BIOLOGICAL AND MICROBIAL CONTROL Identification and Impact of Natural Enemies of cockerelli (: 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 (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: ); western bigeyed bug, Geocoris pallens Stål (Hemiptera: ), 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 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 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 net nymphs were added to each leaßet and allowed to was used for sampling arthropods in the crop foliage settle for 24 h. Preliminary observations showed that by using a prearranged M-shaped pattern with 25 B. cockerelli nymphs are sedentary and would remain sweeps per sampling point within the Þeld. At the on the leaves (C.D.B., unpublished data). After 24 h, Orange Co. crop plantings, 8Ð15 plants were examined the number of psyllids remaining was conÞrmed and randomly within four plots per sampling date, and an then the appropriate cage treatment was added. Cages additional 20 sweeps per plot were collected. The were checked every 2Ð4 d until psyllids were no lon- number of natural enemies and the number of B. ger found. These experiments were conducted as a cockerelli that occurred on infested plants also were randomized complete block design with three blocks recorded. in 2009 and four blocks in 2010. Each block consisted Other alternative prey species were present and of one replicate of the plot treatments, with two rep- recorded from all Þelds, and included , thrips, licates of each cage treatment. whiteßies, ßea beetles, lepidopteran caterpillars, mir- Data Analysis. Multiple linear regressions were used ids, and Lygus hesperus (Knight); however, B. cocker- to analyze the number of natural enemies that occur October 2012 BUTLER AND TRUMBLE:NATURAL ENEMIES OF POTATO PSYLLID 1511 on B. cockerelliÐinfested crop plants. Because of sig- procedure of SAS. Both a repeated measures and niÞcant interactions (P Ͻ 0.05) between the number mixed linear effects models were tested. Results were of B. cockerelli that occur on crops by year and location essentially the same, but the repeated measures model (except for potatoes), we examined the regressions for produced biologically questionable interactions that each year and locality on each crop individually. Be- were contradictory. We therefore report the results cause of pesticide applications in the commercial from the general linear models procedure. Analysis of Þelds, regression analyses also were conducted indi- these data revealed no signiÞcant (P Ͼ 0.05) cage vidually so a comparison could be made between the effects so data from uncaged and open treatments commercial and insecticide-free plots. were pooled. The numbers of psyllids per cage treat- The average number of B. cockerelli that occurred ment were square root transformed to homogenize on crop plants were Þrst analyzed by using analysis of variances and normalize the data. Exclusion cage data variance (ANOVA) in a general linear models proce- were then analyzed using ANOVA in a general linear dure of SAS version 9.2 (PROC GLM, SAS Institute models procedure of SAS. When there was a signiÞ- 2008). The mean numbers of psyllids per crop plant cant interaction (P Ͻ 0.05) between year, date, plot were log transformed, reciprocal square root trans- and cage type, multiple comparison tests using the formed, and reciprocally transformed to homogenize LSMEANS/PDIFF option with a Tukey adjustment variances and normalize the data for bell pepper, to- were done to discriminate differences among the matoes, and potatoes, respectively. When there was a means. signiÞcant interaction (P Ͻ 0.05) between year and location, multiple comparison tests using the Results LSMEANS/PDIFF option with a Tukey adjustment were done to discriminate differences among the Surveys. A variety of natural enemies were recorded means. After the transformation of the dependent during the 2-yr study for each of the solanaceous crops variable, stepwise selection criteria were used to Þnd examined (Table 1). In total, 15 different spider gen- the natural enemies that best described the relation- era in nine families were represented in this survey. ship for the number of psyllids on the crop plants. Potential insect predators included 23 genera from 15 ConÞrmation of the best model was tested using ad- families. The most abundant groups included coc- justed R2, Akaike Information Criterion (AIC), Bayes- cinellids as well as three species of Hemiptera. From ian Information Criterion (BIC), and MallowsÕ Cp the species of coccinellids identiÞed, convergent lady criteria. In general, all model ranking tests agreed on beetle, Hippodamia convergens Gue´rin-Me´neville, which model was the best after the stepwise selection made up the majority consisting of 59.5% of the sam- criteria. Thus the model seems robust. The merits of ples. Two other coccinellids made up Ͼ5% of the individual model rating statistics can be found in Burn- samples included sevenspotted lady beetle, Coccinella ham and Anderson (2002). septempunctata L. (24.3%), and multicolored Asian Multiple regressions alone can be difÞcult to inter- lady beetle, Harmonia axyridis (Pallas) (8.1%). Min- pret; a high density of pests other than just psyllids ute pirate bug, Orius tristicolor (White) and Geocoris could attract natural enemies (particularly general- pallens Stål were present in all Þelds examined. The ists) and lead to a positive correlation that is statisti- mirid Cyrtopeltis modesta (Distant) was very abun- cally signiÞcant yet not primarily due to a response to dant in Orange Co. tomatoes (2009 and 2010) and psyllids. To determine whether the relationships seen potatoes (2010). Eggs from Chrysoperla spp. were for the multiple regression data were confounded by present in all Þelds as well; however, larvae and adults this or related problems, we graphed the total natural were much less common and not found in all Þelds. enemies versus the psyllid populations (Fig. 1). To Parasitoids reared from potato psyllids included T. avoid potential conßicts with pesticide selection and triozae and M. psyllidis. T. triozae was present in all of use, data are presented for pesticide-free tomato, po- the Þelds with the exception of potatoes in 2009; how- tato, and pepper Þelds sampled in 2009 and 2010. ever, the percentage of parasitism was Ͻ20%. M. psyl- Values are total numbers of psyllids and natural ene- lidis was rare (Ͻ2% of the parasitoids reared out of B. mies found on any given date. cockerelli) and only occurred in bell peppers in 2009. For the laboratory feeding assays, the numbers of B. Multiple Regression Analyses. The mean number of cockerelli in all life stages attacked within the 24-h B. cockerelli per plant by year and location are listed exposure with the potential predator were compared in Table 2. For bell peppers, there was a signiÞcant with controls and against each other using a general interaction between year and county for the number linear model (PROC GLM, SAS Institute 2008). When of B. cockerelli per plant (F ϭ 20.31; df ϭ 1, 279; P Ͻ a treatment factor was signiÞcant (P Ͻ 0.05), a prob- 0.0001). For bell peppers, the natural enemies such as ability difference with a Tukey adjustment was used to spiders, coccinellids, G. pallens, O. tristicolor, and the discriminate difference among the treatment means. parasitoid T. triozae exhibited signiÞcant relationships For the exclusion cage studies, the numbers of psyl- between the numbers of these natural enemies on lids per cage were Þrst tested between the open and plants that were infested with B. cockerelli (Table 2). uncaged treatments to rule out possible cage effects For bell peppers in Orange Co. in 2009, the overall (Van Driesche et al. 2008). The mean numbers of model was signiÞcant (F ϭ 7.64; df ϭ 2, 32; P ϭ 0.0019) psyllids in the open and uncaged treatments were and included spiders (␤ ϭϪ0.55; F ϭ 7.57; df ϭ 1, 32; tested by year using ANOVA in general linear models P ϭ 0.0097) and coccinellids (␤ ϭ 0.56; F ϭ 4.77; df ϭ 1512 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 5

Fig. 1. Relationships between total numbers of natural enemies and psyllids over time in 2009 and 2010 plantings of tomatoes (a), bell peppers (b), and potatoes (c) that were not exposed to pesticides.

1, 32; P ϭ 0.0363) as natural enemies that described the relationship for the number of B. cockerelli per plant mean number of psyllids per plant (R2 ϭ 0.32). There (R2 ϭ 0.09). The mean number of G. pallens per were on average 0.51 Ϯ 0.12 spiders and 0.14 Ϯ 0.09 psyllid-infested plants was 0.13 Ϯ 0.05. coccinellids per plant infested by potato psyllids. In In 2010 for Orange Co. bell peppers, both G. pallens Ventura Co. bell peppers in 2009, the overall model (␤ ϭ 0.90; F ϭ 8.37; df ϭ 1, 73; P ϭ 0.0050) and O. was signiÞcant (F ϭ 7.98; df ϭ 1, 80; P ϭ 0.0060) and tristicolor (␤ ϭ 0.44; F ϭ 4.31; df ϭ 1, 73; P ϭ 0.0415) only included G. pallens (␤ ϭϪ0.84; F ϭ 7.98; df ϭ 1, were included in the overall signiÞcant model (F ϭ 80; P ϭ 0.0060) as a natural enemy that described the 8.76; df ϭ 2, 73; P ϭ 0.0004) (R2 ϭ 0.19), and in Ventura coe 02B 2012 October

Table 1. Potential predators and parasitoids of B. cockerelli sampled in bell pepper, potato, and tomato from biweekly surveys that began 7 May 2009–3 December 2010

2009 2010 Order/family Species Bell pepper Potato Tomato Bell pepper Potato Tomato Total Orange Co. Ventura Co. Orange Co. Riverside Co. Orange Co. Ventura Co. Orange Co. Ventura Co. Orange Co. Riverside Co. Orange Co. Ventura Co. Araneae Araneidea Cyclosa sp.ÐÐÐ Ð ÐÐÐÐÐ Ð 1Ð1 Metepeira spp. Ð 1 Ð 3 1 Ð Ð Ð 1 1 1 Ð 8 Nesoscona spp. Ð Ð Ð Ð 1 Ð Ð Ð Ð Ð 3 Ð 4 Dictynidae Embylna reticulata ÐÐÐ Ð ÐÐÐÐÐ Ð 3Ð3 Emblyna spp. Ð Ð Ð Ð 3 Ð 1 Ð Ð Ð Ð Ð 4 UnidentiÞed spp. Ð Ð Ð Ð Ð Ð 1 Ð 1 Ð 1 Ð 3 Linyphiidae Erigone dentosa ÐÐÐ Ð ÐÐÐÐÐ 2ÐÐ2 Meloneta spp.ÐÐÐ 1ÐÐÐÐÐ 2 2Ð5 AND UTLER UnidentiÞed spp. Ð Ð Ð 1 Ð Ð Ð Ð Ð Ð 1 Ð 2 Miturgidae Cheiracanthium spp. Ð Ð Ð Ð Ð Ð Ð Ð 2 Ð Ð Ð 2 Oxyopidae Hamataliwa griesea ÐÐÐÐÐÐÐÐ1ÐÐÐ1 Oxyopes salticus ÐÐÐÐ1ÐÐÐÐÐÐÐ1

Tibellus spp. Ð Ð Ð Ð Ð Ð Ð Ð 2 Ð Ð Ð 2 T Philodromidea RUMBLE Salticidae Habronattus schlingeri ÐÐÐÐÐÐ1ÐÐÐÐÐ1 Habronattus sp. Ð Ð Ð Ð Ð Ð 1 Ð Ð Ð Ð Ð 1

Sassacus vitis ÐÐÐ Ð 1Ð 1Ð1Ð ÐÐ3:N Theridiidae Theridion goodnightorum ÐÐÐÐÐÐ1Ð1Ð 4Ð6

Theridion spp. Ð Ð Ð Ð Ð Ð Ð Ð Ð 1 4 Ð 5 ATURAL Thomididae Mesumenops californicus ÐÐÐÐ1ÐÐÐÐÐÐÐ1 Mesumenops lepidus ÐÐÐ 1ÐÐÐÐÐ Ð ÐÐ1 Mesumenops spp. Ð Ð Ð Ð 9 Ð Ð Ð 2 Ð 12 Ð 23 Xysticus spp. Ð Ð Ð 2 Ð Ð Ð Ð Ð Ð 1 Ð 3 E UnidentiÞed 18 1 6 44 57 8 103 18 44 32 119 14 464 OF NEMIES Coleoptera Anthicidae Notoxus spp.ÐÐÐ 3ÐÐ 1ÐÐ Ð ÐÐ4 Coccinellidae C. septempunctata ÐÐ5ÐÐÐ41Ð8ÐÐ18 Cycloneda sanguinea Ð2ÐÐÐÐ1ÐÐÐÐÐ3 H. axyridis ÐÐ1ÐÐÐ5ÐÐÐÐÐ6P OTATO H. convergens Ð19 1ÐÐ17276 1Ð44 Olla v-nigrum ÐÐÐÐÐÐÐ1ÐÐ 6Ð1 Scymnus spp. Ð Ð Ð Ð Ð Ð 1 Ð Ð Ð Ð Ð 2 UnidentiÞed spp. 5 Ð 1 8 2 1 19 17 38 6 Ð Ð 103 P SYLLID Melyridae Collops necopinus ÐÐ1ÐÐÐ1ÐÐÐ 2Ð2 Staphylinidae Platystethus spiculus Ð7ÐÐÐÐÐÐÐÐÐÐ7 UnidentiÞed spp. Ð Ð Ð 2 2 Ð Ð Ð Ð Ð Ð 3 9 Dermaptera ForÞculidae Forficula auricularia ÐÐÐ 1ÐÐÐÐ 2Ð Ð 14 Diptera Dolichopidae Asyndetus sp.ÐÐÐÐÐÐÐÐ1ÐÐÐ1 Chrysotus spp. Ð 2 Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð 2 Medetera spp. 3 Ð Ð Ð 1 Ð Ð Ð Ð Ð Ð Ð 4 Syrphidae Allographta sp. Ð Ð Ð Ð Ð Ð Ð Ð 1 Ð Ð Ð 1 Sphaerophoria spp. Ð Ð Ð Ð Ð Ð Ð Ð Ð Ð 3 Ð 3

UnidentiÞed spp. Ð Ð Ð 8 1 Ð Ð Ð Ð Ð Ð 1 10 1513 1514 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 5

Co. O. tristicolor (␤ ϭϪ0.43; F ϭ 6.25; df ϭ 1, 87; P ϭ

Total 0.0143) and parasitism by T. triozae (␤ ϭ 0.10; F ϭ 10.22; df ϭ 1, 87; P ϭ 0.0019) were included in the overall signiÞcant model (F ϭ 8.92; df ϭ 2, 87; P ϭ 0.0003) that described the relationship between the number of psyllids per bell pepper plant (R2 ϭ 0.17). On B. cockerelliÐinfested plants in 2010, there was an average of 0.28 Ϯ 0.08 G. pallens and 0.45 Ϯ 0.12 O. tristicolor per plant in Orange Co. and 0.31 Ϯ 0.08 O. tristicolor and 1.21 Ϯ 0.43 T. triozaeÐparasitized psyl- lids per plant in Ventura Co. There was a signiÞcant interaction between year and county for the mean number of B. cockerelli that occurred on tomatoes (F ϭ 23.65; df ϭ 1, 261; P Ͻ

2010 0.0001). Natural enemies in tomatoes that exhibited signiÞcant relationships with the number of B. cock- erelli per plant included spiders, G. pallens, O. tristi- color, and T. triozae (Table 2). For tomatoes in Orange Co. in 2009, the overall model was signiÞcant (F ϭ 7.38; df ϭ 1, 57; P ϭ 0.0087) and only included O. tristicolor (␤ ϭϪ0.05; F ϭ 7.38; df ϭ 1, 57; P ϭ 0.0087) as a natural enemy that described the relationship for the number of B. cockerelli per plant (R2 ϭ 0.11). The mean num- ber of O. tristicolor per tomato plant was 1.34 Ϯ 0.27. In Ventura Co. tomatoes in 2009, overall model was signiÞcant (F ϭ 6.52; df ϭ 3, 69; P ϭ 0.0005) and included spiders (␤ ϭϪ2.15; F ϭ 6.03; df ϭ 1, 69; P ϭ 0.0165), G. pallens (␤ ϭϪ3.02; F ϭ 4.83; df ϭ 1, 69; P ϭ 0.0313), and T. triozae (␤ ϭ 0.03; F ϭ 5.93; df ϭ 1, 69; P ϭ 0.0175) as natural enemies that described the mean number of psyllids per plant (R2 ϭ 0.23). There was an average of 0.11 Ϯ 0.04, 0.04 Ϯ 0.02, and 5.58 Ϯ 2.82 spiders, G. pallens, and T. triozaeÐparasitized psyl- lids per tomato plant that contained psyllids, respec- tively. For tomatoes in Orange Co. in 2010, the overall model was signiÞcant (F ϭ 6.48; df ϭ 1, 72; P ϭ 0.0131) and only included G. pallens (␤ ϭϪ0.36; F ϭ 6.48; df ϭ 1, 72; P ϭ 0.0131) as a natural enemy that described the

2009 relationship for the number of B. cockerelli per plant (R2 ϭ 0.08). The mean number of G. pallens per B. cockerelliÐinfested plants was 0.49 Ϯ 0.15. In Ventura Co. tomatoes in 2010, G. pallens (␤ ϭ Ϫ2.28; F ϭ 22.31; df ϭ 2, 56; P Ͻ 0.0001) and parasitism by T. triozae (␤ ϭ 0.03; F ϭ 16.12; df ϭ 2, 56; P ϭ 0.0002) were included in the overall signiÞcant model (F ϭ 23.04; df ϭ 2, 56; P Ͻ 0.0001) to describe the relation- ship between the numbers of psyllids per plant (R2 ϭ

Bell pepper Potato Tomato Bell pepper Potato Tomato Ϯ 2 19 2 36 1 3 24 6 1 9 36 17 156 1Ð381Ð1Ð39 318Ð12Ð 815Ð 1 43 3 2 86 26 49 41 13 7 55 11 337 5ÐÐ Ð ÐÐÐÐÐ Ð ÐÐ5 0.45). There was an average of 0.29 0.07 G. pallens Ð 17 2 11 108 37 7 5 144 1 200 13 545 ÐÐÐ 1ÐÐ 1ÐÐ 1 2Ð5 10 4 Ð Ðand 8 9.58 Ϯ 4.14 35T. triozae 19Ðparasitized 11 psyllids 1 per 5B. 5 175 273

Orange Co. Ventura Co. Orange Co. Riverside Co. Orange Co. Ventura Co. Orange Co. Ventura Co. Orange Co. Riverside Co. Orange Co. Ventura Co. cockerelliÐinfested plant. For potatoes, there was no signiÞcant effect of year (F ϭ 0.03; df ϭ 1, 181; P ϭ 0.8562) and county (F ϭ 2.08; df ϭ 1, 181; P ϭ 0.1507) regarding the number of spp. eggsspp. larvaespp. adults 16 1 Ð 15 1 Ð 25 1 1 38 6 3 4 1 1 26 Ð Ð 76 Ð 5 85 3 Ð 24 1 53 1 Ð 24 Ð Ð 9 1 395 1 Ð 15 12

spp. ÐB. cockerelli 1 Ðper plant nor 1 was the Ð interaction Ð between Ð Ð Ð Ð Ð Ð 2 ϭ ϭ ϭ spp. Ðyear Ð and county Ð signiÞcant 3 (F 1.85; 2 df Ð1, 181; P 10 Ð 1 3 Ð Ð 19 0.1749) (Table 2). There were no signiÞcant relation- Empicoris Chrysoperla Chrysoperla Chrysoperla C. modesta Nabis Pronotacantha annulata G. pallens Linepithema humile O. tristicolor T. triozae M. psyllidis ships for the number of B. cockerelli per potato plant for Orange Co. in 2009 or Riverside Co. in 2009 and 2010. Only for potatoes in Orange Co. in 2010, the overall model was signiÞcant (F ϭ 10.79; df ϭ 2, 59; P ϭ

Total 69 115␤ 62ϭϪ 176ϭ 294 137 357 191 302 137 489 245 2,574

Table 1. Continued 0.0001) and included O. tristicolor ( 0.19; F Hemerobiidae UnidentiÞed adult Ð Ð Ð Ð Ð Ð Ð 1 Ð Ð Ð Ð 1 Chrysopidae Geocoridae Formicidae Anthocoridae Eulophidae Encyrtidae Order/family Species Neuroptera

Hemiptera ϭ ϭ Hymenoptera 4.40; df 1, 59; P 0.0403) and parasitism by T. triozae coe 02B 2012 October

Table 2. Multiple regression analyses to describe the relationship between the number of B. cockerelli and the number of natural enemies per plant

Multiple regression results by year and location Crop 2009, Orange Co. 2009, Ventura Co. 2010, Orange Co. 2010, Ventura Co. Bell pepper Psyllids per plant 6.7 Ϯ 1.3a 14.9 Ϯ 2.1ab 17.5 Ϯ 2.0b 154.6 Ϯ 23.3c Parameter estimate (Ϯ SE) P Ͼ t Parameter estimate (Ϯ SE) P Ͼ t Parameter estimate (Ϯ SE) P Ͼ t Parameter estimate (Ϯ SE) P Ͼ t Intercept 1.83 Ϯ 0.18 Ͻ0.0001 2.27 Ϯ 0.13 Ͻ0.0001 3.37 Ϯ 0.23 Ͻ0.0001 4.27 Ϯ 0.14 Ͻ0.0001 Araneae spp. Ϫ0.55 Ϯ 0.20 0.0097 Coccinellids 0.56 Ϯ 0.25 0.0363 AND UTLER G. pallens Ϫ0.84 Ϯ 0.30 0.0060 0.90 Ϯ 0.31 0.0050 O. tristicolor 0.44 Ϯ 0.21 0.0415 Ϫ0.43 Ϯ 0.17 0.0143 T. triozae 0.10 Ϯ 0.03 0.0019 F 7.64 7.98 8.76 8.92

df 2, 32 1, 80 2, 73 2, 87 T P Ͼ F 0.0019 0.0060 0.0004 0.0003 RUMBLE R2 0.3233 0.0907 0.1935 0.1702

2009, Orange Co. 2009, Ventura Co. 2010, Orange Co. 2010, Ventura Co. :N

Tomato ATURAL Psyllids per plant 3.7 Ϯ 1.5a 457.6 Ϯ 212.8c 21.7 Ϯ 5.1b 201.1 Ϯ 58.5bc Intercept 0.93 Ϯ 0.04 Ͻ0.0001 3.74 Ϯ 0.30 Ͻ0.0001 2.01 Ϯ 0.20 Ͻ0.0001 3.40 Ϯ 0.30 Ͻ0.0001 O. tristicolor Ϫ0.05 Ϯ 0.02 0.0087 G. pallens Ϫ3.02 Ϯ 1.38 0.0313 Ϫ0.36 Ϯ 0.14 0.0131 Ϫ2.28 Ϯ 0.48 Ͻ0.0001 E Araneae spp. Ϫ2.15 Ϯ 0.88 0.0165 OF NEMIES T. triozae 0.03 Ϯ 0.01 0.0175 0.03 Ϯ 0.01 0.0002 F 7.38 6.72 6.48 23.04 df 1, 57 3, 69 1, 72 2, 56 P Ͼ F 0.0087 0.0005 0.0131 Ͻ0.0001 2 P R 0.1146 0.2261 0.0826 0.4514 OTATO 2009, Orange Co. 2009, Riverside Co. 2010, Orange Co. 2010, Riverside Co.

Potato P Psyllids per plant 0.33 Ϯ 0.13a 3.84 Ϯ 1.0a 2.3 Ϯ 1.0a 2.8 Ϯ 0.9a SYLLID Intercept 0.83 Ϯ 0.04 Ͻ0.0001 O. tristicolor Ϫ0.19 Ϯ 0.09 0.0403 T.triozae Ϫ0.56 Ϯ 0.16 0.0008 F 10.79 df 2, 59 P Ͼ F 0.0001 R2 0.2678 1515 1516 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 5

Table 3. Number (mean ؎ SE) of B. cockerelli attacked and percentage mortality in 24-h no-choice feeding trials with potential predators from bell pepper, 31 August–28 September 2010, Irvine, CA

B. cockerelli adults B. cockerelli nymphs B. cockerelli eggs Order/family Species n No. % No. % No. % attackeda mortality attackeda mortality attackeda mortality Coleoptera Coccinellidae C. septempunctata 7 5.3 Ϯ 1.2bc 53 9.1 Ϯ 2.2bc 39 0.0 Ϯ 0.0a 0 H. axyridis 18 8.5 Ϯ 0.6a 85 17.2 Ϯ 1.7a 72 2.7 Ϯ 0.8ab 12 H. convergens 20 7.1 Ϯ 0.7ab 71 15.5 Ϯ 0.9a 77 6.5 Ϯ 1.5b 32 Hemiptera Anthocoridae O. tristicolor 20 1.8 Ϯ 0.3e 18 9.7 Ϯ 1.1c 48 3.0 Ϯ 1.0a 14 Miridae C. modesta 20 0.8 Ϯ 0.2de 8 6.2 Ϯ 0.8bc 31 0.8 Ϯ 0.4ab 4 Neuroptera Chrysopidae Chrysopa spp. larvae 17 2.9 Ϯ 0.5cd 28 14.4 Ϯ 1.0ab 66 6.6 Ϯ 1.5b 27 Control 29 1.2 Ϯ 0.2e 12 1.7 Ϯ 0.4d 9 0.6 Ϯ 0.2a 3

a Means within a column for the respective B. cockerelli life stage followed by different letters are signiÞcantly different using PROC GLM of SAS.

(␤ ϭϪ0.56; F ϭ 12.57; df ϭ 1, 59; P ϭ 0.0008), which survived by year (F ϭ 126.26; df ϭ 1, 307; P Ͻ 0.0001), described the mean number of B. cockerelli per plant date (F ϭ 264.64; df ϭ 3, 307; P Ͻ 0.0001), habitat (i.e., (R2 ϭ 0.27). There was an average of 0.13 Ϯ 0.05 O. potato versus nightshade) (F ϭ 4.41; df ϭ 1, 307; P ϭ tristicolor and 0.06 Ϯ 0.03 T. triozaeÐparasitized B. 0.0366), and cage type (F ϭ 187.37; df ϭ 1, 307; P Ͻ cockerelli per potato plant that contained psyllids. 0.0001). Based on these results, the numbers of psyllids The relationships between total natural enemies that survived per cage type were analyzed separately and psyllid populations were informative (Fig. 1). In in the potato crop and nightshade plots by year and tomato plantings (Fig. 1a), populations of psyllids de- date (Figs. 2 and 3). Within the potato crop, the clined following a peak in early July of 2009 and mid- average number of B. cockerelli that survived was sig- July in 2010 as natural enemy densities increased. niÞcantly greater in the closed cages compared with Natural enemy populations peaked 2Ð3 wk later in the open cages (F ϭ 55.40; df ϭ 1, 145; P Ͻ 0.0001). both years, supporting the relationships calculated Similar dynamics occurred within the nightshade with the multiple regression analyses. For bell peppers plots. SigniÞcantly more psyllids survived in the closed (Fig. 1b), numbers were fairly low in 2009 and the cages versus the open cages (F ϭ 143.36; df ϭ 1, 145; natural enemies were not efÞcient at controlling the P Ͻ 0.0001). Natural enemies observed in the plots psyllids. In contrast, the much higher values seen in during the time of these experiments included spiders, 2010 again provided a bimodal distribution. The pop- H. convergens, C. septempinctata, H. axyridis, O. tristi- ulation of psyllids peaked in mid-July followed by a color, G. pallens, Nabis spp., C. modesta, Chrysoperla rapid decline as the density of beneÞcials increased spp. larvae, and syrphid larvae. (peak of beneÞcials was 30 July 2010). There were no clear patterns seen with psyllid and natural enemy Discussion populations in potatoes (Fig. 1c), also supporting the results seen with the multiple regression analyses. Based on the data from the surveys, regression anal- Laboratory Feeding Assays. From this list of poten- yses, and laboratory feeding assays, we have identiÞed tial B. cockerelli predators, a subset of natural enemies O. tristicolor, G. pallens, and H. convergens as key was tested in laboratory trials to determine whether they natural enemies of B. cockerelli in southern California, could consume potato psyllids and which stages they which may warrant further research for natural enemy could attack (Table 3). All of the predators except C. conservation or augmentation in the crop and non- modesta and O. tristicolor attacked signiÞcant numbers of crop habitats. The numbers of O. tristicolor exhibited adults compared with the control (F ϭ 40.62; df ϭ 6, 124; signiÞcant relationships with the number of B. cock- P Ͻ 0.0001). H. axyridis attacked the most adults in 24 h erelli per plant in bell peppers in Orange and Ventura compared with all other predators with the exception of Cos. in 2010, tomatoes in Orange Co. in 2009, and H. convergens, and the percentage of mortality inßicted potatoes in Orange Co. in 2010. Furthermore, O. tris- upon B. cockerelli adults was greatest for H. axyridis at ticolor was observed attacking B. cockerelli in bell pep- 85%. Likewise, Chrysoperla spp. larvae also could suc- pers in Ventura Co., 2010 (our unpublished data). As cessfully attack signiÞcant number of adults. with the observations by Knowlton and Allen (1936), For the immature stages of the potato psyllids, all of our results corroborate that O. tristicolor is a predator the natural enemies tested attacked signiÞcant num- of B. cockerelli but go beyond their observations to bers of B. cockerelli nymphs (F ϭ 42.94; df ϭ 6, 124; P Ͻ show that this predator is able to attack signiÞcant 0.0001). Only H. convergens and Chrysoperla spp. lar- numbers of nymphs and adults. For the predator G. vae were able to attack signiÞcant numbers of B. cock- pallens, previous work by Pletsch (1947) in Montana erelli eggs (F ϭ 6.11; df ϭ 6, 124; P Ͻ 0.0001). only found this predator in potatoes, whereas Knowl- Exclusion Cage Study. There were signiÞcant dif- ton (1934a) noted Geocoris decoratus Uhler in pota- ferences in the number of B. cockerelli nymphs that toes in Utah and tested this species in the laboratory October 2012 BUTLER AND TRUMBLE:NATURAL ENEMIES OF POTATO PSYLLID 1517

Fig. 2. Number (mean Ϯ SE) of potato psyllids per cage type by year and date in potatoes plots at the University of California South Coast Research and Extension Center, Orange Co., CA (F ϭ 32.95; df ϭ 21,145; P ϭϽ0.0001). Bars associated with different letters are signiÞcantly different using the LSMEANS/PDIFF option with a Tukey adjustment. as a predator of B. cockerelli. Our research has shown ber of B. cockerelli per plant. Further experiments may that G. pallens exhibits signiÞcant relationships with B. be needed to determine which species may be most cockerelli in bell peppers in Ventura Co. in 2009 and important, but in direct observation in bell peppers in Orange Co. in 2010, and tomatoes in Ventura Co. in Orange Co. the species Cyclosa turbinata Walckanaer 2009Ð2010 and in Orange Co. in 2010. Like O. tristi- (Araneae: Araneidae) produced webs that had color, this predator was present in all Þelds examined trapped B. cockerelli adults (our unpublished data). and lends support to this predator being a natural Although the parasitoid T. triozae has not provided enemy of B. cockerelli. signiÞcant control of B. cockerelli in previous experi- Only coccinellids exhibited signiÞcant relationships ments (Johnson 1971), we believe there is potential with the number of psyllids per pepper plant in Or- for this parasitoid to be used as a control agent in ange Co. in 2009. Again H. convergens accounted for noncrop habitats or crops that are not repeatedly 59.5% of the coccinellids found. This is similar to the Ͼ treated with pesticides. Parasitoids in the Tama- observations made in surveys conducted 60 yr ago rixia have been used successfully as biocontrol agents by Pletsch (1947). H. convergens also consumed sig- against other psyllid species (Dahlsten et al. 1995, niÞcant numbers of all life stages of B. cockerelli. How- Kennett et al. 1999). The number of parasitized B. ever, in direct observations in the Þeld we have ob- cockerelli exhibited signiÞcant relationships in many of served H. convergens ignoring B. cockerelli eggs while the crops we surveyed in southern California; how- searching for prey (our unpublished data). Thus, further ever, despite this, the percentage of parasitism in ag- tests may be needed to verify the importance of egg Ͻ predation on psyllid mortality. Additional tests may be ricultural Þelds was low ( 20%). In particular, the justiÞed because egg feeding by the coccinellid Diomus multiple regression analyses for total natural enemies pumilio (Weise) has been reported as an important con- and the graphs in Fig. 1 show that where the psyllid Ϸ tributing factor in suppression of another psyllid, Acizzia specialist T. triozae accounted for 40Ð55% of the uncatoides (Ferris & Klyver) (Pinnock et al. 1978). Rom- total natural enemy density (bell peppers and tomatoes, ney (1939) also reported that coccinellids (unidentiÞed respectively), the relationships indicated potentially species) can reduce the number of eggs and nymphs of useful biological control. Similarly, Romney (1939) B. cockerelli in Lycium spp. in southern Arizona, New made the claim that T. triozae could reduce the number Mexico, and Texas. of nymphs of B. cockerelli in Lycium spp., but details were Numerous spider species were observed and pres- sparse. In our samples from potatoes, where more than ent in all Þelds examined. Spiders in bell peppers in two thirds of the natural enemies were generalists, the Orange Co. in 2009 and in tomatoes in Ventura Co. in lack of relationships in either the multiple regression 2009 exhibited signiÞcant relationships with the num- analyses or the graphical data (Fig. 1c) suggested that the 1518 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 105, no. 5

Fig. 3. Number (mean Ϯ SE) of potato psyllids per cage type by year and date in nightshade plots at the University of California South Coast Research and Extension Center, Orange Co., CA (F ϭ 47.57; df ϭ 21,145; P ϭϽ0.0001). Bars associated with different letters are signiÞcantly different using the LSMEANS/PDIFF option with a Tukey adjustment. complex of natural enemies as a whole were not re- psyllid populations. Our data from the exclusion cage sponding speciÞcally to the psyllids. study is the Þrst to suggest that natural enemies can Some caution should be noted with these results as have an impact on the survival of B. cockerelli in a Þeld many of the natural enemies that exhibited signiÞcant crop or a noncrop host plant. Just 2 d after initiation relationships with the number of psyllids per plant, the of the experiment, the number of B. cockerelli nymphs range of R2 values (0.08Ð0.45, Table 2) suggest that the decreased signiÞcantly by 59% in potatoes and 66% in natural enemies may not show a predictive relation- nightshade compared with the closed cages for both ship with B. cockerelli in agricultural Þelds. Plants with years of the experiment. Because parasitized psyllids high numbers of predators may attract or arrest more were not observed with these cage experiments, gen- natural enemies than plants with low numbers, leading eralist predators may have been responsible to a correlation. In contrast, efÞcient natural enemies for the decreases in B. cockerelli. The results from this might subsequently lower the pest densities, resulting study open new possibilities of research regarding B. in a negative correlation. However, our primary goal cockerelli management options and research avenues was to identify potential candidates for biological con- with natural enemies for this pest. As has been seen in trol, so we focused on determining which natural other systems, the applications of pesticides could be control agents were present and if there was a statis- timed to minimize the impact on natural enemies and the tical relationship between psyllids and natural ene- choice of selective compounds could potentially con- mies over the course of the crop cycles. For example, serve the natural enemy groups we found feeding on although other potential predators tested in the lab- psyllids (Rutledge et al. 2004). Cultural control practices, oratory included Chrysoperla spp. larvae and C. mod- enhancement of the environment, and other conserva- esta, which attacked signiÞcant number of B. cockerelli tion practices for beneÞcial (Van Driesche et al. nymphs, the number of these predators did not cor- 2008) should be investigated to improve management of relate with the number of B. cockerelli that occurred B. cockerelli in solanaceous crops. on crop plants. Numerous Chrysoperla spp. eggs were found in the Þeld, but very few Chrysoperla spp. larvae, suggesting that larval Chrysoperla spp. may experience Acknowledgments heavy intraguild predation (Rosenheim et al. 1999). We thank J. Butler, N. Solares, B. Vindiola, S. Gilbert, A. No studies to date have systematically examined the Murillo, and N. Drew for assistance with surveys, experi- effects of natural enemies on B. cockerelli in crops, ments, and colony maintenance. We thank B. Lunt (Agri- much less on noncultivated host plants. Thus, we cur- Empire Corp.), R. Martinez (Deardorff Family Farms), P. rently have minimal information on the role that nat- McGrath (McGrath Family Farms), and E. Shell (Sun World ural enemies might be playing in suppression of the International, LLC) for permission to sample crop plants for October 2012 BUTLER AND TRUMBLE:NATURAL ENEMIES OF POTATO PSYLLID 1519

B. cockerelli and natural enemies. Special thanks also to T. dae) in north central Colorado. M.S. thesis, Colorado Prentice (University of California (UC)ÐRiverside), C. Wei- State University, Fort Collins. rauch (UCÐRiverside), D. Yanega (UCÐRiverside), and B. Kennett, C. E., J. A. McMurtry, and J. W. Beardsley. 1999. Zuparko (California Academy of Sciences) for identiÞca- Biological control in subtropical and tropical crops, pp. tions of natural enemies. We thank T. Paine, R. Stouthamer, 713Ð742. In T. S. Bellows and T. W. Fisher (eds.), Hand- B. Carson, G. Kund, K. Hladun, C. Mogren, and J. Diaz- book of biological control. Academic, San Diego, CA. Montano for comments and suggestions that improved an Knowlton, G. F. 1933a. Aphis lion predators of the potato earlier version of this manuscript. This research was funded psyllid. J. Econ. Entomol. 26: 977. by the Robert and Peggy van den Bosch Memorial Scholar- Knowlton, G. F. 1933b. 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Burks (Hymenoptera: Eulophidae) as a biological control agent of Paratrioza cockerelli (Sulc) (Homoptera: Psylli- Received 2 February 2012; accepted 28 June 2012.