Review Article t

New Zealand lessons may aid efforts to control in California

by Lucia G. Varela, James T.S. Walker, attacking pupal and late larval stages Peter L. Lo and David J. Rogers of light brown apple moth and (2) the

Jack Kelly Clark Kelly Jack change in fruit production programs New Zealand’s major fruit industries from frequent applications of broad- spectrum insecticides to less-intensive are dependent upon producing high- spraying with selective products. quality crops for export with a very By using a combination of natural low incidence of pest damage. Light control and selective insecticides, New brown apple moth was an economi- Zealand growers are able to control light brown apple moth and meet the export cally important pest within the fruit standards of more than 60 countries sector in the 1960s through the that import a variety of fruit crops. In 1980s, and it developed resistance the 1980s, organophosphate insecticides to broad-spectrum insecticides. The were sprayed in six to nine applications each season on pome fruit crops for a increase in its pest status focused variety of pests. Over the last decade, research on biological control, and use of organophosphate insecticides has existing native natural enemies were declined by 97%, while the frequency augmented with new introductions of insecticide applications has declined by approximately 50% (Manktelow et from in the late 1960s. By In New Zealand, light brown apple moth al. 2005). The insecticides now used are the early 1990s, this effort resulted is controlled by and selective insecticides. selective. The incidence of light brown in substantially reduced leafroller apple moth fruit damage has declined, populations and fruit damage. The fruit (apples and pears) and berry fruit, as has the larval incidence in crops. and a minor pest of grapes, citrus, In recent U.S. Department of Agri- implementation of integrated pest stone fruit and kiwi fruit. The number culture preclearance inspections of management (IPM) programs in the of acres planted to pome and berry New Zealand apples grown using the New Zealand fruit sector in the mid- fruit — the crops most affected by light Integrated Fruit Production program, to late 1990s practically eliminated brown apple moth — is similar in New the rejection rate of export consignments Zealand and California (table 1). for the presence of light brown apple moth the use of broad-spectrum organo- New Zealand went through a phase was typically less than 1%. A consignment phosphate insecticides, further en- from the 1960s to 1980s when light is rejected if one or more is detected hancing natural control. Today light brown apple moth caused major fruit in 20,000 individually inspected fruit. damage; in apple crops this averaged brown apple moth is successfully Biology and damage from 8% to 26% and as high as 48% managed in IPM and organic pro- (Collyer and van Geldermalsen 1975). The light brown apple moth’s biology grams through a combination of bio- Control programs were based on fre- was previously described in California logical control and threshold-based quent applications of broad-spectrum Agriculture (Varela et al. 2008). In New insecticides. This led to the develop- Zealand, this reportedly feeds applications of selective insecticides. ment of resistance to organochlorines on 265 different host plant species in the early 1960s (Collyer and van he recent discovery of light brown Geldermalsen 1975) and organophos- TABLE 1. Planted area of light brown apple moth apple moth, a leafroller, in Califor- phates by the early 1980s (Suckling et fruit-crop hosts Tnia may affect the management of fruit al. 1984; Suckling and Khoo 1990). Crop New Zealand* California† crops, and because it is a quarantine Over the last two decades, the pest ...... pest in some markets, the discovery status of light brown apple moth in acres (hectares) Pome fruit 23,539 (9,526) 36,500 (14,771) has already had implications for do- New Zealand apples has shifted signifi- Berry fruit 5,913 (2,393) 7,400 (2,994) mestic and export trade in produce cantly. Damage has decreased to typi- Strawberries 420 (170) 35,500 (14,366) and nursery stock. cally less than 2% in unsprayed trees Grapes 72,518 (29,347) 789,000 (319,297) In New Zealand, light brown apple (fig. 1). The decline in fruit damage is Citrus 4,532 (1,834) 251,500 (101,778) moth, Epiphyas postvittana (Walker) associated with lower leafroller density, Stone fruit 5,669 (2,294) 243,800 (98,662) Kiwi fruit 30,112 (12,186) 4,000 (1,619) (: ), was first which in turn is attributed to two key reported in 1891 (Hudson 1928). It be- factors: (1) the introduction in the 1960s * Plant & Food Research Fresh Facts 2008. † USDA NASS 2008. came a major pest, primarily of pome and subsequent spread of parasitoids

6 CALIFORNIA AGRICULTURE • VOLUME 64, NUMBER 1 45 40 35 30 25 20 15 Fruit damage (%) 10 5 0 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008

Fig. 1. Leafroller fruit damage on unsprayed apple trees in Hawke’s Bay, New Zealand, 1986 to 2008. ★ = no records kept.

(Thomas 1965), including fruit crops, populations. The effectiveness of this ornamental plants, windbreak trees program relies on a complex of native and broadleaf weeds. and introduced natural enemies that This leafroller is predominantly a attack all life stages (table 2) both in foliage feeder (Lo et al. 2000). The newly intensively managed fruit crops and hatched larva spins a protective, silken, the natural landscape. The reduction of tubular shelter on the lower surface of broad-spectrum insecticide use since leaves or ties together young leaves at the late 1990s has enhanced natural Fig. 2. Major agricultural growing regions of New Zealand, and scale comparison with the U.S. West shoot tips. Second and later stages may control. The present state of biological Coast (inverted to show corresponding latitudes). web leaves together or attach them to control came about by (1) accidental fruit. Fruit feeding is incidental and introductions of parasitoids and preda- fruit damage is superficial; the penetra- tors, (2) the switching of hosts by some velop outside of the host body. In some tion of fruit by larvae is uncommon. native natural enemies and (3) the species, only one will develop Fruit damage may increase during the deliberate introduction from 1967 to in or on each host (solitary); in others, season because of the larger fruit sur- 1972 of parasitoids that attack the later several to hundreds of young larvae may face area in contact with leaves or other stages of light brown apple moth. develop from a single prey (gregarious). fruit (Lo et al. 2000). An insect parasitoid completes its L.J. Dumbleton (1932, 1935) was the New Zealand extends from 34o to larval development on or inside a host. first to report on natural enemies of 47 o latitude (a geographic range similar Most beneficial insect parasitoids are the light brown apple moth in New to the lower 48 U.S. states) but has a or , the adult of which depos- Zealand. He listed Dolichogenidea tas- maritime climate that is mild and rela- its one or more eggs on or inside a par- manica (Cameron) () as the tively humid, similar to that of coastal ticular life stage (egg, larva or ) of most frequent parasitoid, found in 20% California (fig. 2). The two major grow- its host. When the egg hatches, the para- to 50% of the larvae reared. D. tasmanica ing regions for New Zealand apples are sitoid larva feeds on the host’s tissue, attacks small leafroller larvae, deposit- Hawke’s Bay and Nelson (Tasman). The ultimately killing the host as it matures ing its eggs inside first- or second- climate of these two regions approxi- and becomes free living as an adult. larvae. The parasitoid larva develops mates that of California’s Central Coast Endoparasitoids (endo) develop inside of inside its host and emerges from the and North Coast, except that in New the prey while ectoparasitoids (ecto) de- third and fourth leafroller stage to form Zealand rainfall is year-round while in California precipitation is concentrated TABLE 2. Major parasitoids attacking light brown apple moth (LBAM) stages in New Zealand in fall and winter. Light brown apple moth has four LBAM life stage/instar generations per year in northern North Species Family Parasitoid type Origin Attack Emerge from Island, three generations in the southern Dolichogenidea Braconidae Solitary, endo* Accidentally First and second Fourth North Island and northern South Island, tasmanica introduced Glyptapanteles Braconidae Gregarious†, endo Endemic Third and fourth Late larval two to three generations in Canterbury demeter and two generations in Central Otago Goniozus jacintae Bethylidae Gregarious, ecto‡ Australia Second to fourth Late larval (Wearing et al. 1991). The second- and Solitary, endo Australia Third to fifth Mid- to late third-generation larvae cause the brevifacies larval or pupal most fruit damage (Collyer and van Pales funesta Tachinidae Solitary, endo Endemic Fourth to fifth Late larval Xanthopimpla Ichneumonidae Solitary, endo Australia Pupal Pupal Geldermalsen 1975; Lo et al. 2000). rhopaloceros Historical biological control Glabridorsum Ichneumonidae Solitary, ecto/ Australia Pupal Pupal stokesii endo A biological control program has * Parasitoid develops within its host. evolved in New Zealand that sup- † More than one parasitoid develops per host. presses light brown apple moth ‡ Parasitoid develops outside its host.

http://californiaagriculture.ucanr.org • January–March 2010 7 With a strategic commitment to biological control within an IPM context, California may ultimately achieve the same levels of light brown apple moth control as obtained in New Zealand.

a cocoon inside the webbed nest next In 1967 and 1969, Thomas collected to the consumed leafroller larva (Paull parasitoids in the eastern temperate and Austin 2006). D. tasmanica was ac- areas of Australia, from Sydney in New cidentally introduced to New Zealand, South Wales to Hobart in . Of probably with light brown apple moth the specimens collected, six species that from Australia (Dumbleton 1935). attack late leafroller stages were released Photos: New Zealand Institute for Plant & Food Research Limited New Zealand Institute for Plant & Food Photos: Dumbleton (1936) reported only between 1967 and 1972. Five species suc- one early parasitoid importation from cessfully established themselves, but Australia in 1922; it was later identified only three that attack light brown apple as Goniozus jacintae Farrugia (Bethylidae) moth became relatively widespread. (Berry 1998). This parasitoid lays one These three species are the tachinid or more eggs externally in the folds be- (Hardy), which tween segments of third- to sixth-stage attacks late larval stages, and the pupal (Danthanarayana 1980). ichneumonid parasitoids Xanthopimpla The parasitoid larvae feed externally rhopaloceros Krieger and Glabridorsum and later form cocoons inside the nest stokesii (Cameron). All three species had formed by the leafroller. The rest of the been released at several locations in the species Dumbleton described attacking North Island, and in the Nelson area light brown apple larvae either had ar- and Canterbury in the South Island. In rived with light brown apple moth or 1999, T. brevifacies was rereleased in the were native to New Zealand. Two native Nelson area, using specimens collected parasitoids identified by Dumbleton are in Hawke’s Bay (Shaw et al. 2001). still frequently encountered: the gre- In surveys conducted in 1996 and garious endoparasitoid Glyptapanteles 1997 (Munro 1998), X. rhopaloceros and demeter (Wilkinson) (Braconidae), which T. brevifacies were found throughout attacks third- and fourth-stage leafroller the North Island and the north end of larvae, and the tachinid fly Pales funesta the South Island. Both species failed to (Hutton), which attacks fourth and fifth establish in Canterbury. X. rhopaloceros larval stages. had a faster rate of spread than T. brevi- G. demeter is the most frequently facies; X. rhopaloceros was first reported Parasitoids are that complete their cited native parasitoid attacking light established in the north end of the North development inside a host. A number of them brown apple moth. In a study con- Island in 1973. Published reports in 1975 are known to attack light brown apple moth, ducted in organic apple orchards, and 1976 indicate that this species ap- including, top, Xanthopimpla rhopaloceros, center, Glabridorsum stokesii and, bottom, Dolichogenidea spp. was the most abun- peared in Auckland in numbers large Dolichogenidea tasmanica. dant parasitoid attacking leafrollers enough that the public made inquiries to found in the apple foliage; G. demeter the authorities (Munro 1998). By the late was the dominant parasitoid reared 1970s and early 1980s it was recorded in quantified, there is indirect evidence from leafrollers collected from broad- the south of the North Island, becoming that they have contributed to significant leaf weeds in the apple orchard under- widespread in Hawke’s Bay by 1985 and declines in larval fruit-feeding dam- story (Rogers et al. 2003). in Nelson by 1992. age by light brown apple moth, and Thomas (1989) reported 19 species T. brevifacies was first reported as consequently to reduced insecticide of parasitoids reared from light brown established in the northern tip of the use. These generalist parasitoids, in apple moth eggs, larvae and pupae col- North Island in 1972. Archival records particular T. brevifacies, also have had lected in New Zealand prior to 1967. show that it was found in the northern an impact on endemic leafroller species D. tasmanica was the most abun- part of the island in the 1980s, moving and are likely to compete with native dant, and few parasitoids attacked through the western side and reaching parasitoids in the natural environ- the later larval and pupal stages. Wellington (in southern North Island) ment (Munro and Henderson 2002), but Trichogrammatid parasitoids, includ- in 1998. Recorded finds from the eastern since no prerelease data on the relative ing Trichogramma funiculatum and North Island began in the early 1990s abundance of lepidopteran species was Trichogrammatoidea bactrae, parasitized with reports from Hawke’s Bay in 1995. gathered, it is difficult to determine the the eggs of light brown apple moth with In the South Island the first reports exact impact. Before any proposed in- wide variation in parasitism levels, were from Nelson in 1997. troduction of the natural enemies, pos- rarely rising above 10% (Thomas 1989; Although the impacts of T. brevifa- sible impacts on both native hosts and Stevens 1995). cies and X. rhopaloceros have not been natural enemies should be considered.

8 CALIFORNIA AGRICULTURE • VOLUME 64, NUMBER 1 parasitoid emerged. D. tasmanica remains reared from the first four larval , Current biocontrol strategies the most abundant leafroller parasitoid, reducing light brown apple moth larvae Leafroller larvae and pupae (predom- comprising 66% to 97% of the parasitoids by 85% on average. A high proportion of inantly light brown apple moth) and reared from apple and stone fruit trees, neonate light brown apple moth larvae parasitoid cocoons were collected from berry fruit and grapevines. The next fail to settle and establish successful lea- orchards and vineyards in Hawke’s Bay most abundant parasitoids were T. brevi- frolls, and die before reaching the second between 1993 and 2009 (Lo, unpublished facies (1% to 27%), G. demeter (2% to 16%) instar. Later larval stages are then sub- data). These specimens were reared to and Goniozus jacintae (2% to 12%). D. tas- jected to high levels of parasitism that determine which species of leafroller or manica comprised 90% of the parasitoids potentially further reduced light brown

National Research Council reviews pest status of light brown apple moth by Rhonda J. Smith petitioners argued against eradication species, is not evaluated consistently as a feasible regulatory action. In June and has limitations that are not clearly 2009, APHIS wrote a draft response acknowledged or explained. 2007, the light brown apple moth to the petitions and requested that it Finding 4: The credibility of the re- was classified by the U.S. De- be reviewed by the National Research sponse is undermined by factors such INpartment of Agriculture’s Plant Council (NRC). as inadequately documented statements Health and Inspection Service (APHIS) The NRC’s September 2009 “Letter and scientifically imprecise terminology. as an actionable, quarantine-significant Report” addressed whether the federal Finding 5: APHIS has not published a pest, meaning that its presence has government had the regulatory author- proposed or final rule of the federal or- potentially significant economic im- ity to classify light brown apple moth der in the Federal Register for comment portance. Its presence in California re- as an actionable, quarantine-significant under the Administrative Procedure sulted in a federal order restricting the pest, and evaluated both the scientific Act and missed the opportunity to jus- interstate movement of specific agricul- basis for this regulatory decision and tify its actions to the public. tural commodities and their byproducts the quality of the evidence presented. Finding 6: APHIS chose to limit the from affected counties. To meet the fed- The 31-page report had two take- scope of its response by not addressing eral order, the moth is subject to quar- home messages. First, APHIS did have the use of eradication as the current antine and eradication efforts by both the authority to classify light brown ap- control strategy, and thus “may have APHIS and the California Department ple moth as an actionable pest and thus exacerbated public concerns about the of Food and Agriculture (CDFA). could take regulatory action. Second, eradication effort.” In 2009, more than 3,500 square the evidence used as the basis for the The NRC scientists could only ad- miles of California were in the quar- classification decision was insufficient dress what was contained in the APHIS antine area. Growers and others who and unclear, and in some instances the response; however, they emphasized move regulated articles off-site are re- evidence was not clearly supported by that APHIS did not include a rationale quired to have compliance agreements the data provided. for choosing eradication, which is one with the county agricultural commis- Finding 1: Only qualitative, rather of several possible approaches to con- sioner’s office. In Sonoma County, for than quantitative, criteria on economic/ trol a regulated pest. Instead, APHIS example, affected commodities include environmental damage are required for restricted its response to the issue of the wine grapes, apples, cane berries, the Secretary of Agriculture to deter- light brown apple moth’s classification strawberries, nursery stock, cut flowers mine a regulatory response to a pest. status and missed an opportunity to ex- and most vegetables and herbs, as well APHIS met the minimal standard by plain its decisions to the general public. as green waste. Compliance agreements providing evidence of the moth’s poten- It is important to read the full NRC are also required of the entity that tial invasive nature and economic and Letter Report, which recommends that receives product, such as wineries, pro- environmental impacts, but the agency’s APHIS refocus on the question of why cessing and packing plants. Wine-grape justification is not scientifically rigorous. this pest is so important to the United haulers are required to have compliance Finding 2: The data used to predict States and base their response on a de- agreements if they transport grapes the potential geographic distribution of tailed economic analysis. from a quarantine area. light brown apple moth in the United Go to: http://www.nap.edu/catalog. In September 2008 and February States and the subsequent economic im- php?record_id=12762. For information on 2009, APHIS received one petition pact analyses are not based on “sound, CDFA’s Light Brown Apple Moth Project, from four citizens, and another from rigorous science.” go to: http://www.cdfa.ca.gov/phpps/PDEP/ the Pesticide Action Network of North Finding 3: The evidence presented lbam/lbam_main.html. America plus other organizations, re- to make estimates of the potential eco- questing that light brown apple moth nomic damage to agricultural produc- be reclassified from an actionable to tion and trade, as well as environmental R.J. Smith is Viticulture Farm Advisor, UC Coopera- a nonactionable pest. In addition, the damage to native and endangered plant tive Extension, Sonoma County.

http://californiaagriculture.ucanr.org • January–March 2010 9 70 Nonorganic 170 25 107 121 10 83 Organic 60 252 32 91 tions in 2003 (Manktelow et al. 2005). 50 32 After 2001, just one or two reduced-risk 40 46 314 insecticide applications may be required 30 for light brown apple moth control when 20 53 122 377 fruit are grown for domestic consump-

Parasitized larvae (%) 10 303 tion. For export apples, pest manage- 0 1993–94 1994–95 1995–96 1996–97 1997–98 1998–99 1999–00 2000–01 2001–02 2002–03 ment is largely driven by codling moth control. This, together with the increased Fig. 3. Parasitized leafroller larvae from apple orchards in Hawke’s Bay, New Zealand. Yearly levels of biological control, provides a sample size is at the top of each column. very high level of management of light Pre-1996 (n = 33) Post-1996 (n = 230) brown apple moth. The impact of the replacement of or- ganophosphate insecticides on biological Dolichogenidea spp. control was demonstrated in Hawke’s A. sicarius Bay apple orchards. The proportion of G. demeter parasitized leafroller larvae and pupae Goniozus spp. from nonorganic apple orchards in-

X. rhopaloceros creased significantly between 1993 and

T. brevifacies 1994, and between 1999 and 2000 (fig. 3) (Lo, unpublished data). Of 478 leafrol- P. funesta lers collected from 23 orchards between 1993 and 1995, 7% were parasitized. In contrast, from 1996 to 2000, 604 leafrol- lers were collected from 19 orchards, Fig. 4. Parasitoid species reared from leafrollers collected in nonorganic apple orchards in and 42% were parasitized. In 1998, after Hawke’s Bay, New Zealand, 1993–1995 and 1996–2000. implementation of the Integrated Fruit Production Program, it became increas- apple moth populations by an estimated began implementing the Integrated ingly difficult to find leafroller infesta- 95% (Lo, unpublished data). Fruit Production Program (Walker et al. tions in nonorganic apple orchards. It is difficult to compare the rela- 1997), and within 5 years the industry By 2000, the whole sector had adopted tive importance of each natural enemy had substantially eliminated broad- Integrated Fruit Production practices, without a comprehensive life-table spectrum organophosphates from their and larval collections ended because of study. Nevertheless, the significance of spray schedules (Manktelow et al. 2005). the scarcity of leafroller fruit damage. D. tasmanica is evident in the relatively To address changing European In organic apple orchards where there high percentage of parasitism of young Union market demands for fruit pro- was no major change in spray programs larvae (about 50% of instar stages two duced using environmentally sus- between 1993 and 2003, parasitism was to four) compared with later immature tainable production systems, a pilot high throughout this period, albeit with stages (about 20%). Although the later Integrated Fruit Production Program some annual fluctuations. parasitoids are less abundant than was initiated in pome fruit throughout In addition to an increase in parasit- D. tasmanica, their importance should New Zealand in 1996. In this program, ism after the change to selective insecti- not be underestimated. They are remov- insect control relied on the increased cides, there is also a greater diversity in ing leafrollers that are more likely to use of biological control, monitoring the parasitoid fauna attacking leafrollers breed and contribute to the growth of and threshold-based applications of in New Zealand. In nonorganic apple subsequent populations. reduced-risk insecticides — those com- orchards, three parasitoid species were Perhaps the large increase in para- patible with integrated pest manage- reared from pre-1996 collections com- sitism in New Zealand apple orchards ment (IPM) (Walker et al. 1997). Light pared with seven species in later years during the 1990s also reflected the brown apple moth control is based on (fig. 4). In studies conducted in berry coincidental change from broad- one recommended application of an in- fruit in 1985 and 1986 in Hawke’s Bay spectrum to selective insecticides such secticide at petal fall (early November). (Charles et al. 1996), 14% to 70% of larvae as insect growth regulators. Many Any subsequent insecticide use after collected and reared were parasitized. broad-spectrum insecticides are nerve Dec. 15 is based on a cumulative thresh- More than 90% of the parasitoids reared poisons and consequently are toxic to old of 30 male moths caught in phero- were the solitary species D. tasmanica. both pests and beneficial species. In mone traps. The remaining were the gregarious lar- contrast, selective insecticides act on The program was progressively val parasitoids G. demeter and Goniozus metabolic pathways of pests but not adopted by growers and became the spp. Parasitism of larvae and pupae col- those of natural enemies, and therefore minimum export standard by 2001. lected from berries was 62% from 1996 have substantially lower toxicity to Total organophosphate insecticide use to 1999, and 79% from 2008 to 2009 (Lo, the latter, in particular parasitoids. In decreased from an average of 9 applica- unpublished data). D. tasmanica was less 1996, the New Zealand apple industry tions per season in 1996 to 0.3 applica- dominant than in the Charles et al. (1996)

10 CALIFORNIA AGRICULTURE • VOLUME 64, NUMBER 1 study, because T. brevifacies and Meteorus without any use of these insecticides, mented programs based on the con- pulchricornis were found in addition to and they suffer only negligible fruit cepts embodied within Integrated G. demeter and Goniozus spp. damage from light brown apple moth. Fruit Production: use of thresholds for Some of the new insecticides are pesticide inputs, with an emphasis on Current insecticide use significantly less disruptive to natu- selective control options (Manktelow The selective insecticides used in ral enemies than the broad-spectrum et al. 2005). Wine-grape industry re- pome fruit today in New Zealand pri- organophosphates used in the past. cords show that, for leafroller control, marily target codling moth, but they Residual bioassays measuring the effects national insecticide use has shifted are also effective against light brown of field application rates of insecticides from an average of one organophos- apple moth and provide high levels to D. tasmanica showed that tebufenozide phate application in 1997 to less than of control. They include tebufenozide and emamectin benzoate were harm- 0.4 insect growth regulator applications (Confirm), methoxyfenozide (Intrepid), less (less than 21% mortality) to adults by 2008. The two insect growth regula- indoxacarb (Avaunt), chlorantranili- 7 days after treatment. Indoxacarb and tor insecticides used in wine grapes prole (Altacor) and emamectin benzoate lime-sulfur residues caused 80% to for leafroller control are tebufenozide (Proclaim). All are effective and pro- 99% mortality, while carbaryl (Sevin), and methoxyfenozide. The need for an vide long residual control with low to diazinon and spinosad (Success) were application is determined by damage moderate impacts on beneficial natural very harmful (more than 99% mortal- observed during the previous harvest. enemies. About 8% of the New Zealand ity) (Newman et al. 2004). These toxicity When treatment is needed, a single pre- apple crop is grown organically; the categories followed the standard criteria bloom spray is applied. insecticides used in these orchards for laboratory studies defined by the Considerations for California include spinosad (Entrust) and Bacillus International Organization for Biological thuringiensis (Bt). Significant propor- and Integrated Control of Noxious With a strategic commitment to bio- tions of organic growers successfully and Plants (Hassan 1985). logical control within an IPM context, produce export apple crops using mat- By early 2000, all of New Zealand’s California may ultimately achieve the ing disruption for codling moth control major fruit industries had imple- (continued on next page)

References Berry JA. 1998. The bethyline species (: Manktelow D, Stevens P, Walker JTS, et al. 2005. Trends Suckling DM, Chapman RB, Penman DR. 1984. Bethylidae: Bethylinae) imported into New Zealand in Pesticide Use in New Zealand: 2004. Report to the Insecticide resistance in the lightbrown apple moth for biological control of pest leafrollers. NZ J Zool Ministry of Environment, Project SMF4193. 73 p. Epiphyas postvittana (Walker): Larval responses to 25:329–33. azinphosmethyl. J Econ Entomol 77:579–83. Munro VMW. 1998. A record of the releases and re- Charles JG, Walker JTS, White V. 1996. Leafroller phe- coveries of the Australian parasitoids Xanthopimpla Suckling DM, Khoo JGI. 1990. Cross-resistance in the nology and parasitism in Hawkes Bay, New Zealand, rhopaloceros Krieger (Hymenoptera: Ichneumonidae) lightbrown apple moth Epiphyas postvittana (Lepi- canefruit gardens. NZ J Crop Hort Sci 24:123–31. and Trigonospila brevifacies Hardy (Diptera: Tachinidae) doptera: Tortricidae). NZ J Crop Host Sci 18:173–80. introduced into New Zealand for leafroller control. NZ Collyer E, van Geldermalsen M. 1975. Integrated Entomol 21:81–91. Thomas WP. 1965. Studies on Epiphyas postvittana control of apple pests in New Zealand. 1. Outline of (Walker) (Lepidoptera, Tortricidae) and its parasitoid experiment and general results. NZ J Zool 2:101–34. Munro VMW, Henderson IM. 2002. Nontarget effect of complex. M.Sc. thesis, University of Canterbury. entomophagous biocontrol: Shared parasitism between 130 p. Danthanarayana W. 1980. Parasitism of the light native lepidopteran parasitoids and the biocontrol agent brown apple moth Epiphyas postvittana (Walker), Trigonospila brevifacies (Diptera: Tachinidae) in forest Thomas WP. 1989. Epiphyas postvittana (Walker), by its larval ectoparasite, Goniozus jacintae Farrugia habitats. Env Entomol 31:388–96. lightbrown apple moth (Lepidoptera: Tortricidae). (Hymenoptera: Bethylidae), in natural populations in In: Cameron PJ, Hill RL, Bain J, Thomas WP (eds.). A Victoria. Aust J Zool 28:685–92. Newman IC, Walker JTS, Rogers DJ. 2004. Mortality of Review of Biological Control of Invertebrate Pests and the leafroller parasitoid Dolichogenidea tasmanica (Hym: Weeds in New Zealand, 1874 to 1987. Wallingford, Dumbleton LJ. 1932. The apple leaf-roller (Tortrix Braconidae) exposed to orchard pesticide residues. NZ UK: CAB Int. p 187–95. postvittana Walker). NZ J Sci Tech 14:83–92. Plant Protect 57:8–12. [USDA NASS] US Department of Agriculture National Dumbleton LJ. 1935. Apanteles tasmanica Cam., a Paull C, Austin AD. 2006. The hymenopteran parasi- Agricultural Statistics Service. 2008. California Agri- braconid parasite of leafroller larvae. NZ J Sci Tech toids of light brown apple moth, Epiphyas postvittana cultural Statistics, Agricultural Overview 2007. 17:572–6. (Walker) (Lepidoptera: Tortricidea) in Australia. Aust J http://www.nass.usda.gov/Statistics_by_State/ Entomol 45:142–56. California/Publications/California_Ag_Statistics. 10 p. Dumbleton LJ. 1936. The biological control of fruit pests in New Zealand. NZ J Sci Tech 18:588–92. Plant & Food Research. 2008. Fresh Facts: New Zealand Varela LG, Johnson MW, Strand L, et al. 2008. Light Horticulture 2008. http://www.hortresearch.co.nz/files/ brown apple moth’s arrival in California worries com- Hassan SA. 1985. Standard methods to test the side- aboutus/factsandfigs/ff2008.pdf. 36 p. modity groups. Cal Ag 62:57–61. effects of pesticides on natural enemies of insects and mites developed by the IOBC/WPRS Working Group Rogers DJ, Walker JTS, Moen IC, et al. 2003. Understory Walker JTS, Hodson AJ, Wearing CH, et al. 1997. Pesticides and Beneficial Organisms. Bull OEPP/EPPO influence on leafroller populations in Hawke’s Bay or- Integrated fruit production for New Zealand pipfruit: 15:214–55. ganic apple orchards. NZ Plant Protect 56:168–73. Evaluation of pest management in a pilot programme. Proc 50th NZ Plant Protect Conf. p 258–63. Hudson GV. 1928. The Butterflies and Moths of New Shaw PW, Lo P, Wallis DR. 2001. Recent introduction and Zealand. Wellington, New Zealand: Ferguson Osborn. establishment of the leafroller parasitoid Trigonospila Wearing CH, Thomas WP, Dugdale JS, Dan- 386 p. brevifacies (Hardy) (Diptera: Tachinidae) in Nelson. NZ thanarayana W. 1991. Tortricid pests of pome and Plant Protect 54:33–6. stone fruits, Australian and New Zealand species. In: Lo PL, Suckling DM, Bradley SJ, et al. 2000. Factors Tortricid Pests: Their Biology, Natural Enemies and affecting feeding site preferences of lightbrown apple Stevens PS. 1995. Host preferences of Trichogram- Control; World Crop Pests, Vol. 5. Amsterdam: El- moth, Epiphyas postvittana (Lepidoptera: Tortricidae), matoidea bactrae fumata (Hym.: Trichogrammatidae) sevier. p 453–72. on apple trees in New Zealand. NZ J Crop Hort Sci an egg parasitoid of leafrollers (Lep.: Tortricidae). Ento- 28:235–43. mophaga 40:379–85.

http://californiaagriculture.ucanr.org • January–March 2010 11 Research Article t

(continued from previous page) Airborne particles in the San Joaquin same levels of light brown apple moth Valley may affect human health control as obtained in New Zealand. Many fruit crops in California already receive control measures for native by Mai A. Ngo, Kent E. Pinkerton, Sandra Free- San Joaquin Valley, which extends ap- and introduced leafrollers, and these land, Michael Geller, Walter Ham, Steven Cliff, proximately 250 miles from San Joaquin tactics may prove to be effective for Laurie E. Hopkins, Michael J. Kleeman, Urmila County in the north to Kern County light brown apple moth without a P. Kodavanti, Emily Meharg, Laurel Plummer, in the south. San Joaquin Valley agri- great deal of modification. Julian J. Recendez, Marc B. Schenker, Constan- culture encompasses more than 400 If the New Zealand experience tinos Sioutas, Suzette Smiley-Jewell, Christine plant and animal commodities — with is any indication, adequate control Haas, Joyce Gutstein and Anthony S. Wexler Fresno and Tulare counties leading in of this leafroller can be achieved agricultural value for the production more effectively through a vigorous of grapes, almonds, milk, oranges and program of biological control and Air quality is a primary concern for cattle. Approximately 4 million people the use of selective insecticides for many San Joaquin Valley residents. In live in the San Joaquin Valley (State other pest species. That approach addition to rapid population growth, of California 2007) and the number of identified a need to introduce natural farmworkers is estimated to be between a widening interface between urban enemies to attack light brown apple 175,000 to 500,000. moth through all stages of develop- and agricultural communities, and in- While the San Joaquin Valley is one ment. The focus on introductions to creasing traffic along the I-5 and Hwy. of the world’s most productive agri- address parasitism gaps, especially 99 corridors, farming practices in the cultural regions, it is also frequently those targeting the late larval and in violation of U.S. ambient air-quality San Joaquin Valley subject agricultural pupal stages, proved to be highly ef- concentration standards, particularly fective. Further exploration of natural workers to high concentrations of those for atmospheric particulate mat- enemies in New Zealand may yield airborne particulate matter potentially ter (PM) (Velasco 2005), which is de- guidance for possible parasitoid im- associated with adverse health effects. fined as liquid or solid material such portations to North America. as soil dust or smoke suspended in We created a research team and mobile As New Zealand has already found, the air. Particulate levels for the South it is unlikely that any one parasitoid field unit equipped with a special inha- Coast Air Basin and the Central Valley will be so specific that it attacks only lation system, particle monitoring and in California are the highest recorded light brown apple moth. Therefore, any characterization abilities, and housing in the country, exceeding the national introduction of natural enemies into ambient air-quality standards for California must be preceded by a care- for the transport and care of animals each season of the year. Workers and ful cost-benefit analysis. Light brown to examine the effects of particulate residents of the San Joaquin Valley are apple moth is a polyphagous insect, matter throughout the San Joaquin exposed to airborne particulate matter feeding on many plant species, and Valley. With this system, a variety of from a broad range of sources includ- some native leafrollers may occupy the ing farming practices such as the till- same niche. The benefit of suppressing biological endpoints can be examined ing of dry soil, agricultural burning, populations of light brown apple moth to determine respiratory, systemic and crop harvesting and diesel-powered and allowing reduced use of insecti- neurological responses to short-term water pumping. Particle emissions in- cide must outweigh possible adverse particle exposure. Field research of this clude inorganic compounds from soil impacts on populations of endemic lofted by, for example, dairy operations moths and natural enemies. This is an nature coupled with biological assays and off-road vehicles, or organic mat- issue that must be carefully considered and location-specific inhalation studies ter from animal feed and disturbed, in the development of a strategic plan can help researchers and regulators dried manure. for the long-term management of this The three parameters — size, com- to better understand potential health pest in California. position and distribution — for each effects due to environmental and oc- classification of particles are sufficiently cupational airborne-particle exposures different that each can produce unique faced by workers and residents in the health outcomes following inhalation. L.G. Varela is Integrated Pest Management Epidemiological studies have shown San Joaquin Valley. (IPM) Advisor, UC Statewide IPM Program and a strong correlation between the ex- UC Cooperative Extension; and J.T.S. Walker is posure of human populations to par- Senior Fruit Crop Entomologist, P.L. Lo is Senior Scientist, and D.J. Rogers is Senior Scientist, The griculture is a major industry in ticulate matter and acute and chronic New Zealand Institute for Plant & Food Research ACalifornia, generating $36 billion health effects, including increased Limited, Hawkes Bay, New Zealand. in 2007 (CDFA 2009). The state claims deaths due to cardiovascular illness and nine of the 10 most productive counties emergency room visits related to the se- References (see page 11) in the nation. The majority are in the verity of asthma symptoms (Sheppard

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