Research Article t New navel orangeworm sanitation standards could reduce almond damage

by Bradley S. Higbee and Joel P. Siegel

The navel orangeworm (NOW), a pri- mary pest of almonds and pistachios in California, is controlled in part by sanitation, with a current threshold of two mummy nuts or fewer per tree. However, almond and pistachio acreage has increased dramatically since the tree mummy threshold was established. This study addresses the impact of this expansion and the possible need for a more stringent standard. Beginning in 2002, the Paramount Farming Company con- ducted a series of large-scale studies reevaluating the current tree mummy threshold in almond orchards, as well Sanitation practices in almond orchards can have a significant impact on insect pest damage. Almond “mummies” remaining on the tree after harvest provide overwintering sites for navel as the impact of ground mummies orangeworm, which then infests the new crop. and proximity to pistachio orchards. The data supports a more stringent prises almost all pistachio plantings Zalom, personal communication). By threshold of 0.2 mummies per tree. In in California (see page 18). From 2003 the late 1980s, average damage in al- addition, a new threshold for ground to 2007, there has been unprecedented monds was reduced to approximately expansion in the acreage of both crops: 4%, due to the efforts of researchers mummies of four per tree for ‘Non- 30% for almond and 31% for pistachio. at the U.S. Department of Agriculture pareil’ almonds is supported in Kern In 2005, the combined farm-gate (USDA) (Curtis 1979) and the University County, although this needs to be value of almonds and pistachios was of California (Engle and Barnes 1983; approximately $2.9 billion, according Zalom et al. 1984). validated in other regions. Proximity to the Almond Board of California. This reduction in navel orangeworm to pistachios was an important risk These crops contribute substantially damage was accomplished via a mas- factor for navel orangeworm damage to the U.S. export balance of trade. sive commitment to orchard sanitation, of 2% or less in almonds. Likewise, Approximately 67% of the almond (ABC using a threshold of no more than two 2006) and 49% of the pistachio crop unharvested (mummy) nuts remaining the influence of pistachios extended was exported in 2005, according to the in each tree, along with early harvest of 3 miles from the center of the 10-acre California Pistachio Industry Annual the ‘Nonpareil’ crop and on-farm fumi- almond orchard sections in our exper- Report. Kern County had the single gation with insecticides after harvest iments to the margin of the nearest greatest concentration of both crops in (UC IPM Online 2007). These practices 2005, with 20% of total standing almond lowered damage by both reducing navel pistachio orchard. acres (131,400) and 31.9% of total stand- orangeworm populations and remov- ing pistachio acres (48,770) (NASS 2006). ing nuts before they could become in- lmond and pistachio plantings Navel orangeworm (NOW), Amyelois fested by the large populations of navel comprise more than 880,000 acres transitella Walker (Wade 1961), is the orangeworm that occur from August inA the Central Valley (NASS 2006). Al- major pest of almonds and pistachios through September. monds account for about 83% and pis- in California, and direct damage by While the 4% damage level was satis- tachios for about 17% of these plantings this insect can exceed 30% in both factory for approximately 20 years, both (730,000 and 153,000 acres, respectively). crops. During the late 1970s through food-quality standards and commodity ‘Nonpareil’ is the most popular almond the early 1980s, navel orangeworm values are dynamic, and today there is variety, comprising 37.7% of all stand- devastated the almond crop, causing even less tolerance for damage. Since ing acreage in 2006, and ‘Kerman’ com- average damage of 8.8% in 1978 (F.G. 2002, the almond industry’s average

24 CALIFORNIA AGRICULTURE • VOLUME 63, NUMBER 1 Jack Kelly Clark Kelly Jack

Navel orangeworm control can be achieved in almonds by careful orchard sanitation, early harvest of the ‘Nonpareil’ variety and postharvest fumigation with insecticides. Clockwise from top left: a navel orangeworm adult; a fertile navel orangeworm egg laid on a mummy almond; a hatched egg; and an almond mummy infested with navel orangeworm larvae.

damage goal for navel orangeworm has pooled data from 2003 through 2006, rows (four ‘Nonpareil’ trees and four been 2% or less. Factors contributing we report on how ‘Nonpareil’ kernel pollinizer trees) in each 10-acre sec- to this current threshold include the damage is affected by numbers of both tion. (Almonds are not self-compatible crop’s increased value and the associa- tree and ground mummies, as well as and in order to achieve maximum tion of kernel damage by navel orange- proximity to pistachios. yield, ‘Nonpareil’ must be pollinated worm with aflatoxin contamination, by varieties other than itself. As a Post-sanitation studies a major quality concern (Schatzki and consequence, any block of almonds Ong 2001; ABC 2006). In addition, the Between December 2002 and contains at least two different variet- European Union — the largest market February 2006, a series of long-term, ies.) Separate counts were made of nuts for California almonds — has imposed labor-intensive studies on mummy on the ground and those remaining more-stringent import standards abundance following sanitation was in the trees. All of the fallen nuts from that have lowered the allowable level conducted in ranches belonging to all outside the drip line (or berm) between of aflatoxin B1 to 2 parts per billion divisions of the Paramount Farming the eight trees were counted, and (OJEU 2007). Company in Kern County. More than nuts in the trees were knocked down In order to reduce navel orange- 50 ranches were divided into 160-acre with bamboo poles (poling) and then worm damage and increase almond blocks, which were then subdivided counted. The average number of mum- quality, the Paramount Farming into 40-acre plots, which in turn were mies per tree was calculated for both Company initiated research in Kern quartered into the 10-acre sections com- fallen nuts and nuts remaining in the County in 2002 to evaluate the complex prising our sample units. tree for every year of our study. A total interactions between current sanita- Abundance of mummies. Between of 1,920 sections was used in this analy- tion practices, orchard damage history January and mid-February, 2003 sis, corresponding to 19,200 acres and and proximity to an alternate navel through 2006, we selected four adjacent 15,360 trees. In 2003 and 2004, all these orangeworm host (pistachios). Using trees from each of two consecutive mummies were collected and dissected,

http://CaliforniaAgriculture.ucop.edu • January–March 2009 25 and data for the 2 years were pooled In order to properly sanitize mies (0.23, P < 0.00001). There was a (233,821 ground mummies and 7,371 an almond orchard in Kern negative correlation between navel or- tree mummies). angeworm damage and distance to the Damage to kernels. In August and County, it is essential to pistachio margin (−0.29, P < 0.00001), early September, 2003 through 2006, remove mummies from the indicating that damage decreased with within 5 days of harvest, samples of 1,500 trees and destroy them on distance. Tree and ground mummies to 2,000 nuts were collected from these were moderately correlated (0.39, same 10-acre sections by walking a di- the ground. P < 0.00001), indicating that when tree agonal transect and taking 50 to 100 nuts mummies were high in a section so at intervals of approximately 100 feet. A were ground mummies, but there was total of 2,596,008 kernels was obtained tion [SD]) and the range was 0 to 69.7 considerable variation. Both tree and by a combination of hand-cracking and a per tree, while the average number of ground mummies were negatively cor- small hulling and shelling machine. All ground mummies was 5.0 (± 5.3 SD) related with distance to the pistachio kernels were examined using a lighted and the range was 0 to 43.7 per tree. In margin (−0.09, P < 0.0001; −0.06, P < 3× magnifier, by personnel trained to the pooled dataset for 2003 and 2004, 0.005 respectively). These marginal identify common insect and cultural de- 13.64% of tree mummies and 7.91% correlations are statistically significant fects. On several occasions, subsamples of ground mummies collected were due to the large sample size, and they were sent to a Paramount processing infested with navel orangeworm. The indicate that there was a slight ten- plant for independent grading, and the relative risk for tree-mummy compared dency for fewer mummies to be recov- processor grades were in agreement to ground-mummy infestation was 1.72 ered closer to the pistachio margins. with the laboratory grades. (Chi square = 277, P < 0.0001), indicating Mummies and new crop damage Damage to kernels was scored and that tree mummies were 1.72 times as descriptive statistics including mean, likely to be infested as ground mum- Tree mummies. Damage in the new standard deviation and pairwise cor- mies. This infestation disparity is likely crop exceeded the 2% threshold when relations were calculated using JMP due to differential mortality between there were 0.7 mummies or more per software (v. 7.0.1, SAS Institute, Cary, navel orangeworm in trees and on the tree in the winter (table 2), a reduction NC). In addition, relative risk, a statistic ground, but we did not specifically of 65% from the current guideline. commonly used in epidemiology to address this in our study. A similar However, further relative risk analysis evaluate the likelihood of a dichoto- pattern exists in pistachios collected supports a more stringent threshold of mous outcome (one of two outcomes; in February (Siegel et al. 2008), but the 0.2 mummies per tree. When sections in this study the outcome of interest study did not specifically determine containing 0.2 or more mummies per was damage of at least 2%) was used to causes of mortality. The average dis- tree were compared to sections that compare damage differences between tance from the center of the almond had fewer than 0.2 mummies per tree, the tree and ground mummies, and to sections to the margin of the closest pis- the relative risk was 2.15 (Chi square assess differences in kernel damage tachio block was 8,600 feet (1.6 miles). = 156, P < 0.0001), indicating that they by rounding the navel orangeworm In this study, the average kernel dam- were 2.15 times as likely to have kernel damage to the nearest tenth and then age per sample due to navel orangeworm damage equal to or exceeding the 2% contrasting all sections with damage of was 1.6% (± 2.3% SD) and the range was threshold. In addition, other factors 2% or more with sections that had dam- 0 to 20.8%. The standard deviation was beside the number of tree mummies age below this level (Kelsey et al. 1986). greater than the means for mummies Distance in feet was calculated from and kernel damage due to the inclusion the center of each almond section to the of sections with no navel orangeworm TABLE 2. Relationship between average numbers margin of the nearest pistachio block damage and/or no mummies. of tree and ground mummies per tree and using ArcMap (ESRI, Redlands, CA) The correlations among these vari- ‘Nonpareil’ kernel damage by navel orangeworm, and the Paramount Farming Company ables using the parametric statistic, 2003–2006 GIS mapping database. Pearson product moment coefficient (r), Tree mummies Damage Sections are summarized in table 1. Tree mum- Damage higher in tree mummies avg. no./tree % no. mies were the most strongly correlated 0 1.63 605 The average number of tree mum- with navel orangeworm damage (0.46, 0.01–0.49 1.22 1,092 mies was 0.7 (± 5.0 standard devia- P < 0.00001), followed by ground mum- 0.5–0.69 1.57 91 0.7–0.79 2.32 39 0.8–1.75 3.53 61 TABLE 1. Correlations among ‘Nonpareil’ kernel damage by navel orangeworm (NOW), ≥ 1.76 7.85 44 mummies per tree and distance to nearest pistachio margin, 2003–2006 Ground mummies avg. no./tree % no. NOW damage Tree mummies Ground mummies Distance 0–4.9 1.39 1,272 NOW damage 1.00 0.46 0.23 −0.29 4.91–7.9 1.57 300 Tree mummies 0.46 1.00 0.39 −0.09 7.91–8.9 1.72 67 Ground mummies 0.23 0.39 1.00 −0.06 8.91–9.0 2.78 44 Distance −0.29 −0.09 −0.06 1.00 ≥ 9.1 2.72 238

26 CALIFORNIA AGRICULTURE • VOLUME 63, NUMBER 1 clearly influence navel orangeworm and 15,000 feet (table damage, because in the sections that 3). Navel orangeworm 20 lacked tree mummies, the average ker- damage was highest in nel damage was 1.6%. the almond sections that Ground mummies. In this study, were 0.25 mile or less 15 the number of ground mummies per from pistachios; there tree was also related to damage in were 87 sections in this the new crop (table 2). We found that class and 55.2% of them kernel damage exceeded the current had damage of 2% or 10 guideline of 2% when there were 8.9 or more. At a distance of Damage (%) more ground mummies per tree. Use 3 miles or more from of the statistic relative risk indicated pistachios, there were 5 that a more stringent threshold of four 1,752 almond sections ground mummies per tree is justified, and 26.7% of them had because sections containing four or damage of 2% or more. 0 more mummies were 1.34 times more In contrast to sections likely to have kernel damage exceed- inside the 3-mile limit, 0 10,000 20,000 ing the 2% threshold than sections those beyond 3 miles Distance (feet) with fewer than four mummies on the (15,840 feet) were 25% to Fig. 1. Relationship between percent navel orangeworm ground (Chi square = 13.6, P < 0.0001). 50% less likely to have damage and distance (feet) from center of almond block to There is currently no established damage that exceeded nearest pistachio margin. threshold for ground mummies. We the 2% threshold (data suggest using an average of four not shown). ground mummies per tree for Kern there is a potential load of 1,200,000 Reducing NOW damage to 2% County. We did not establish causal- to 1,800,000 almonds per acre before ity in this study, and mummies on the Mummy abundance. In order to harvest. Harvest operations and sub- ground may harbor the overwintering meet a new threshold of 2% or less sequent sanitation must remove or navel orangeworm population, serve kernel damage in Kern County, the destroy 99.965% to 99.977% of these as a host for the first generation of the average number of mummies should nuts in order to successfully meet the new crop year, or both. What is clear be reduced to 0.2 per tree, and an ad- challenge of sanitation to ensure 2% is that mummies on the ground were ditional threshold should be established or less kernel damage. Using these more than 36 times as prevalent as of four ground mummies per tree after estimates, our current average sanita- mummies in trees in the pooled data- mummy destruction by flail mowing. In tion efficiency ranged from 99.953% to set for 2003-2004, and these ground a 100-tree planting per acre, these new 99.969%. Economic analysis is needed mummies may contribute to navel or- standards correspond to 20 tree mum- to establish a cost-benefit relationship angeworm damage due to their abun- mies and 400 ground mummies per between more stringent sanitation dance. In order to properly sanitize an acre, leaving an acceptable total of 420 and economic return, in order to en- almond orchard in Kern County, it is or more nuts per acre. able growers to determine the optimal essential to remove mummies from the Sanitation. Assuming that an av- amount of resources to devote to these trees and destroy them on the ground. erage ‘Nonpareil’ almond tree in a practices. 1-acre planting bears between 12,000 Pistachio proximity. Pistachios as Proximity to pistachio and 18,000 nuts (UC 2006), and that far away as 3 miles from the center of Damage caused by navel orange- the accompanying pollinizer variet- almond blocks may contribute to navel worm decreased as distance to the ies bear the same number of nuts, orangeworm damage. Further research nearest pistachio margin increased (fig. 1). The best fit was obtained using TABLE 3. Relationship between ‘Nonpareil’ kernel damage by navel orangeworm this quadratic equation: % ‘Nonpareil’ and distance to nearest pistachio margin, 2004–2006 kernel damage = 0.0265156 − 0.0000016 × distance + 0.00000000013 × (distance Distance Relative risk* Damage ≥ 2% Sections − 8,889.8)2. miles % no. Although this equation is statisti- ≤ 0.25 2.27† 55.2 87 cally significant F( ratio 112.3, P < ≤ 0.50 2.15† 48.5 233 2 ≤ 1.00 2.61† 45.2 577 0.0001, r = 0.105) it does not account ≤ 1.50 3.29† 39.4 961 for most of the variation, confirming ≤ 2.00 3.14† 33.6 1,258 that other factors also play a role in ≤ 2.50 2.18† 28.6 1,562 navel orangeworm damage. The rela- ≤ 3.00 1.66‡ 26.7 1,752 tionship between damage and pista- * Relative risk values > 1 indicate increased likelihood of navel orangeworm damage ≥ 2%. chio proximity declined with distance † P < 0.0001. ‡ 0.005 > P > 0.001. and ceased somewhere between 14,000

http://CaliforniaAgriculture.ucop.edu • January–March 2009 27 is needed to develop a coordinated staff of the Entomology Laboratory at Paramount ▲ A large-scale study in Kern County strategy for managing this pest in both Farming Company, particularly Lori Smith and almond orchards found that navel orangeworm damage to nuts can be crops, as well as to determine whether Mike Bryant, for technical assistance and gather- brought below 2% by reducing the additional measures are necessary to ing the tremendous amount of data required for average number of mummies per tree manage almonds in proximity to pis- this study. We also thank Scott Guseman and to 0.2 or fewer, and the average number Lyndi Smith for their assistance with data manage- of ground mummies to four or fewer tachios. Initial studies on the extent of per tree. By the time trees bloom in the navel orangeworm movement between ment and Gary Schengel for his invaluable help in spring, sanitation should be complete, almonds and pistachios indicate that in mapping the orchards. We thank Lawrence Lacey since it is difficult to perform once new pistachios, male navel orangeworm can and Joseph Smilanick for their constructive com- growth appears. move up to 1,100 yards in 1 day while ments on the manuscript. females moved up to 100 yards in 1 day (Burks and Higbee 2006). Conditions vary throughout the products originating in the United States. Doc no. References C(2007) 3613; Aug. 18, 2007. 3 p. growing regions of the Central Valley [ABC] Almond Board of California. 2006. Orchard and there are likely to be differences sanitation and navel orangeworm control. Fact Schatzki TF, Ong MS. 2001. Dependence of aflatox- that influence the factors identified in sheet. Modesto, CA. 1 p. http://almondboard.com. ins in almonds on the type and amount of insect damage. J Ag Food Chem 49:4513–9. the Kern County study. Therefore it is Burks CS, Higbee BS. 2006. NOW mating disruption, essential to validate these findings in dispersal and damage prediction. Proc 34th Annual Siegel JP, Kuenen LPS, Higbee BS, et al. 2008. Post- Almond Industry Conf. Modesto, CA. p 1–19. harvest survival of navel orangeworm assessed in other Central Valley areas. Collaborative pistachios. Cal Ag 62:30–5. studies between USDA, UC, UCCE and Curtis CD. 1979. Implementing orchard cleanup. Almond Facts 44:20–1. [UC] University of California. 2006. Regional almond Paramount Farming Company research- variety trials planted in 1993 progress report. UC Co- ers are under way as part of a newly Engle CE, Barnes MM. 1983. Cultural control of operative Extension and UC Davis. 26 p. navel orangeworm in almond orchards. Cal Ag established areawide program for the 37(9-10):19. UC IPM Online. 2007. UC Pest Management control of navel orangeworm in al- Guidelines; Almond; Navel Orangeworm. www.ipm. monds, pistachios and walnuts. Kelsey JL, Thompson WD, Evans AS. 1986. Methods ucdavis.edu/PMG/r3300311.html (accessed October in Observational Epidemiology. New York: Oxford 2007). Univ Pr. 366 p. Wade WH. 1961. Biology of the navel orangeworm, [NASS] National Agricultural Statistics Service. 2006. Paramyelois transitella (Walker), on almonds and 2005 Almond Acreage Report. US Department of walnuts in northern California. Hilgardia 31:129–71. B.S. Higbee is Research Entomologist, Paramount Agriculture. Sacramento, CA. 8 p. www.nass.usda. Farming Company, Bakersfield; and J.P. Siegel gov. Zalom FG, Barnett WW, Weakley CV. 1984. Efficacy of winter sanitation for managing the navel orange- is Research Entomologist, USDA Agricultural [OJEU] Official Journal of the European Union. 2007. worm, Paramyelois transitella (Walker), in California Research Service, San Joaquin Valley Agricultural Commission decision on aflatoxin contamination on almond orchards. Prot Ecol 7:37–41. Sciences Center, Parlier. The authors thank the

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