Research Article t

of Industrial Hygienists. Lewis Pub. New controls investigated Faucett J, Meyers J, Tejeda D, et al. 2001. An instrument to measure muscu- for vine loskeletal symptoms among immigrant Hispanic farmworkers: Validation in the nursery industry. J Agric Saf Health 7(3):185–98. Kent M. Daane Garg A, Chaffin D, Herrin G. 1978. Walter J. Bentley n the early 1990s, the vine mealybug Prediction of metabolic rates for manual Vaughn M. Walton was accidentally introduced into the materials handling jobs. Am Ind Hyg Assoc J ICoachella Valley (Gill 1994; Godfrey 39(8):661–74. Raksha Malakar-Kuenen et al. 2003), probably from Mexican or Glisan B. 1993. Customized prevention Jocelyn G. Millar programs play vital role in back protection Argentinian table-grape vineyards. This Chuck A. Ingels process. Occup Health Safety 62(12):21–6. invasive pest quickly spread to grape- Ed A. Weber Hashemi L, Webster BS, Clancy EA, growing regions in the San Joaquin Val- Volinn E. 1997. Length of disability and Carmen Gispert cost of workers’ compensation low back ley (1998), Central Coast (1999), North pain claims. J Occupational Environ Med t Coast (2001), Sacramento Valley (2002), 39(10):937–45. Sierra foothills (2002) and Monterey Leamon TB. 1994. Research to reality: A critical review of the validity of various cri- The vine mealybug is a newly inva- area (2002). As of fall 2005, the vine teria for the prevention of occupationally sive pest that has spread throughout mealybug had been found in 17 Califor- induced low back pain disability. Ergonom- California’s extensive grape-growing nia counties, and it is likely that more ics 37(12):1959–74. infestations have not been detected. Marras WS, Allread WG, Burr DL, regions. Researchers are investigating Vineyard decrease crop Fathallah FA. 2000. A prospective valida- new control tools to be used in com- tion of a low-back disorder risk model and quality by excreting honeydew, which an assessment of ergonomic interventions bination with or as an alternative to promotes sooty molds, and by infest- associated with manual materials handling standard organophosphate insecticide tasks. Ergonomics 43(11):1866–86. ing grape bunches (Flaherty et al. 1992). Marras WS, Lavender SA, Leurgans SE, controls. growth regulators and The vine mealybug (Planococcus ficus et al. 1993. The role of dynamic three- nicotine-based insecticides provide [Signoret]) has biological characteristics dimensional trunk motion in occupation- that make it more damaging than other ally related low back disorders: The effect good alternative pesticides for use in of workplace factors, trunk position, and some vineyards. Ongoing studies on vineyard mealybugs (Godfrey et al. trunk motion characteristics on risk of in- the augmentative release of natural 2002). For example, the vine mealybug jury. Spine 18(5):617–28. has a high reproductive rate, with some enemies and mating disruption also Marras WS, Lavender SA, Leurgans SE, females depositing more than 250 eggs, et al. 1995. Trunk motion and occupation- show promise, but commercial prod- ally related low back disorder risk. Ergo- and a fast development time, with four nomics 38:377–410. ucts are not yet available to growers. to seven generations per year in the San Meyers J, Miles J, Faucett J, et al. 2001. Priority risk factors for back injury in agri- cultural field work: Vineyard ergonomics. J Agromed 8(1):37–52. [NRC-IOM] National Research Council and Institute of Medicine. 2001. Musculo- skeletal disorders and the workplace: Low back and upper extremities. Panel on Mus- culoskeletal Disorders and the Workplace, Commission on Behavioral and Social Sci- ences and Education. Washington, DC: Nat Acad Pr. [OSU] Ohio State University Research News. 2001. Landmark study uncovers rea- sons behind recurring back injury. Decem- ber. Columbus, OH. http://researchnews. osu.edu/archive/backemg.htm. US Public Health Service. 1991. Healthy People 2000: National health promotion and disease prevention objectives. US De- partment of Health and Human Services, Washington, DC. Obj. 10.2. Waters TR, Putz-Anderson V, Garg A, Fine LJ. 1993. Revised NIOSH equation for the design and evaluation of manual lift- ing tasks. Ergonomics 36(7):749–76. Waters T, Putz-Anderson V, Garg A. 1994. Applications Manual for the Revised NIOSH Lifting Equation. DHHS (NIOSH) Pub No 94–110. The nonnative vine mealybug, female (left) and winged male (right), excretes abundant Webster B, Snook S. 1990. The cost of honeydew, and infests and feeds on grape leaves and bunches. The authors investigated compensable low back pain. J Occup Med sustainable alternatives to conventional insecticides, which are often ineffective because 32(1):13. the mealybug can reside under the bark.

http://CaliforniaAgriculture.ucop.edu • january–march 2006 31 Joaquin Valley. In addition to producing no-insecticide control. Treatment plots Insecticide trials abundant honeydew, the vine mealy- were three rows by 80 to 125 vines bug feeds on grape leaves and bunches Until recently, the recommended (0.5 to 0.7 acres), running the length through much of the summer. This pest insecticide program for vineyard of each row. In the drip-irrigated vine- also has a wide host range, which in- mealybugs was a delayed dormant yards, a 4- to 6-hour pretreatment irri- cludes common weeds (such as malva), organophosphate insecticide (chlorpy- gation prepared the soil. Imidacloprid potentially increasing residual popula- rifos [Lorsban, Dow Chemical]) and/or was then applied through the irriga- tions outside the vineyard. Finally, like in-season applications of a short- tion system, and a 6- to 8-hour post- other vineyard mealybugs, the vine residual organophosphate (e.g., diazinon treatment irrigation was used to move mealybug can transmit grapevine viral [Helena Chemical]) or carbamate (e.g., the insecticide into the root zone. The diseases (Golino et al. 1999). methomyl [Lannate, DuPont]) (Bentley furrow-irrigated vineyards were pre- Unfortunately, the vine mealybug is et al. 2003). While these insecticides pared by French plowing the berm and a pest that is here to stay in California can provide adequate vine mealybug furrow area to expose surface roots, and will likely continue to spread. Its control, their repeated use may also followed by a 1-day pretreatment irriga- dissemination is facilitated by the sticky kill natural enemies of the mealybug, tion. Imidacloprid was then applied into nature of the honeydew; infested plant reducing the level of biological control the furrows using an herbicide spray material may be moved by wind-blown (Walton and Pringle 1999). We studied rig, and the application was followed by leaves, , farm equipment and the effectiveness of two insecticides a 1-day posttreatment irrigation. field crews. Grape clusters harvested considered less disruptive than the Mealybug density was monitored from infested vineyards may also pro- organophosphates: imidacloprid before treatment application (between mote the pest’s movement to new vine- (Admire, Bayer), a systemic, nicotinoid March 13 and 19, 2002) by a field dis- yard blocks because some mealybugs insecticide; and buprofezin (Applaud, section of two spurs per vine on 25 ran- can survive the destemming process Nichino America), an insect growth domly selected vines per plot for a total and grower-managed compost piles. regulator. We report here on a part of of 625 vines per vineyard (Geiger et al. As a result, caution must be taken with this larger study. 2001). To determine treatment effect, the disposal of harvest waste. Finally, Systemic insecticide. In 2002, we crop damage was evaluated at harvest because mealybugs often reside beneath tested the effectiveness of imidaclo- using a 0-to-3 cluster rating system, the vine’s bark or underground, the prid as a systemic insecticide (applied where 0 = no mealybug damage, 1 = detection of infested nursery stock is through irrigation water and taken up by honeydew (indicating the presence of difficult and the effectiveness of contact the vine roots) at different timings. The mealybugs), 2 = honeydew and mealy- insecticides is reduced. study was conducted in two vineyards, bugs but the cluster is harvestable, and In response to the serious conse- one with drip and the other with furrow 3 = unmarketable (Geiger and Daane quences of vine mealybug infesta- irrigation, near Del Rey (Fresno County). 2001). In each treatment plot, 25 vines tions in California, a consortium of The vineyards were mature (more than were randomly selected and nine clus- University, private, and county and 20 years old) ‘Thompson Seedless’ ters per vine were sampled. state personnel has initiated regional blocks, planted in a well-drained, sandy- Foliar treatments. In 2003, we tested trapping and control efforts (Daane, loam soil and managed for raisin grapes. five treatments in the existing 2002 drip- Bentley, et al. 2004). Effective, In each vineyard, imidacloprid was and furrow-irrigated plots. The five insecticide-based control programs applied at full label rate in a random- treatments were: (1) 32 ounces imida- have been developed for regions ized complete block with five blocks, cloprid per acre, applied in May 2003 to where the pest is well established. In a each containing the following five treat- plots that had received the same treat- series of studies, we focused on more ments: 32 ounces imidacloprid per acre ment in April 2002; (2) no insecticide ap- sustainable controls that may work in applied in (1) April, (2) May or (3) June; plied in 2003 to plots that had received combination with or as alternatives to (4) 16 ounces imidacloprid per acre ap- 32 ounces imidacloprid per acre in May standard insecticide programs. plied in both April and May; and (5) a 2002; (3) 12 ounces buprofezin per acre,

32 CALIFORNIA AGRICULTURE • VOLUME 60, NUMBER 1 Left to right, the vine mealybug was introduced into California in the early 1990s, and is currently found in at least 17 counties; infested windblown leaves can easily spread the pest from vine to vine, and vineyard to vineyard; grape bunches are rendered unmarketable; a damaged grapevine trunk.

until late spring, further reducing their exception that we sampled 50 randomly early-season densities (Daane, Malakar- selected vines per treatment plot and Kuenen, et al. 2004). Third, foraging five clusters per vine. ants protect mealybugs from parasitoids Disrupting mealybug mating (Daane, Sime, et al. 2004). And finally, the parasitoid prefers larger mealybugs, Until recently, a major hurdle in con- especially for the production of female trolling mealybugs was the difficulty of parasitoids. detecting them in nurseries and vine- We tested inoculative releases of yards. In 2001, a more effective monitor- applied in June 2003 to plots that had Anagyrus as a possible mechanism to ing method was developed utilizing received 32 ounces imidacloprid per overcome some of these barriers. Field the mealybug’s sex pheromone. Female acre in June 2002; (4) 2 quarts chlorpyri- studies were conducted in five mature mealybugs, which are wingless, emit a fos per acre, applied in February 2003 to Thompson Seedless vineyards that were sex pheromone to attract adult males, plots that had received 16 ounces imida- managed for raisin grapes and located which have wings. This pheromone has cloprid per acre in both April and June near Del Rey. Treatments were Anagyrus been identified (Hinkens et al. 2001), 2002; and (5) no-insecticide control plots release and a no-release control, with synthesized and successfully used in (same plots as in 2002). 1-acre treatment plots set in a random- monitoring programs (Millar et al. 2002; Because the 2002 plots were retreated, ized split plot design, and each vineyard Walton et al. 2004). The synthetic sex we conducted a more detailed spring serving as a replicate. Anagyrus were pheromone’s effectiveness and ability survey to determine if the preexisting provided by the Foothill Agricultural to be mass-produced led to our current mealybug density would affect the 2003 Research (FAR) Insectary. We released studies on mating disruption of the vine treatments. Mealybug density was deter- 10,000 Anagyrus per acre on June 12, mealybug. mined in March 2003 using a 5-minute July 3 and July 30, 2003, scheduled to oc- We conducted studies in 2003 that search on each of five randomly selected cur when the mealybugs were in exposed used a microencapsulated formulation of vines per plot (Geiger et al. 2001). To locations on the vine (e.g., on the leaves). the sex pheromone, applied to sections determine the treatment effect, crop Throughout the season, vine mealybug of five Thompson Seedless vineyards damage was evaluated at harvest, as de- density was determined by 5-minute located near Del Rey, Sanger and Fowler scribed previously. searches on each of 10 randomly selected (Fresno County). Treatments were phero- Natural enemy augmentation Selective insecticides, augmentation of natural enemies, and As an alternative to insecticides, we mating disruption programs could provide growers with investigated biological control of the vine mealybug. Natural enemies attacking the better tools to manage the vine mealybug. vine mealybug in California vineyards include the encyrtid parasitoids Anagyrus vines per treatment plot. Mealybug mone applications (mating disruption) pseudococci (Girault), Allotropa sp. and numbers were recorded by develop- and a no-pheromone control, with 3- to Leptomastidea abnormis (Girault); several ment stage (e.g., first, second or third 5-acre plots set in a randomized split species of green and brown lacewings; instar and adult). Parasitoid activ- plot design and each vineyard serving and coccinellid beetles, including the ity was evaluated by collecting 100 as a replicate. A 20- to 25-row buffer mealybug destroyer, Cryptolaemus mon- mealybugs from each treatment plot, (330 yards) was used between treatment trouzieri (Mulsant). Of these, Anagyrus is which were recorded by development plots. The sex pheromone used was the most effective natural enemy of the stage and location, categorized either produced by Kuraray (Tokyo, Japan) vine mealybug in the San Joaquin Valley; as “protected” (e.g., underground or and then microencapsulated by Suterra as many as 90% of the exposed mealy- under trunk bark) or “exposed” (e.g., on (Bend, Ore.). The pheromone was ap- bugs collected near harvest time were leaves or clusters). When possible, we plied using an air-blast spray rig at a parasitized (Daane, Malakar-Kuenen, et selected mealybugs in a one-to-one ratio rate of 0.282 ounces active ingredient in al. 2004). However, the parasitoid’s ef- from exposed and protected locations. 50 gallons of water per acre. Three ap- fectiveness is hampered by at least four The collected mealybugs were stored in plications were made in each field, with factors. First, from October to April vine gelatin capsules and held for parasitoid application dates between May 12 to 15, mealybugs reside primarily underneath emergence, and then percentage para- June 16 to 19, and Aug. 2 to 4. the bark, where they are protected from sitism and parasitoid species were re- Male mealybug flight was moni- foraging parasitoids. Second, Anagyrus corded. Crop damage was evaluated at tored using three Pherocon Delta IIID overwinter as immatures inside the harvest using the cluster rating system traps baited with sex pheromone lures mealybug and adults do not emerge (method described previously), with the (Suterra) in each treatment plot. Traps

http://CaliforniaAgriculture.ucop.edu • january–march 2006 33 and lures were changed every 2 and 4 nificantly less cluster damage than the weeks, respectively. Mealybug density control (fig. 1A). Average cluster dam- was determined using a 5-minute search age ratings in the April, May and April/ on each of 10 randomly selected vines per June imidacloprid treatments were treatment plot (method described previ- a significant 90.5%, 92.5% and 92.4% ously). Crop damage was evaluated at lower than in the control, respectively. harvest (method described previously), Average cluster damage in the June on 20 randomly selected vines per treat- imidacloprid treatment was a significant ment plot and five clusters per vine. 67.9% lower than in the control, but sig- The microencapsulated formulation nificantly higher than in imidacloprid starts emitting sex pheromone immedi- treatments applied earlier in the season. ately after application and its longevity In the furrow-irrigated vineyard, is dependent on temperature. To de- cluster damage ratings in all treatments termine the field longevity, samples of with imidacloprid were significantly pheromone-treated and clean (control) lower than the control (F = 221.58, df leaves were compared for their attrac- = 12, P < 0.0001); however, there was a tiveness to adult mealybug males. Ten greater separation of the imidacloprid leaves each were randomly sampled treatments (fig. 1B). Cluster damage from pheromone-treated and control in the May treatment was 59.3% lower vines at 1, 7, 14, 21, 28, 35 and 42 days than the control, and significantly lower after pheromone application. The leaves than all treatments. Meanwhile, the were placed individually on the sticky April and April/June treatments were surface of a pheromone trap, which was only 21.3% and 31.0% lower, respec- then placed 3.4 yards from a mealybug tively, than the control. The average colony. After 24 hours, the numbers of cluster damage rating in the June appli- Fig. 1. Percentage cluster damage ratings adult males in traps with treated or un- cation of imidacloprid was 14.8% lower for imidacloprid and control treatments in treated leaves were counted. than the control, but significantly higher (A) drip-irrigated and (B) furrow-irrigated than all other imidacloprid treatments. vineyard. Clean = no mealybug damage; Statistical analysis low = honeydew, indicating the presence The results show that imidacloprid of mealybugs; moderate = honeydew and For all of these studies (insecticides, provided the greatest reduction in clus- mealybugs present; severe = unmarketable. natural enemies and mating disruption), ter damage when applied in April or Different letters indicate significant difference the results are presented as means per May through a drip-irrigation system, among treatments (P < 0.01). treatment (± SEM). Treatment impacts and was less effective when delivered were compared using analysis of vari- through the furrow-irrigation system. is too little soil moisture, especially in ance (ANOVA), with the means sepa- We believe furrow-irrigated blocks have heavier soils with higher clay content. In rated using Tukey’s HSD test (P < 0.05) a more widespread root zone, which contrast, the insecticide may be flushed for three or more treatments or using a makes delivery of the insecticide to the too quickly through and out of the root t-test for two treatments. Treatment in- entire root zone difficult and results zone when too much water is applied in fluences on cluster damage, as measured in a more dilute application and poorer sandy soils. Once in the vine, imidaclo- by the rating scale, were compared in a uptake of the applied imidacloprid. prid must be delivered to sections where 2 × 2 contingency table with treatments Irrigation both pre- and post-imidacloprid the mealybugs are feeding. Because all separated using Pearson’s chi-square application is also critical, and this too vineyard mealybugs are phloem feeders, (P = 0.05). Differences among specific is more difficult to properly manipulate there will be sections of the vine where treatments were evaluated as a series of with furrow irrigation. the concentration and effectiveness of pairwise comparisons, adjusting the criti- It is important to note that these stud- systemic insecticides vary (for example, cal value using the standard Bonferroni ies were conducted in the San Joaquin the concentration of a systemically deliv- technique (P = 0.01). Repeated measures Valley on a sandy-loam soil; soil structure ered insecticide may be higher in canes ANOVA analyses were used to deter- may change the efficacy of systemically and lower in grape clusters). Researchers mine season-long differences in mealy- applied materials. Imidacloprid and other are currently investigating the uptake of bug densities, percentage parasitism and systemic chloronicotinyls are moved systemic chloronicotinyls in the vine (N. pheromone trap catches. with the irrigation water into the soil, Toscano, personal communication) and picked up by the vine’s root system, and this information, developed for glassy- Alternatives to organophosphates then moved through the vine in its xy- winged sharpshooter (Homalodisca coagu- Systemic insecticide. In the drip- lem. For this reason, proper delivery of lata [Say]), will greatly benefit mealybug irrigated vineyard, there was a signifi- imidacloprid may vary greatly among control strategies. cant treatment impact on cluster dam- vineyards depending on soil and vine Systemic vs. foliar insecticides. In age (F = 1085.4, df = 12, P < 0.0001). conditions. For example, there is evidence spring 2003, there were no significant All treatments receiving imidacloprid, that the insecticide can bind with soil pretreatment differences in mealybug regardless of application date, had sig- particles above the root zone when there densities among treatment plots in ei-

34 CALIFORNIA AGRICULTURE • VOLUME 60, NUMBER 1 ther the drip- or furrow-irrigated vine- yards (drip: F = 0.922; df = 4, 145; P = 0.453; or furrow: F = 1.518; df = 4, 145; P = 0.200). Therefore, treatment impact was not obscured by pretreatment dif- ferences resulting from the previous year’s insecticide application. In the drip-irrigated vineyard, there was a significant treatment impact on cluster damage ratings (F = 221.58, df = 12, P < 0.0001). Pairwise comparisons Fig. 2. Percentage cluster of the ratings for individual treatments damage ratings for insecticide and control were a significant 87.3%, 82.7% and treatments in (A) drip- 85.0% lower in the imidacloprid-2003, irrigated and (B) furrow- buprofezin and chlorpyrifos treatments, irrigated vineyard. respectively, as compared to the control Clean = no mealybug damage; low = honeydew, (fig. 2A). There was no difference be- indicating the presence of tween the imidacloprid-2002 application mealybugs; moderate = and the control. In the furrow-irrigated honeydew and mealybugs vineyard, there was a significant treat- present; severe = unmarketable. Different ment impact on cluster damage ratings letters indicate significant (F = 132.96, df = 12, P < 0.001) (fig. 2B). difference among The most effective treatments were treatments (P < 0.05). imidacloprid-2003 and buprofezin, where cluster damage was 70.7% and the vine mealybug population recov- (fig. 3). The average cluster damage 85.6% lower than the control, respec- ered in all imidacloprid treatment plots rating was 57% lower in the Anagyrus tively. There was a significant 44.1% between summer 2002 and spring 2003. release (0.22 ± 0.03) than in the control reduction in the chlorpyrifos treatment, This is presumably because imidacloprid (0.51 ± 0.05) treatment (t = 5.52; df = 1, whereas cluster damage in the imidaclo- cannot reach all parts of the vine, which 444; P < 0.001). However, we are unable prid-2002 treatment was not significantly leaves small pockets of mealybugs that to conclude that the released Anagyrus different from that in the control (fig. 2B). can recolonize. Currently, ongoing inves- were solely responsible for this reduc- The fact that there was no significant tigations are determining the movement tion. First, while there was no treatment difference between imidacloprid ap- and concentration of systemically ap- difference in vine mealybug density plied in 2002 and the control suggests plied nicotenoid compounds, like imida- on March 27 (t-test = 1.66, P = 0.101), that there was not an adequate year-to- cloprid, to different sections of the vine which was when the treatment plots year carryover of imidacloprid in the (personal communication, N.C. Toscano). were randomly assigned, there were soil or root systems for vine mealybug Buprofezin provided excellent control, fewer mealybugs on June 5 (t-test = control. The poor control achieved with comparable to both imidacloprid and 3.70, P < 0.001), which was just before chlorpyrifos in the furrow-irrigated chlorpyrifos, and can be used effectively in the Anagyrus release. Second, there was block may be due to the location of the vineyards with furrow-irrigation systems. no season-long difference in percentage vine mealybug population in this vine- We recommend that buprofezin be used parasitism (repeated measures ANOVA: yard, which had older vines (more than as an alternative to in-season organophos- F = 2.11; df = 1, 521; P = 0.15), although 30 years) that provided many protective phate treatments. Because buprofezin is an this is often an unreliable tool to mea- areas under the bark of the trunk and insect growth regulator, it is most effective sure the impact of natural enemies. spurs where mealybugs could remain on smaller mealybugs undergoing insect Nevertheless, the results provide hidden during much of the spring. molts. For this reason, it will have greater encouraging information for the com- Control programs. Imidacloprid pro- impact when applied earlier in the season, mercial use of Anagyrus to control vine vided the greatest reduction in cluster before the mealybug population has over- mealybug. From 7,458 mealybugs col- damage when applied in April or May lapping generations. It will be least effec- lected and held in gelatin capsules, 1,978 through a drip-irrigation system. We tive postharvest because late in the season were parasitized (26.5%) and 1,235 para- recommend that imidacloprid be applied (October and November) the development sitoids were reared to the adult stage. near 70% bloom, typically from late April of most mealybugs has slowed and the The parasitoids reared were Anagyrus, to mid-May. As noted, imidacloprid was population often consists primarily of L. abnormis, Allotropa sp. and Chartocerus less effective when delivered through adults and ovisacs. sp. (the Chartocerus is a hyperparasitoid, the furrow-irrigation system. Even when which is probably attacking Anagyrus). Parasitoids help control mealybug properly timed (May) and delivered Anagyrus was the dominant adult para- (pre- and postapplication irrigation), a The season-long mealybug density sitoid, comprising more than 93% of the single imidacloprid application did not was significantly lower in the Anagyrus total (table 1). Third-instar mealybugs locally extirpate vine mealybugs. In fact, release than in the control treatment were most commonly attacked, reflect-

http://CaliforniaAgriculture.ucop.edu • january–march 2006 35 Fig. 4. Season-long average (± SEM) percentage parasitism of settled (second instar to adult) vine mealybugs (MB), with data separated Fig. 3. Season-long average (± SEM) of settled (second instar by treatment and location where mealybugs were collected. Season- to adult) vine mealybugs was significantly lower in treatments long percentage parasitism was significantly higher in exposed than with Anagyrus pseudococci release, as compared to no- hidden locations for both control (repeated measures ANOVA: F = insecticide control plots (repeated measures ANOVA: F = 13.27; 247.3; df = 1, 273; P < 0.001) and release (repeated measures ANOVA: df = 1, 76; P < 0.001). F = 501.5; df = 1, 249; P < 0.001) treatments. ing the host preference of Anagyrus. (such as on the leaf). On the June 1 sam- vineyards near Del Rey. We are also Mealybug size affected the gender pling date, which was prior to Anagyrus enthusiastic about the commercial po- of the reared Anagyrus: first- and release, no mealybugs could be found in tential of Anagyrus and note the low second-instar mealybugs yielded pri- exposed locations. After releases began, rating for average cluster damage in the marily males (100% and 83.3% ± 1.1%, there was a significantly greater per- release treatment, which showed that an respectively), whereas third-instar centage parasitism of exposed mealy- average of 78% of all clusters were clean and adult mealybugs yielded primar- bugs in the release than in control plots and the remaining 22% had only minor ily females (95.4% ± 1.1% and 92.9% ± on the initial sample (fig. 4). Parasitism honeydew damage. 2.2%, respectively). rose steadily in both release and control The results of Anagyrus percent- Season-long percentage parasitism, plots because of the strong resident age parasitism and mealybug host with data separated by date and loca- population of Anagyrus in this untreated stage preference will also help de- tion of collected mealybugs, shows the field, reaching more than 80% by late velop future release strategies. For importance of timing augmentative August, after which we could find no example, most live mealybugs in the releases after mealybugs have moved live mealybugs in exposed locations. September and October samples were from protected locations (fig. 4). While Year-to-year declines. Resident found in protected locations of the the season-long percentage parasitism Anagyrus are providing significant re- vine, such as under the bark. These of mealybugs collected from protected ductions in late-season vine mealybugs, protected locations greatly reduce the locations (such as under bark) never which form the base for the following ability of foraging Anagyrus to locate exceeded 20%, there was a consistent season’s mealybug population. In fact, and parasitize vine mealybugs. We season-long rise in parasitism of mealy- we have recorded a year-to-year decline believe this results in lowered para- bugs collected from exposed locations in mealybug abundance in sampled sitism levels of the overwintering mealybug population, leading to the TABLE 1. Percentage parasitism and parasitoid species composition, observed low levels of Anagyrus the by vine mealybug development stage following spring (fig. 3). Furthermore, we reared primarily Parasitoid species male Anagyrus from first- and Mealybug Anagyrus Leptomastix development stage Parasitism pseudococci Allotropa sp. abnormis Chartocerus sp. second-instar mealybugs. These re- sults show that Anagyrus releases ...... % (± SEM)...... First instar 4.7 ± 0.5 97.2 ± 2.8 2.8 ± 2.8 0 0 should be timed to coincide not only Second instar 37.9 ± 0.9 89.0 ± 1.1 7.2 ± 0.9 2.3 ± 0.6 1.5 ± 0.4 with the presence of mealybugs in Third instar 53.2 ± 1.4 90.4 ± 1.3 7.6 ± 1.2 0.2 ± 0.2 1.8 ± 0.3 exposed locations, but also with the Adult 11.1 ± 0.8 93.0 ± 1.2 4.0 ± 1.2 0 3.0 ± 1.1 presence of third-instar mealybugs, Total 26.5 ± 0.5 92.1 ± 0.7 5.5 ± 0.6 0.7 ± 0.3 1.7 ± 0.3 which are needed to support the pro- duction of female Anagyrus.

36 CALIFORNIA AGRICULTURE • VOLUME 60, NUMBER 1 Fig. 5. Season-long average (± SEM) pheromone trap catches of Fig. 6. Season-long average (± SEM) of settled (second to adult adult male vine mealybugs in mating disruption and no-insecticide stage) vine mealybugs in mating disruption and no-insecticide control treatments were significantly different (repeated measures control treatments were not significantly different (repeated ANOVA: F = 15.27; df = 1, 6; P = 0.008). measures ANOVA: F = 1.85; df = 1, 77; P = 0.18).

bugs in the mating disruption plots. ing that a few years before there had been Mating disruption promising This increase in parasitism levels in nearly complete crop loss. We found that One of the five vineyard blocks was mating disruption plots has also been much of the mealybug reduction was partially treated with chlorpyrifos; this found in a recent South African study the result of natural parasitism levels by vineyard was removed from the data anal- (Walton and Daane, unpublished data). Anagyrus. Clearly, the mating disruption ysis and will be discussed separately. In Anagyrus may cue in on the mealybug program is quite compatible with biologi- the remaining four vineyards, season-long pheromone and either remain in the cal control. male mealybug trap catches were signifi- vineyard aggressively searching for Currently, we are testing mating cantly lower in the mating disruption treat- mealybug hosts, or be pulled in from disruption programs that deliver the ment than in the control (fig. 5). Essentially, nearby vineyards. pheromone either as a microencapsu- pheromone traps were “shut down” in the As mentioned previously, the cluster lated formulation (provided by Suterra) mating disruption treatment because the damage rating was lower in the mat- or in dispensers (provided by Suterra, vineyard was so inundated with sex pher- ing disruption plots. Nonetheless, our Shin-Etsu Chemical [Tokyo, Japan] and omone that the vine mealybug males could research suggests that mating disrup- Scentry Biologicals [Billings, Mont.]). not find the traps. More importantly, there tion may not be the most effective tool The advantages of the microencapsu- was a significant reduction in crop damage to quickly lower high-density mealybug lated formulation include application in the mating disruption treatment (t-test: populations. First, mating disruption using standard pesticide rigs, the dis- t = 5.76, P < 0.001), with most of the clus- works more slowly because it prevents persion of millions of microcapsules per ters rated 0, or clean, and hardly any rated the next generation from forming rather acre to provide thorough coverage, and 3, or unmarketable (90.5% ± 1.5% and 1.2% than killing the mealybugs already pres- numerous point sources on each vine. ± 0.2%, respectively). ent. Second, mealybug density appears to One disadvantage, found in the 2003 However, while crop damage was influence the effectiveness of vine mealy- study, is that pheromone activity was lower, season-long mealybug densi- bug mating disruption. depleted after only 21 days; therefore, ties were not significantly different In our trials, the overall level of crop multiple applications per season are re- between the pheromone and control damage was low even in the control treat- quired. However, the longevity of prod- treatments (fig. 6). We believe that ment, with about 80% of the clusters clean uct delivery (either in microcapsules or this may be explained by differences (rated 0 or 1). This was in part by design, dispensers) is a technical problem that in mealybug location on the vine. For as earlier studies with mating disruption may be solved in product formulation. example, in the pheromone-treated in heavily infested vineyards showed no The advantages of dispensers are that plots, most live mealybugs were found treatment effect (Walton and Daane, un- they can be applied by hand, have the under the bark on the trunk, while in published data). We suspect that this may potential for longer activity (and so one the control they were under the bark, be due to the fact that at high mealybug or two applications per season), and and exposed in leaves and clusters. We densities, adult males would emerge in have the potential for use in California believe the between-treatment differ- close proximity to females. Therefore, for certified organic farms. ence in mealybug location results from these trials we selected vineyards with Sustainable pest treatments a beneficial artifact of the mating dis- initially low or moderate mealybug densi- ruption: we consistently found higher ties. Still, there was even less damage in The vine mealybug is a serious pest parasitism rates of the exposed mealy- these vineyards than expected, consider- that is here to stay. Along with its po-

http://CaliforniaAgriculture.ucop.edu • january–march 2006 37 Left to right, Jose Tinoco places a pheromone trap; Raksha Malakar-Kuenen, a postdoctoral researcher, samples for mealybugs; UC Riverside entomologist Jocelyn Millar and colleagues synthesized a vine mealybug sex pheromone, which has allowed for more effective monitoring.

gyrus pseudococci (: ) tential for damaging vines and reducing regions may have compliance agreements as a parasitoid of the vine mealybug, Plano- marketable yields, it often requires the in place for required treatments; growers coccus ficus (Homoptera: Pseudococcidae). considerable use of insecticides. While should contact their local UC Cooperative Biol Cont 31:123–32. properly timed insecticide applications Extension or county agricultural commis- Daane KM, Sime KR, Cooper ML, Battany MC. 2004. Ants in your vineyard? UC Plant provide excellent control, their increased sioner’s office for information. Prot Quarterly 11(2):1–3. use runs counter to the grape industry’s Flaherty DL, Christensen LP, Lanini WT. move toward sustainable farming methods. 1992. Mealybugs. In: Flaherty DL, et al. (eds.). Grape Pest Management. ANR Pub 3343, Presently, organophosphates, nicoti- Oakland, CA. p 159–65. noids (imidacloprid) and insect growth K.M. Daane is Associate UC Cooperative Geiger CA, Daane KM. 2001. Seasonal regulators (buprofezin) are being used Extension (UCCE) Specialist, Division of movement and sampling of the grape in vine mealybug control programs. Insect Biology, UC Berkeley; W.J. Bentley is mealybug, Pseudococcus maritimus (Eh- rhorn) (Homoptera: Pseudococcidae), in San Selection of the proper material or com- Areawide Entomologist, UC Statewide IPM Joaquin Valley vineyards. J Econ Entomol bination will depend on the time of year, Program; V.M. Walton and R. Malakar- 94:291–301. mealybug density and vineyard condi- Kuenen are Postgraduate Researchers, Geiger CA, Daane KM, Bentley WJ. 2001. tion (for example, imidacloprid may Division of Insect Biology, UC Berkeley; Development of a sampling program for im- proved management of the grape mealybug. work best on sandy-loam soils). Selective J.G. Millar is Professor, Department of Cal Ag 55(3):19–27. insecticides, augmentation of natural en- Entomology, UC Riverside; C.A. Ingels is Gill R. 1994. Vine mealybug. California emies and mating disruption programs Farm Advisor, UCCE Sacramento County; Plant Pest and Disease Report, Jan–June, 8. California Department of Food and Agricul- could provide growers with better tools E.A. Weber is Viticulture Farm Advisor, ture, Sacramento, CA. to manage the vine mealybug. UCCE Napa County; and C. Gispert is Godfrey K, Ball J, Gonzalez D, Reeves Nevertheless, continued vigilance Viticulture Farm Advisor, UCCE Riverside E. 2003. Biology of the vine mealybug in is needed to reduce populations and County. We thank the California Table vineyards in the Coachella Valley, California. Southwest Entomol 28:183–96. limit the pest’s further spread. Growers Grape Commission, California Raisin Mar- Godfrey KE, Daane KM, Bentley WJ, et al. should train all their workers in mealy- keting Board, American Vineyard Founda- 2002. Mealybugs in California vineyards. ANR bug identification and react quickly to tion, UC Statewide IPM Program and the Pub 21612, Oakland, CA. 4 p. USDA Western Regional IPM Program for Golino DA, Sim S, Rill R, Rowhani A. any new finds. Managers of infested 1999. Four species of California mealybugs blocks should follow all the recom- funding. Farm managers at the Chooljian can transmit leafroll disease. Am J Enol mended treatment protocols (www. Brothers and Carolyn Chooljian provided Viticul 50:367–8. ipm.ucdavis.edu/PMG/r302301911. field sites and helped coordinate field ac- Hinkens DM, McElfresh JS, Millar JG. 2001. Identification and synthesis of the sex attrac- html), and manage their equipment and tivities. Lee Marvin and Glenn Yokota co- tant pheromone of the vine mealybug, Plano- workforce to minimize this pest’s spread. coordinated all field trials. Jose Tinoco, coccus ficus. Tetrahedron Letters 42:1619–21. Wineries should be aware of the status of Rodney Yokota, Johnny Sanchez, Gary Millar JG, Daane KM, McElfresh JS, et vineyards delivering fruit and take steps Guelce and Susan Malek provided labora- al. 2002. Development and optimization of methods for using sex pheromone for to properly dispose of stems coming tory and field assistance. monitoring the mealybug Planococcus ficus from infested blocks. Grapevine nurser- (Homoptera: Pseudococcidae) in California References ies should implement quality-assurance vineyards. J Econ Entomol 95:706–14. Bentley WJ, Zalom FG, Garnett J, et al. Walton VM, Daane KM, Pringle KL. 2004. measures to prevent the vine mealybug’s 2003. and mites. UC Pest Management Utilizing the sex pheromone of Planococcus further spread on plant materials. Guidelines. ANR Pub 3448, Oakland, CA. 85 p. ficus to improve pest management in South By implementing appropriate control Daane KM, Bentley WJ, Weber EA. 2004. African vineyards. Crop Prot 23:1089–96. measures, the overall impact and dis- Vine mealybug: A formidable pest spreads Walton VM, Pringle KL. 1999. Effects of throughout California vineyards. Practical pesticides used on table grapes on the mealy- semination of the vine mealybug will be Winery Vineyard 3:35–40. bug parasitoid Coccidoxenoides peregrinus reduced. Different regions vary in levels Daane KM, Malakar-Kuenen RD, Walton (Timberlake) (Hymenoptera: Encyrtidae). So of vine mealybug infestation, and some VM. 2004. Temperature development of Ana- Afr J Enol Viticul 20:31–4.

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