Protracted Emergence of Overwintering Amyelois transitella (: ) from and in California Author(s): L.P.S. Kuenen and J. P. Siegel Source: Environmental Entomology, 39(4):1059-1067. 2010. Published By: Entomological Society of America DOI: 10.1603/EN09277 URL: http://www.bioone.org/doi/full/10.1603/EN09277

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. POPULATION ECOLOGY Protracted Emergence of Overwintering Amyelois transitella (Lepidoptera: Pyralidae) From Pistachios and Almonds in California

1 L.P.S. KUENEN AND J. P. SIEGEL

United States Department of AgricultureÐAgricultural Research Service, San Joaquin Valley Agricultural Sciences Center, 9611 South Riverbend Avenue, Parlier, CA 93648

Environ. Entomol. 39(4): 1059Ð1067 (2010); DOI: 10.1603/EN09277 ABSTRACT The navel orangeworm, Amyelois transitella (Walker), is the primary pest of pistachios and almonds in California. Four years of research (2002Ð2006) were conducted in Madera and Kern Counties to elucidate the pattern of adult emergence of the overwintering navel orange- worm population. Springtime emergence from unharvested (mummy) nuts was protracted (600 degree-days or more from 1 January of each year) and in 2004 and 2006 extended to mid-July. The population structure, sex ratio, and timing of emergence differed between and mummies. Pistachio populations had a signiÞcantly greater proportion of late stage individuals compared with almond mummies, 85.7 versus 34.1%. The sex ratio of adults emerging from pistachio mummies was signiÞcantly skewed with a ratio 57:43 male:female compared with 50:50 in almond mummies. Emergence from mummies held outdoors (variable temperature) began in early March and continued through early June in both pistachio mummies and almond mummies. The adult emergence pattern from pistachio mummies contained a single emergence peak, whereas emergence from almond mummies occurred in multiple peaks. These same patterns occurred when mummies were held at constant temperature, and the emergence peak from pistachio mummies occurred sooner. The impact of these Þndings on understanding navel orangeworm population dynamics and current control recommendations is discussed.

KEY WORDS navel orangeworm, pistachios, almonds, overwintering emergence, sex ratio

The navel orangeworm (Amyelois transitella Walker), (Engle and Barnes 1983a, Sanderson et al. 1989a). Þrst found in the United States on navel oranges in Adults emerge from the mummies on the ground and Arizona (Mote 1922), is a multivoltine scavenger on in the trees, and females lay their eggs on other mum- fallen or damaged fruits, and infests sound nuts when mies or new crop nuts when available to continue their their hulls have split. Since its appearance in Califor- life cycle. Adults that subsequently emerge from these niaÕs Central Valley in the late 1940s (Wade 1961), mummies oviposit on the new crop when available, or commercially grown almonds, Þgs, pistachios, and remaining mummies (Sanderson et al. 1989a). In sub- walnuts have been infested by navel orangeworm, and sequent ßights, females oviposit on new crop nuts this moth is currently the primary pest of pistachios (or on mummy nuts remaining on the trees or and almonds in California. Over the period 1995Ð2004, ground), and oviposition continues through Novem- there was a dramatic expansion of both pistachio and ber (Kuenen and Rowe 2003). The timing of almond almond plantings (54 and 31%, respectively), and cur- susceptibility depends on variety, and new crop Non- rently there are over 251,000 ha of almonds and 50,000 pareil almonds, the most common variety grown, are ha of pistachios in California (Anonymous 2005). The susceptible to infestation when the hulls split and value and importance of these crops have substantially expose the nuts, typically beginning during late June increased (Ϸ2.92 billion dollars combined in 2005), or early July (Kuenen and Barnes 1981). Development and concurrent with this rise in value there is an on new crop almonds is faster than on mummy al- increased demand to reduce navel orangeworm dam- monds (Seaman and Barnes 1984, Sanderson et al. age below current levels. 1989b), and the adults that emerge may infest more The navel orangeworm overwinters in the previous almonds before harvest, depending on variety and seasonÕs crop residue (mummies) as larvae or pupae harvest date. In contrast to almonds, the pistachio shell without apparent diapause. Development occurs spo- opens inside the intact hull; therefore, most pistachios radically through the winter and spring whenever are not susceptible to navel orangeworm infestation temperatures exceed the lower threshold of 12.8ЊC until their hulls split, typically starting in late August to early September (Beede et al. 1984). However, a 1 Corresponding author, e-mail: [email protected]. small fraction of the pistachio crop known as early 1060 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 4 splits becomes vulnerable to infestation by early Au- both the ground adjacent to the trunks (berm) and the gust, because both hull and shell split together, ex- canopy in early January, and almond mummies were posing the kernel (Doster and Michailides 1995). In collected from the ground the same week. Plant debris addition, there are numerous small pistachios that we was removed, and enough mummies were saved to Þll call pea-split nuts. These nuts are approximately the emergence cages (below). A total of 8,600 and 6,400 size of green peas (4Ð8 mm diameter) and have in- pistachio mummies was pooled and used to assess completely formed shells, such that they can readily navel orangeworm emergence in 2002Ð2003 and 2003Ð pop open from internal or external pressure. We have 2004, respectively, and 1,100 and 1,000 almond mum- found that pea-split nuts often split in late June or July mies were used in 2002Ð2003 and 2003Ð2004, respec- apparently from high heat or later as the nut meats tively. For the constant temperature regime, we used grow, and thus provide an even earlier new crop food 30,000 pistachio mummies collected from berms and source for navel orangeworm. 9,250 mummies collected from trees in December To reduce the levels of overwintering navel orange- 2004, in Madera County, and in January 2006, we used worm, orchard sanitation is recommended for navel pistachio mummies collected from the berm and trees orangeworm during the winter months because it both in Madera and Kern Counties (50,000 and 30,000, destroys the overwintering population and reduces respectively), and almond mummies collected from the resources available for the Þrst ßight of navel the ground in Madera and Kern Counties (25,895 and orangeworm (Curtis 1976, Engle and Barnes 1983b, 16,765, respectively). also Sibbett and Van Steenwyk 1993). This cultural Variable Temperature Exposure. In 2002 and 2003, practice in almonds consists of shaking mummies from pistachio and almond mummies were held outdoors the trees after attachment has been weakened by Ϸ60 cm above the ground on wooden frames covered winter rain and fog, and then destroying the mummies with hardware cloth (0.64-cm mesh). These frames on the ground by ßailing before mid-February (Bent- were fully exposed to ambient light, temperature, rain, ley et al. 2002). In pistachios, cultural control consists and fog. In early March, mummies were transferred of blowing fallen mummy nuts off the berm (under (one-layer deep) to aluminum-framed cages with certain circumstances the mummies may also be window-screen sides and a sleeve opening on one side. knocked off the tree after attachment to the rachis is These cages were held on the same wooden frames weakened by rain and fog) and disking the mummies and moved to the north side of a water tower, where into the soil of the drive rows (Bentley et al. 2008). they were sheltered from direct sunlight for Յone- These practices are not 100% efÞcient, and insecti- third of the photoperiod to mimic partial exposure to cides are used to protect these crops because the sunlight in an orchard; however, no other protection population of navel orangeworm increases during the from the elements was provided. Adults were col- summer and the acceptable percentage of damaged lected twice weekly, and their emergence date was nuts is low in both crops. recorded until no moths were collected for 2 wk. All Missing from this view of navel orangeworm biology adults were frozen, and their sex was subsequently is the progression of navel orangeworm emergence determined by examination of their genitalia under a from mummies, and our goal in conducting this re- dissecting microscope. search was to quantify the emergence patterns from Constant Temperature Exposure. In these experi- pistachio and almond mummies, and to determine ments conducted in 2004Ð2005 and 2006, pistachio and whether females from the overwintering population almond mummies were placed in 18.9-liter plastic (Þrst ßight) can oviposit on new crop nuts. In this buckets covered with screens and held at 26.7ЊC, and study, we present data on the overwintering popula- emergence was monitored weekly, as described by tion structure, sex ratio in adults emerging from pis- Siegel et al. (2008). All adults were counted and placed tachio and almond mummies, and emergence pattern in 50-ml plastic tubes for subsequent sex determina- of overwintering navel orangeworm, including over- tion, as described above. When emergence was heavy lap with new crop nuts. in the almond mummies in 2006, six to eight tubes were Þlled with Ϸ600Ð1,000 adults for sex determination and the remaining moths were counted as they ßew Materials and Methods from the buckets. These experiments were terminated Mummy Collection and Holding. All of the pista- after 60 d when 740 degree-days (DD) were accumu- chio mummies used in these studies were the Kerman lated in the incubator. Differences in the average DD variety (this variety constitutes Ͼ95% of all pistachios accumulated for all adult emergence from pistachio currently grown in California), and almond mummies mummies and almond mummies were evaluated with used were Nonpareil and Carmel varieties. The mum- one-way analysis of variance using JMP 7.02 (SAS mies used in 2002Ð2006 were collected from orchards Institute, Cary, NC). in southern Madera County. Pistachio mummies and Population Structure. In late January 2003, 500 ran- almond mummies were also collected in January 2006 domly selected pistachio and 500 randomly selected from heavily infested orchards in Kern County. Two almond mummies were dissected, and all larvae and temperature regimes were evaluated in these studies, pupae were recorded and classiÞed into two age cat- a variable regime from 2002 to 2004 and constant egories. One category, late instars, consisted of Þfth- temperature in 2004Ð2006. In the variable tempera- and sixth-instar larvae plus pupae, and the second ture regime, pistachio mummies were collected from category consisted of the remaining instars; no un- August 2010 KUENEN AND SIEGEL:EMERGENCE OF OVERWINTERING NAVEL ORANGEWORM 1061 hatched eggs were found on any of the mummies. The Table 1. Instar distribution of navel orangeworm dissected differences in age structure between almond and pis- from 500 mummies of pistachio and almond collected in early January 2003 tachio mummies were analyzed using 2 ϫ 2 contin- ␹2 gency analysis. Instar Almonds Pistachios Sex Ratio Analysis. The data from all experiments Second 9 0 were pooled to maximize sample size. Deviation from Third 63 1 a 50:50 sex ratio for each nut species was evaluated by Fourth 73 3 ␹2 analysis with one degree of freedom, and differ- Fifth and sixth 71 22 ences in the sex ratio between pistachio mummies and Pupa 4 2 almond mummies were evaluated using 2 ϫ 2 contin- Total collected 220 28 gency ␹2 analysis. Determining Prevalence of Navel Orangeworm in in 2003, prevalence was 7.2% in pistachio mummies Pistachios. Assessing navel orangeworm infestation in and 67.8% in almond mummies. The prevalence of pistachio mummies using the total number of mum- navel orangeworm in the 2004-collected mummies mies collected is misleading because as many as 30% was twice as high in ground mummies, 19.9% (11,460 of the pistachios on the tree are blank nuts that contain Þlled, split mummies), compared with 9.8% in tree no kernels and therefore cannot be infested (Gold- mummies (3,352 Þlled, split mummies). In 2006, the hamer and Beede 2004). These blank pistachio mum- prevalence of navel orangeworm was again greater in mies may predominate in the orchard after harvest almond mummies than in pistachio mummies, 7.8% (Siegel et al. 2008). In this study, a subset of mummy compared with 4% in Madera County and 50.2% com- pistachios was dissected to establish the proportion of pared with 15% in Kern County. The sex ratio of mummies that could be infested, and this percentage emerged adults from 2002 to 2006 was skewed from was multiplied by the total number of mummies col- pistachio mummies with a male:female ratio of 57:43 lected to estimate the number of available mummies. (␹2 ϭ 42, df ϭ 1, P Ͻ 0.001), whereas almond mum- In 2002 and 2003, 500 pistachio mummies were dis- mies had a 50:50 sex ratio (Table 2). sected each year, and in 2004Ð2005 and 2006, 5,000 In the variable temperature regime experiment in pistachio mummies were dissected each year for this 2002Ð2003, adult emergence began in late March calculation. and continued through the Þrst week of June (Fig. Degree-Day Accumulation. DD accumulation from 1). There was a single emergence peak from pista- 1 January of each year was determined using the chio mummies, and when it ended, 75% of the adults University of California integrated pest management had emerged, whereas three emergence peaks were web-based DD calculator (Anonymous 2009). The evident from almond mummies and it was only at the lower developmental threshold was set to 12.8ЊC, and end of the third peak that 75% of the adults had the upper developmental threshold was set to 34.4ЊC emerged. The DD accumulation for 50 and 75% with a horizontal upper development cutoff (Zalom et adult emergence occurred earlier in pistachio mum- al. 1998). DD accumulation for the mummies held mies than in almond mummies, corresponding to a outside our laboratory used California Meteorological difference of 1 and 3 wk, respectively. It took three Instrument Station (CMIS 39) Ϸ0.5 km distant; DD times longer (in DD) to go from 50 to 75% emer- accumulations for Madera County used CMIS 145 gence from almond mummies than from pistachio (Ϸ18 km from the collection site); and DD accumu- mummies. In 2003Ð2004, a similar pattern of a single lations for Kern County used CMIS 54 (Ϸ18 km from emergence peak from pistachio mummies and mul- the collection site). For the mummies held at constant tiple emergence peaks from almond mummies oc- temperature, DD accumulation was determined as curred (Fig. 2), although the dates for 50 and 75% follows: (incubator temperature Ϫ 12.8ЊC) ϫ days emergence differed from 2002. That is, from pista- elapsed; incubator temperatures were conÞrmed chio mummies, 50% emergence occurred 1 wk ear- with HOBO data loggers (Onset Computer, Pocas- lier than in the previous year, and from almond set, MA). mummies 50% emergence occurred 2 wk later than the previous year. The date for completion of 75% Results emergence followed this same pattern. In 2006, navel orangeworm emergence from pista- The proportion of late instars and pupae was sig- chio mummies and almond mummies at constant tem- niÞcantly higher in pistachio mummies, 85.7%, than in perature followed the same pattern as emergence un- almond mummies, 34.1% (Table 1; ␹2 ϭ 26, df ϭ 1, P Ͻ der variable temperature regimes. Pistachio mummies 0.001). Only a single third-instar larva was found in the collected from Madera County had a single emer- dissected pistachio mummies, whereas in almond mummies there were three equal groups of larvae comprising third instars, fourth instars, and late instars Table 2. Total male and female navel orangeworm collected plus pupae. The prevalence of navel orangeworm was from pistachio mummies and almonds, 2002–2006 substantially lower in pistachio mummies than in al- Host Male Female Total mond mummies based on dissection and emergence from the cages. In 2002, prevalence was 1.0% in pis- Almonds 3,817 3,790 7,607 tachio mummies and 36.9% in almond mummies, and Pistachios 2,176 1,668 3,844 1062 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 4

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March April Degree Days June Fig. 1. Adult navel orangeworm emergence from pistachio mummies and almond mummies collected in January 2002 from Madera County, California, and held outdoors at Parlier. DD calculated using CMIS 39. gence peak, whereas almond mummies had two dis- equivalent of 1Ð15 July. To assuage our own con- tinct emergence peaks (Fig. 3). The DD accumulated cerns about possible reinfestation of our sampled for 50 and 75% emergence were similar in both groups mummies by newly emerged females, we conducted of mummies, perhaps because the orchards were ad- preliminary studies in laboratory jars that were jacent. In the Kern County mummies (Fig. 4), both 50 monitored daily to characterize development ex- and 75% emergence occurred sooner from pistachio tremes and found no development of new adults in mummies than from almond mummies, and emer- the time frame used in this study. We continued this gence from almond mummies lasted an additional 150 type of monitoring during the course of our exper- DD. When the data from both counties were com- Ϯ iments described in this study and found no evi- bined, mean emergence ( SD) occurred 19.7% dence of moth emergence from eggs laid by females sooner from pistachio mummies than from almond emerged in this study. Final support comes from mummies (F ϭ 1,230; df ϭ 1, 17,434; P Ͻ 0.0001), Sanderson et al. (1989b), who found the mean navel 283.4 Ϯ 84.7 DD (7,004 adults) compared with 353.1 Ϯ orangeworm development rate on mummy almonds 151.1 DD (10,431 adults). In these pooled datasets, was Ϸ514 DD for onset of emergence (add Ϸ75 DD over 9% of the adults emerged during the DD equiv- Ϸ alent of early to late June, and in pistachio mummies for our Þrst observed emergence 600 DD; any the last recorded emergence was on the DD equiva- emergence after this time was decreasing rather lent of 15 July. than increasing if ever increasing numbers of males In 2004Ð2005, both the berm and tree-collected and females had mated and laid eggs on the mummy pistachio mummies had a single emergence peak samples). Furthermore, the difÞculty in establishing (Fig. 5), and the DD accumulated for 50 and 75% a laboratory colony from feral moths is generally emergence were similar. Emergence ceased at the known for most , most likely because of the DD equivalent of 15 July and was more protracted activity of insects trying to escape the cage(s) rather than in the samples from the other years. Approx- than trying to mate; thus, establishment of larvae imately 10% of emergence occurred at the DD arising from mated females is even more remote. August 2010 KUENEN AND SIEGEL:EMERGENCE OF OVERWINTERING NAVEL ORANGEWORM 1063

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Discussion with almond mummies; several factors alone or in concert may be responsible. First, the timing of nut We have demonstrated in this study that the pattern susceptibility plays a major role in determining infes- of navel orangeworm adult emergence differed be- tween overwintering hosts, pistachio mummies, and tation in the Þeld. Under current management almond mummies when held outdoors under a vari- schemes, new crop pistachios may only be susceptible for half the time that new crop Nonpareil almonds are able/ambient temperature regime, and that the age Ϸ structure of the overwintering immature navel or- ( 4 versus 9 wk, respectively) because of differences angeworm in the mummies appeared to be the un- in both hull split and harvest date. In addition, other derlying cause. The single cluster of late-instar larvae varieties of almonds become susceptible after Non- and pupae in pistachio mummies corresponded to the pareils and navel orangeworm larvae develop in the observed single emergence peak, and both were con- hulls of most or all almond varieties, further expanding sistent with the earlier emergence observed from pis- the age spread of navel orangeworm in almonds versus tachio mummies. In almond mummies, the three larval pistachios. The shorter and later susceptibility of pis- age group clusters corresponded to the multiple adult tachios most likely led to the reduced age spread of emergence peaks, and the substantial number of immature navel orangeworm in pistachio mummies, younger larvae was consistent with the increased time which in turn engendered the single emergence peak required for 50 and 75% adult emergence. For both observed from pistachio mummies at both variable years of the outdoor studies, adult emergence contin- and constant temperature. ued into June. When we subsequently held much Second, nutritional suitability among nut varieties larger samples of pistachio and almond mummies un- and between species, as well as nutritional stability der constant temperature conditions, we observed an over time, will affect age structure because neonates even more protracted emergence and the last moths that hatch on the same day on different hosts will emerged in the DD equivalent of June and into early develop at different rates. Navel orangeworm devel- July in 2 yr. opment rate is dependent on nut maturity, initially It is unclear what causes the different navel orange- increasing as immature nuts age and then decreasing worm age structures observed in pistachio compared as mummy nuts degrade (unpublished data). Devel- 1064 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 4

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50 50% 75% 0 0 50 100 150 200 250 300 350 400 450 500 550 600 650 April MayDegree Days June Fig. 3. Comparison between adult navel orangeworm emergence from almond mummies and pistachio mummies collected from the ground (January 2006) in adjacent orchards in Madera County, California. Emergence continued from almond mummies and pistachio mummies through the DD equivalent of 26 June, using CMIS 145. opment can be almost twice as long in almond mum- The suite of fungi that grow on these mummies may mies (Sanderson et al. 1989b) and pistachio mummies be quite different, and fungal metabolites may inßu- (unpublished data) than in new crop nuts. Legner ence navel orangeworm development and mortality. (1983) reported that it took 5 mo for adults to com- For example, we reported that substantial navel or- plete adult emergence (Ͼ1,900 DDЊC) from infested angeworm mortality occurred in mummy pistachios Nonpareil almonds collected in July and held at between December and February because of unde- 25.6ЊC. Prolonged development like this also occurs in termined factors (Siegel et al. 2008); the skewed sex other almond varieties, but does not occur in pista- ratio observed in this study may result from mortality chios (unpublished data). as a result of these factors. Third, allelochemical differences between pista- Previously, we have noted that navel orangeworm chio mummies and almond mummies may affect the males were captured in female-baited traps through- timing and sex ratio of emerging adults. For example, out the growing season (Kuenen and Rowe 2003), and the skewed sex ratio observed in adults emerging from a major goal of the current study was to determine pistachio mummies indicates that female mortality whether elements of the Þrst ßight (overwintering was higher, assuming that male and female eggs were navel orangeworm) could bridge directly into new laid without bias. Because this did not occur in almond crop nuts, or whether there is an obligate cycle of mummies and because this skewed sex ratio does not development in mummies. Our data for 2002 and 2003 occur when adults emerge from new crop pistachios are consistent with an obligate Þrst in-season gener- (unpublished data), our Þnding underscores that nuts ation of navel orangeworm on mummy nuts, because are a dynamic resource whether fresh or mummies. there are no new crop nuts available before late June. August 2010 KUENEN AND SIEGEL:EMERGENCE OF OVERWINTERING NAVEL ORANGEWORM 1065

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However, we recognized that this conclusion may Focusing on navel orangeworm developmental DD is have been a function of insufÞcient sample size. only one piece of the puzzle because it is not Therefore, we moved to the second protocol (Siegel necessarily closely linked to nut development/avail- et al. 2008) that could incorporate much larger sample ability, and further research is needed on the phenol- sizes. For instance, in the 39,250 pistachio mummies ogy of pistachios, because there is no current model. collected in 2004, a portion of the Þrst ßight (9%) Consequently, in a given year there are undoubtedly emerged as late as mid-July; by this time new crop orchards where a portion of the Þrst ßight oviposits on almonds are available (Kuenen and Barnes 1981). In new crop nuts, whereas in other orchards there is 2006, Ϸ10% of the adults emerged through the degree- obligate development of a generation of navel orange- day equivalent of the month of June when Nonpareil worm on mummies only. almond hull split begins. In pistachios, both pea-split Damaging levels of infestation may occur in an area and malformed small nuts containing kernels that can when something is altered from the norm, such as support navel orangeworm development are suscep- increased or early availability of early split pistachios, tible as early as mid-June; consequently, late emerging so that a higher percentage of the Þrst ßight success- adults from the overwintering generation can Þnd fully oviposits on new crop nuts, which in turn speeds suitable new crop nuts in both pistachios and almonds. navel orangeworm population growth. Furthermore, The dates for 50 and 75% emergence will vary among the combination of differential development rates in counties and years because DD are accumulated at pistachios and almonds and movement between these different rates throughout the San Joaquin Valley. two crops result in overlap between the navel orange- 1066 ENVIRONMENTAL ENTOMOLOGY Vol. 39, no. 4

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0 50 150 250 350 450 550 650 750 AprilMay July Degree Days Fig. 5. Contrasting navel orangeworm emergence from pistachio mummies collected from the ground (berm) and from trees in an orchard in Madera County, December 2004. Emergence continued until the DD equivalent of 15 July 2005 using CMIS 145. worm ßights, which increases as the summer progresses. combined to effectively suppress navel orangeworm Thus, from late June forward, it is impossible to assign populations in pistachios and almonds. eggs laid on ovitraps, males captured in female-baited traps, or larvae collected from nuts to a particular gen- eration, thus clouding the view of discrete generations of Acknowledgments navel orangeworm in the Þeld. In conclusion, this study has several implications for We thank James Bettiga, Kevin Olsen, and Bradley Higbee navel orangeworm control in pistachios and almonds. for their help in providing mummies, and Richard Gill, Pa- Our data of prolonged emergence, differential devel- tricia Noble, and Heather Rowe for their assistance in mummy collection and monitoring emergence. This work opment on mummy and new crop nuts, and subse- was supported in part by the California Pistachio Commis- quent overlap among generations, as well as the lack sion. of developmental synchronization by means of dia- pause, question the traditional view that navel orange- worm populations consist of discrete generations. References Cited Functionally, it may make more sense to refer to sep- arate ßights rather than separate generations; and Anonymous. 2005. California agricultural resource direc- even this may be misleading, because navel orange- tory 2005. California Department of Food and Agricul- worm are present (males can be trapped) throughout ture, Sacramento, CA. the summer (Kuenen and Rowe 2003). Anonymous. 2009. University of California, agriculture and Control of this insect is particularly challenging natural resources. UC IPM online (http://www.ipm. ucdavis.edu/WEATHER/ddretrieve.html). because the Þrst ßight (adults from overwintering Beede, R. H., W. J. Bentley, R. E. Rice, L. S. Abelein, R. immatures) may last as long as 5 mo, and in almonds Cortez, and G. B. Weinberger. 1984. Navel orangeworm the prolonged, multipeak emergence of navel orange- management in pistachios, pp. 61Ð68. Calif. Pistachio As- worm makes it difÞcult, and probably economically soc. Ann. Rpt. (http://www.acpistachios.org/research. unfeasible, to target the entire Þrst ßight with cur- php). rently available insecticides. Pistachios may be a bet- Bentley, W. J., K. M. Daane, L. C. Hendricks, E. C. Mussen, ter target for spring insecticide treatment(s) because C. Pickel, R. E. Rice, and F. G. Zalom. 2002. Insects and peak emergence is compressed, but sanitation in pis- mites, 2nd ed, pp. 53Ð107. In L. L. Strand (ed.), Integrated tachios is problematic and pistachio blocks have a pest management for almonds. University of California, Agriculture and Natural Resources, Oakland, CA. larger resident population than their almond counter- Bentley, W. J., J. P. Siegel, B. Holtz, and K. M. Daane. 2008. parts (Burks et al. 2008). Movement between these Navel orangeworm and obliquebanded leafroller as pests two nut crops (Higbee and Siegel 2009) necessitates of pistachio, pp. 179Ð191. In L. Ferguson (ed.), Pistachio the development of a coordinated control strategy, production manual, 5th ed. University of California, and it is likely that several strategies will need to be Davis, CA. August 2010 KUENEN AND SIEGEL:EMERGENCE OF OVERWINTERING NAVEL ORANGEWORM 1067

Burks, C. S., B. S. Higbee, D. G. Brandl, and B. E. Mackay. Legner, E. F. 1983. Patterns of Þeld diapause in the navel 2008. Sampling and pheromone trapping for comparison orangeworm (Lepidoptera: Phycitidae) and three im- of abundance of Amyelois transitella in almonds and pis- ported parasites. Ann. Entomol. Soc. Am. 76: 503Ð506. tachios. Entomol. Exp. Appl. 129: 66Ð76. Mote, D. C. 1922. A new orange pest in Arizona. Calif. State Curtis, C. E. 1976. Economics of NOW control and imple- Dep. Agr. Monthly Bull. 11: 628Ð631. menting orchard cleanup. Almond Facts 41: 5Ð8. Sanderson, J. P., M. M. Barnes, R. R. Youngman, and C. E. Doster, M. A., and T. J. Michailides. 1995. The relationship Engle. 1989a. Developmental rates of the navel orange- between date of hull splitting and decay of pistachio nuts worm (Lepidoptera: Pyralidae) at various constant tem- by Aspergillus species. Plant Dis. 79: 766Ð769. peratures. J. Econ. Entomol. 82: 1096Ð1100. Engle, C. E., and M. M. Barnes. 1983a. Developmental Sanderson, J. P., M. M. Barnes, and W. S. Seaman. 1989b. threshold temperature and heat unit accumulation re- Synthesis and validation of a degree-day model for navel quired for egg hatch of navel orangeworm (Lepidoptera: orangeworm (Lepidoptera: Pyralidae) development in Cal- Pyralidae). Environ. Entomol. 12: 1215Ð1217. ifornia almond orchards. Environ. Entomol. 18: 612Ð617. Engle, C. E., and M. M. Barnes. 1983b. Cultural control of Seaman, W. S., and M. M. Barnes. 1984. Thermal summation for the development of the navel orangeworm in almond navel orangeworm in almond orchards. Calif. Agr. 37: 19. (Lepidoptera: Pyralidae). Environ. Entomol. 13: 81Ð85. Goldhamer, D. A., and R. H. Beede. 2004. Regulated deÞcit Sibbett, G. S., and R. A. Van Steenwyk. 1993. Shredding irrigation effects on yield, nut quality and water-use ef- “mummy” walnuts is key to destroying navel orangeworm Þciency of mature pistachio trees. J. Hort. Sci. & Biotech. in winter. Calif. Agr. 47: 26Ð28. 79: 538Ð545. Siegel, J. P., L.P.S. Kuenen, B. S. Higbee, P. Noble, R. Gill, Higbee, B. S., and J. P. Siegel. 2009. New navel orangeworm G. Y. Yokota, R. Krugner, and K. M. Daane. 2008. Post sanitation standards could reduce almond damage. Calif. harvest survival of navel orangeworm assessed in pista- Agr. 63: 24Ð28. chios. Calif. Agr. 62: 30Ð35. Kuenen, L.P.S., and M. M. Barnes. 1981. Spatial and tem- Wade, W. H. 1961. Biology of the navel orangeworm, Para- poral development of maturation of Nonpareil almonds myelois transitella (Walker), on almonds and walnuts in and infestation by the navel orangeworm, Amyelois tran- northern California. Hilgardia 31: 129Ð171. sitella (Walker). Environ. Entomol. 10: 673Ð675. Zalom, F. G., J. H. Connell, and W. J. Bentley. 1998. Vali- Kuenen, L.P.S., and H. C. Rowe. 2003. Season-long moni- dation of phenology models for predicting development toring of navel orangeworm with female sex pheromone of the navel orangeworm Amyelois transitella (Walker) in and egg traps. In Proceedings, Ninth Annual Research California almond orchards. Acta Hortic. 470: 525Ð533. Meeting of Methyl Bromide Alternatives Organization. (http://mbao.org/2003/mbrpro03.html). Received 29 September 2009; accepted 2 March 2010.