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Butler, C.D. and J. T . Trumble. 2012. Identification and Impact of Natural

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Butler, C.D. and J. T . Trumble. 2012. Identification and Impact of Natural BIOLOGICAL AND MICROBIAL CONTROL Identification and Impact of Natural Enemies of Bactericera cockerelli (Hemiptera: Triozidae) in Southern California 1 CASEY D. BUTLER AND JOHN T. TRUMBLE Department of Entomology, University of California, Riverside, 900 University Ave., Riverside, CA 92521 J. Econ. Entomol. 105(5): 1509Ð1519 (2012); DOI: http://dx.doi.org/10.1603/EC12051 ABSTRACT Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) is a major pest of potato, (Solanum tuberosum L.), tomato (Solanum lycopersicum L.), and peppers (Capsicum spp.). The purpose of our research was to identify and determine the impact of natural enemies on B. cockerelli population dynamics. Through 2 yr of Þeld studies (2009Ð2010) at four different sites and laboratory feeding tests, we identiÞed minute pirate bug, Orius tristicolor (White) (Hemiptera: Anthocoridae); western bigeyed bug, Geocoris pallens Stål (Hemiptera: Geocoridae), and convergent lady beetle, Hippodamia convergens Gue´rin-Me´neville (Coleoptera: Coccinellidae) as key natural enemies of B. cockerelli in southern California potatoes, tomatoes, and bell peppers. In natural enemy exclusion cage experiments in the potato crop and in American nightshade, Solanum americanum Miller, the number of B. cockerelli surviving was signiÞcantly greater in the closed cage treatments, thus conÞrming the affect natural enemies can have on B. cockerelli. We discuss how this information can be used in an integrated pest management program for B. cockerelli. KEY WORDS Hemiptera, Coccinellidae, biological control, predator The potato/tomato psyllid, Bactericera cockerelli mirids, nabids, and syrphid larvae have all been re- (Sulc) (Hemiptera: Triozidae), is a serious pest of corded to feed on B. cockerelli (Knowlton 1933a,b, solanaceous crops such as potato (Solanum tuberosum 1934a; Knowlton and Allen 1936). A survey of poten- L.), tomato (Solanum lycopersicum L.), peppers (Cap- tial predatory natural enemies of B. cockerelli in po- sicum spp.), and eggplant (Solanum melongena L.) in tatoes was conducted by Pletsch (1947) in potato Central and North America, and most recently in New Þelds and found geocorids, coccinellids, and Zealand (Cranshaw 1994, Liu and Trumble 2007, Teu- chrysopids; although, no direct observations were lon et al. 2009, Crosslin et al. 2010). This pest has made of these natural enemies attacking potato psyl- caused millions of dollars in damage by direct feeding lid. Al-Jabr (1999) assessed two green lacewing spe- on crop plants and by transmitting a bacterial patho- cies, Chysoperla carnea Stephens and Chrysoperla ru- gen currently known as Candidatus Liberibacter psyl- filabris (Burmeister), as potential biological control laurous (a.k.a. Ca. L. solanacearum) (Munyaneza et al. agents of B. cockerelli in greenhouse tomato. These 2007, Hansen et al. 2008, Liefting et al. 2009, Crosslin two chrysopid species could complete development et al. 2010). on a diet of the B. cockerelli, but C. rufilabris was better One of the Þrst assessments that should be made in adapted to surviving in the greenhouse environment an integrate pest management program is the potential (Al-Jabr 1999). A Þeld trial involving augmentative role of natural enemies in controlling pests (Pedigo additions of C. carnea to psyllid-infested potatoes did and Rice 2006). B. cockerelli is reportedly attacked by not result in the reduction of psyllid numbers (Al-Jabr a number of natural enemies in North America (Cran- 1999). Natural enemies of B. cockerelli also include two shaw 1994). However, most of these reports are Ͼ40 primary parasitoids: Metaphycus psyllidis Compere yr old, focused on greenhouse populations, or they (Hymenoptera: Encyrtidae) and Tamarixia triozae were published before the new invasive biotype (Burks) (Hymenoptera: Eulophidae). However, these moved into California (Liu and Trumble 2007). two parasitoids have not provided signiÞcant control In Þeld locations in North America such as Arizona, of B. cockerelli in bell pepper or potato crops (Com- New Mexico, Texas, and Utah, chrysopids, antho- pere 1943, Johnson 1971, Cranshaw 1994). Thus, corids, and coccinellids have been observed attacking throughout the years various studies have been con- B. cockerelli (Anonymous 1932, Knowlton 1933a, ducted to document the natural enemies that attack B. Romney 1939). Under artiÞcial laboratory conditions, cockerelli, but few studies have identiÞed key natural chrysopid larvae, coccinellids, geocorids, anthocorids, enemies or their affect in the crop and noncrop hab- itats that this psyllid is known to inhabit (Romney 1 Corresponding author, e-mail: [email protected]. 1939, Cranshaw 1994). The natural enemy community 0022-0493/12/1509Ð1519$04.00/0 ᭧ 2012 Entomological Society of America 1510 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 5 that attacks B. cockerelli is unknown in California. In elli was the most abundant insect in all Þelds exam- addition, essentially no information on the potential ined. Voucher specimens of potential natural enemies population level suppression of natural enemies on B. were deposited at the Entomology Research Museum, cockerelli population dynamics is available (Goolsby et University of California, Riverside. al. 2007). Laboratory Feeding Assays. Results from the sur- At this time, within-Þeld biological control has not veys indicated that some natural enemy species were been implemented, mostly because B. cockerelli are more abundant than others. Based on the results of the treated with pesticides even at extremely low infes- relative abundance to natural enemies from the sur- tation levels in an attempt to reduce pathogen trans- veys, six natural enemies were further tested in lab- mission. Before biological control agents can be fully oratory feeding assays. B. cockerelli were reared and exploited in these systems, more studies are required maintained according to the methods described by to assess the effectiveness of predators and parasitoids Butler et al. (2011). Predators were collected from bell on B. cockerelli populations in southern California. peppers 31 August-28 September 2010 from Irvine, Thus, the objectives of this research were to identify CA. Predators were added to a 9-cm-diameter petri key natural enemies of B. cockerelli in potato, tomato, dish that contained a moistened Þlter paper and an and bell pepper plantings and to determine the impact excised tomato leaf with 20 eggs, 20 secondÐthird of natural enemies on B. cockerelli in key crop and instar nymphs, and 10 adult B. cockerelli (n ϭ 7Ð20 noncrop habitat in southern California. These data are petri dish arenas per predator species depending on a necessary Þrst step in developing a regional man- availability, and 29 control replicates with no preda- agement approach for this pest that includes natural tors to account for nonpredator mortality). Predators enemies. had access to B. cockerelli for a 24-h period. At the end of the 24-h period, the numbers of B. cockerelli at- tacked in all life stages were counted, and the per- Materials and Methods centage of mortality was calculated per stage. Surveys. Surveys were conducted throughout the Exclusion Cage Studies. These experiments were 2009 and 2010 cropping seasons in potatoes, tomatoes, conducted in late-season plantings of potato and the and bell peppers. Biweekly sampling surveys began 7 American nightshade, Solanum americanum Miller, in May 2009 and ended 3 December 2010. Commercial 2009 and 2010 at the University of California South potato Þelds in Lakeview, CA (Riverside Co.) as well Coast Research and Extension Center in Orange Co. as tomato and bell pepper Þelds in Camarillo, CA B. cockerelli has a wide host range and this psyllid is (Ventura Co.) experienced pesticide applications. Or- able to oviposit and complete development on Ͼ40 ganically grown bell pepper plants were also surveyed host species (Knowlton and Thomas 1934) but is most in Oxnard, CA (Ventura Co.) in 2009. Insecticide-free commonly found on solanaceous plants (Al-Jabr potato, tomato, and bell pepper plantings were sam- 1999). Experimental plots were established using a 2 pled at the University of California, South Coast Re- by 2 factorial design. The Þrst factor involved type of search and Extension Center in Irvine, CA (Orange plant: potatoes or American nightshade. Nightshade Co.). Thus, we covered a wide range of production plots were established 1 m distant from the potato systems and practices to Þnd potential natural ene- plots to minimize potential environmental variability. mies. The second factor varied exposure of B. cockerelli to Collection techniques included visual counts (both natural enemies by using exclusion cages. Cage treat- destructive sampling and in situ counts of potential ments were either closed, open (frame structure with- natural enemies on the crop plants) and sweep netting out screen) or no cages (after Van Driesche et al. of arthropods within agricultural Þelds. For the com- 2008). A 7.0- by 7.5-cm cage with thrips-proof mesh mercial Þelds, visual counts were conducted using a (SpiderNetϩ, Meteor Agricultural Nets Ltd., Israel) systematic sampling design whereby a total of 15Ð25 was placed over the terminal leaßet on the upper third plants per Þeld per sample date were examined. These of the plant. plants were sampled from three to Þve transects Leaßets were cleared of psyllids and natural ene- within a Þeld at every 20 m for up to 80 m on each mies before 10Ð15 lab-reared ÞrstÐsecond instar sample date. In addition, a 38-cm diameter sweep
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