheat showed that the pest populations increased throughout the study in the control treatment, but peaked after 1 mo in the X. flavipes-treated drums. By comparison, better T. castaneum population suppression was achieved in spinosad or spinosad ϩ X. flavipes treatments. Although X. flavipes can survive and reproduce in spinosad-treated wheat, under our test conditions spinosad alone provided adequate suppression of T. castaneum populations in stored wheat. KEY WORDS Saccharopolyspora spinosa, stored-product insects, biological control, natural enemies SPINOSAD, A COMMERCIAL PESTICIDE based on the fermen- vergens Gue´rin-Me´neville (Coleoptera: Coccinelli- tation products of the bacterium Saccharopolyspora dae); phytoseid mite, Phytoseiulus persimilis Athias spinosa Mertz & Yao, is efÞcacious against several Henriot (Acari: Phytoseiidae); and common green insects associated withstored grain in laboratory lacewing, Chrysoperla plorabunda (Fitch) (Neurop- (Fang et al. 2002a, Toews and Subramanyam 2003) and tera: Chrysopidae). Boucher (1999) reported that spi- Þeld evaluations (Fang et al. 2002b). Spinosad is cur- nosad applied to bell peppers effectively controlled rently labeled for use on vegetable crops, ornamentals, the pepper maggot, Zonosemata electa (Say) (Diptera: and forest trees (Thompson et al. 2000), but not on Tephritidae), but it did not reduce populations of stored grain. In May 2002, an experimental use permit beneÞcial arthropods, including unspeciÞed species of for use on grain at 1 mg([AI])/kg was approved by the Coccinellidae, Chrysopidae, Cecidomyiidae, Syrphi- U.S. Environmental Protection Agency (EPA Exper- dae, Nabidae, and hymenopteran-parasitized Aphidi- imental Use Permit No. 62719-EUP-50) that facilitated dae. Mason et al. (2002) found that spinosad was toxic full-scale Þeld trials withthispesticide on farms in to the parasitoids Trichogramma inyoense Pinto & Oat- Kansas and other states. man (Hymenoptera: Trichogrammatidae) and Micro- The compatibility of low rates of spinosad with plitis mediator Haliday (Hymenoptera: Braconidae). parasitoids of stored product insect pests is unknown. Bret et al. (1997) reported that spinosad was much less In the present investigation, we evaluated the sus- toxic to beneÞcial insects in Þeld crops than synthetic ceptibility of several parasitoids and a predator of pesticides. Schoonover and Larson (1995) reported stored product insect pests to spinosad-treated wheat that spinosad was practically nontoxic to the insidious in the presence and absence of hosts or prey. Addi- ßower bug, Orius insidiosus (Say) (Heteroptera: An- tionally, we determined the effectiveness of spinosad thocoridae); convergent lady beetle, Hippodamia con- in combination witha predator to suppress thered ßour beetle, Tribolium castaneum (Herbst) (Co- This paper reports research results only. Mention of a proprietary leoptera: Tenebrionidae), in hard red winter wheat product name does not constitute an endorsement for its use by stored in 208-liter plastic drums. T. castaneum was used Kansas State University or the United States Department of Agricul- in experiments because the adults are relatively less ture. susceptible than other stored-product insect species 1 Current address: USDAÐARS, Grain Marketing and Production ResearchCenter, 1515 College Ave., Manhattan,KS 66502 (e-mail: to spinosad at 1 mg/kg (Fang et al. 2002a,b; Toews and [email protected]). Subramanyam 2003). 0022-0493/04/1174Ð1180$04.00/0 ᭧ 2004 Entomological Society of America June 2004 TOEWS AND SUBRAMANYAM:SUSCEPTIBILITY OF NATURAL ENEMIES TO SPINOSAD 1175 Materials and Methods Spinosad Toxicity to Natural Enemies. The survival of natural enemies in spinosad-treated wheat was de- Wheat. Hard red winter wheat, previously stored termined in the presence and absence of host insects for 24 mo in a round metal bin at the Kansas State in separate laboratory experiments. In the Þrst exper- University Grain Storage Training Center, Manhattan, iment, each0.95-liter glass jar, Þlled with100 g of KS, was used in tests. Four weeks before use in ex- uninfested wheat, was treated with 100 ␮l of distilled periments, the wheat was fumigated with aluminum water (control) or 100 ␮l of spinosad solution to pro- phosphide (Pestcon Systems, Inc., Raleigh, NC) to kill any live insects. Wheat (Ϸ2 kg) was removed for use vide rates of 0Ð1 mg/kg. Eachnatural enemy by rate in experiments from the bin by using a 1.2-m-long treatment was replicated eight times, and each repli- grain trier (Seedburo Equipment Co., Chicago, IL). cate was treated separately. After adding distilled wa- The dockage content, shrunken/broken kernels, for- ter or spinosad solution to the grain, the jars were eign material, damaged kernels, and total defects of Þtted withwire meshand Þlter paper lids and tumbled wheat, determined following ofÞcial methods (GIPSA for 20 min on a ball-mill roller (Morse Manufacturing 1997), was 0.1, 1.0, 0.3, 0.6, and 1.9% by weight, re- Co., model 200VS, East Syracuse, NY), to ensure uni- spectively. The test weight or bulk density of wheat form insecticide coverage on kernels. Twenty-four was 79.1 kg/hl, and the moisture content was 12.1%. hours after tumbling, 20 adults each of A. calandrae Before use in laboratory experiments, the wheat was (Savannahstrain), H. hebetor, T. elegans, or X. flavipes Ϫ Њ were introduced into untreated- or spinosad-treated frozen for7dat 13 C to kill any insects that survived Њ the fumigation. Moisture content of the wheat used in wheat in a jar. All jars were held at 28 C, 65% RH, and all experiments ranged from 11.7 to 13.3%. a photoperiod of 16:8 (L:D) h. After 24-h exposure, Insects. All natural enemies of stored-product in- natural enemies were separated from the wheat using sects were reared in the laboratory to produce a standard testing sieve with1.68-mm meshopenings sufÞcient numbers of known ages. Cultures of the (No. 12, Seedburo Equipment Co.). Natural enemies Indianmeal moth, Plodia interpunctella (Hu¨ bner) that could walk or ßy when prodded with a Þne cam- (Lepidoptera: Pyralidae), were reared on a turkey- elÕs-hair brush were considered to be alive. mashdiet (Subramanyam and Cutkomp 1987). The In the second experiment, adults of A. calandrae rice weevil, Sitophilus oryzae (L.) (Coleoptera: Cur- and T. elegans were exposed to wheat infested with culionidae), was reared on whole hard red winter S. oryzae and treated withwater or spinosad solution. wheat, and T. castaneum was reared on whole wheat Some members of the Pteromalidae require host feed- ßour plus 5% (by weight) brewerÕs yeast. The para- ing for normal oo¨genesis (Clausen 1940); thus, we sitoids Theocolax elegans (Westwood) (Hymenoptera: investigated the potential that host feeding may in- Pteromalidae) and two strains (Savannahand Bam- crease parasitoid survival in spinosad-treated wheat. berg) of Anisopteromalus calandrae (Howard) (Hy- Wheat was Þrst infested with S. oryzae and held in an menoptera: Pteromalidae), were obtained from the environmental chamber until fourth instars were USDA-ARS, Grain Marketing and Production Re- present, based on published developmental data search Center, Manhattan, KS. The Bamberg strain is (ShariÞ and Mills 1971). The wheat was then treated resistant to malathion (Baker 1994, Baker and Weaver witheitherwater or 1 mg/kg spinosad solution. 1993), whereas the Savannah strain is not. T. elegans H. hebetor was not included in this study because and A. calandrae were reared by introducing 100 adult S. oryzae is not a host for this parasitoid. In this ex- wasps (Ͻ3 d old) into 100 g of whole wheat containing periment, the Bamberg strain of A. calandrae was in- approximately 100 fourthinstars of S. oryzae. Habro- cluded to determine whether malathion resistance bracon hebetor (Say) (Hymenoptera: Braconidae) and would confer any survival beneÞts to parasitoids in a predator, the warehouse pirate bug, Xylocoris flavi- spinosad-treated wheat. Survival was assessed as de- pes (Reuter) (Heteroptera: Anthocoridae), were ob- scribed above. tained from BioFac Crop Care (Mathis, TX). H. he- X. flavipes Suppression of T. castaneum in betor was reared using the wandering stage larvae Spinosad-Treated Wheat. Because X. flavipes exhib- (Þfthinstars) of P. interpunctella, whereas X. flavipes ited signiÞcant survival in the previous experiments, was reared on T. castaneum eggs (Յ3 d old) placed in we investigated the ability of X. flavipes to suppress rolled oats. We placed 40 X. flavipes adults in 100 g of T. castaneum immatures in spinosad-treated wheat. rolled oats with Ϸ200 T. castaneum eggs, twice each Individual 0.95-liter jars containing 100 g of wheat week. All insects were reared in 0.95-liter glass jars received one of the following four treatments: distilled placed in environmental growthchambers(model water, 1 mg/kg spinosad, 1 mg/kg spinosad ϩ three I-36VL, Percival ScientiÞc, Boone, IA) maintained at female and two male X. flavipes adults, or distilled 28ЊC and 65% RH with a photoperiod of 16:8 (L:D) h.