ᆣӫ፣क़

(ᖪ 27: 1-15 (2007ٿέ៉ Formosan Entomol. 27: 1-15 (2007)

Irradiation for Postharvest Control of Quarantine

Peter A. Follett U.S. Department of Agriculture, Agricultural Research Service, U.S. Pacific Basin Agricultural Research Center, Hilo, 96720, U.S.A. Man-Miao Yang, Kuang-Hui Lu* Department of Entomology, National Chung Hsing University, Taichung 402, Tse-Wei Chen Plant Quarantine Division, Bureau of and Plant Health Inspection and Quarantine, Council of Agriculture, Executive Yuan, Taipei 100, Taiwan

ABSTRACT

Interest in the use of irradiation as a phytosanitary treatment for agricultural commodities is growing worldwide, particularly since publication of the International Plant Protection Convention (IPPC) standard that endorses and facilitates trade based on this disinfestation method. Irradiation is broadly effective against insects and mites at doses that do not compromise quality of most commodities. Unlike other disinfestation techniques, irradiation does not need to kill the pest immediately to provide quarantine security, and therefore live but sterile or not viable insects may occur with the exported commodity making inspection for the target pests redundant. Generic irradiation treatments have been approved in the USA to control broad groups of insects in all commodities. The approved generic doses are 150 Gy for tephritid fruit flies and 400 Gy for all insects except pupae and adults (which may require higher doses). Generic irradiation treatments will accelerate the approval of irradiation quarantine treatments for specific crops and expedite new trade in agricultural products because research will no longer be needed for each quarantine pest and commodity. The availability of generic treatments makes irradiation an attractive option compared with other quarantine treatments.

Key words: irradiation, phytosanitary treatment, quarantine pest, probit 9 alternatives, generic treatments

Introduction may become plant pests will increase. The establishment of new pests can be World trade in agricultural commodities costly due to increased crop damage, continues to grow. As agricultural trade control programmes, and quarantine is increasing, the risk of introducing restrictions on trade. Quarantine treatments exotic insects into new areas where they or systems eliminate, sterilize, or kill

*Correspondence address e-mail: [email protected]! Irradiation for Postharvest Control of Quarantine Insects 1 regulatory pests in exported commodities 2006). For example, , Taiwan, and to prevent their introduction and the European Union have not approved establishment into new areas. As the use of irradiation as a phytosanitary exclusion is the goal for quarantine pests, treatment. However, irradiation as a the tolerance for the pest in the phytosanitary measure is now approved commodity is essentially zero (Follett and internationally by the International Plant Neven, 2006). Quarantine or phytosanitary Protection Convention (FAO, 2003), and treatments such as heat, cold, irradiation, may provide an alternative for replacing and fumigation disinfest host commodities current treatment methods. Herein, several of pests before they are exported to recent developments in the application of areas where the pests do not occur. irradiation and risk management are Whereas development of heat, cold, and discussed that should expand the use of fumigation treatments involves generating the technology worldwide and facilitate data for each commodity and pest trade in agricultural commodities, combination, irradiation treatments are particularly fresh commodities. developed for a pest species irrespective of the fruit or vegetable host. This is Radio-tolerance of insects possible because ionizing radiation penetrates groups vary in their commodities quickly without changing tolerance to irradiation (Table 1). Among the commodity’s temperature, and most insects, Diptera (flies), Coleoptera (beetles), commodities can tolerate irradiation at Hemiptera (true bugs) tend to be less doses that control the pest (Morris and radiotolerant than Lepidoptera ( Jessup, 1994, Thomas, 2001). Developing and butterflies), although there is heat, cold and fumigation treatments, on considerable variation among the species the other hand, involves finding a that have been tested within these groups balance between killing the pest and (Hallman, 2000, Bakri et al., 2005). minimizing the adverse effects of the Estimates for Hemiptera (scales, mealybugs, treatment process on commodity quality aphids and whiteflies) and Thysanoptera (Paull, 1994). (thrips) are based on a small number of Unlike other disinfestation techniques, studies. Two of the most radiotolerant irradiation does not need to kill the pest insects are the Indian meal , Plodia immediately to provide quarantine security, interpunctella, and the Angoumois grain and therefore live (but sterile or not moth, Sitrotroga cerealella, both stored viable) insects may occur with the exported products pests (Ahmed, 2001, Ignatowicz, commodity making inspection for the 2004). The Angoumois grain moth target pests redundant as a confirmation reproduced at 500 but not 600 Gy of treatment application and efficacy. (Ignatowicz, 2004). Most insects are This places an added level of importance controlled at doses below 300 Gy. Several on the certification procedures for species of mites have been tested and irradiation facilities and proper they appear to be relatively tolerant of documentation accompanying export ionizing radiation. Theoretically, the high shipments confirming treatment at dose in the range for each pest group in approved doses. It also places an added Table 1 could be used as a generic dose. responsibility on researchers to ensure However, the dose ranges are often that the minimum absorbed dose approved estimates from limited data or from a for each quarantine pest has an adequate limited sample of species within the margin of safety. Irradiation technology group. Few studies have conducted the is not universally accepted as a large-scale validation tests needed to phytosanitary treatment (Follett and Neven, confirm the efficacy of an irradiation dose

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 2 Table 1.! Range of doses predicted to control various arthropod pest groups Pest Group Desired Response Dose Range (Gy) Hemiptera Sterilize adult or prevent generation turnover 50-250 Thrips Sterilize actively reproducing adult 150-350 Tephritid fruit flies Prevent adult emergence from eggs/larva 50-150 Bruchid seed weevils Sterilize actively reproducing adult 70-300 Curculionid weevils Sterilize actively reproducing adult 80-150 Scarab beetles Sterilize actively reproducing adult 50-150 Stored product beetles Sterilize actively reproducing adult 50-250 Stored product moths Sterilize actively reproducing adult 100-600 Lepidopteran borers Prevent adult emergence from eggs/larva 100-250 Sterilize adult from late pupa 200-400 Mites Sterilize actively reproducing adult 200-400 Modified from FAO (2003)

predicted to give 100% mortality (discussed desired response required for regulatory below). purposes because it prevents the emergence of adult flies that could be trapped and Methodology for developing irradiation trigger regulatory actions, despite being quarantine treatments sterile. When the insect pupates in the The goal of irradiation as a host, preventing adult emergence may be phytosanitary treatment is to provide difficult so adult sterility is the goal. quarantine security for any regulated Often adults occur with the commodity pests residing in or on the exported (e.g. Follett, 2006a). When the adult commodity. This is most often accomplished stage can occur in the commodity and is by preventing development to the the most tolerant stage, the measure of reproductive stage or sterilizing the treatment efficacy is the level of sterility. reproductive stage of the insect. For sexually reproducing species, sterilizing If multiple species on a commodity one sex may be sufficient to prevent are regulated pests, irradiation studies reproduction but both sexes must be begin by comparing the tolerance of the sterilized if mating status is unknown as quarantine pests, then, in-depth studies is usually the case. Males are often but focus on the most tolerant stage of the not always more tolerant than females. most tolerant species, to arrive at a Reciprocal crosses between irradiated and single dose providing quarantine security control males and females at several for the commodity. Typically the most sub-sterilizing doses are useful to advanced developmental stage of the determine the more tolerant sex (Follett insect occurring in the commodity is the and Lower, 2000). In large-scale validation most tolerant when the goal is preventing tests, males and females should be mated adult emergence or reproduction. The before treatment and females should have most advanced stage may be the larva (or begun ovipositing. After irradiation nymph), pupa, or adult. When larval treatment, surviving males and females development is completed in the host but are combined and allowed to mate and the insect pupates outside the host, reproduce to determine the success of the irradiation is applied to prevent adult dose. Adult females irradiated at a emergence. In the case of tephritid fruit sterilizing dose will often oviposit flies, preventing adult emergence is the (particularly if they were gravid when

Irradiation for Postharvest Control of Quarantine Insects 3 irradiated) but eggs will not hatch or increase radio-tolerance) (Follett and hatching neonates do not develop. With Armstrong, 2004, Hallman, 2004). If asexual species the female is the focus of artificial inoculation is used, insects should all tests. In rare cases irradiated insects be placed where they occur naturally or will recover so it is important to continue allowed time to redistribute to preferred tests until all insects have died. feeding sites in the commodity. Dosimeters Many insect species have life history should be placed where the insects occur attributes that complicate testing methods. to accurately measure absorbed doses. For example, diaspidid scale insects are Once dose response tests are completed, sessile (attached to the plant) and long- large-scale tests are conducted with the lived, and so experiments must use host most tolerant life stage at a dose material (e.g. pumpkin) that does not predicted to cause 100% mortality. The deteriorate after irradiation treatment dose determined to provide quarantine and before the insects die. Some species security from testing large numbers of require live host material to survive. The insects is often higher than that predicted long-lived semi-sessile coccid scale, green from small-scale dose response tests to scale (Coccus viridis) only survives on give 100% mortality. Insects are irradiated live host material such as gardenia, in the commodity after inoculation with a coffee and hibiscus, which complicates known number of insects or in naturally testing since irradiation treatment causes infested host material. For internal rapid plant deterioration (Hara et al., feeding insects naturally infesting the 2002). Diapausing and non-diapausing commodity, the number of viable insects strains of insects may have different treated is estimated by the number of tolerances to radiation, and may require insects successfully emerging in paired different bioassay methods (Hallman, samples of untreated controls. Untreated 2003). control insects are always included in To determine the most tolerant stage tests with irradiated insects so that for a species, all stages are treated with a mortality can be adjusted for natural range of irradiation doses. Generally five variation and to guard against changes doses should be selected and five replicates in experimental conditions over the of at least 30-50 insects should be used. course of testing that cause higher than In some cases a single diagnostic dose is normal mortality. While control mortality used to separate tolerance among stages ≤ 20% is desirable, higher mortality may or species. The ideal diagnostic dose be normal when using wild insects and causes only moderate mortality in the naturally infested commodities. stage or species predicted to be most Probit analysis is the standard tolerant. This improves the chances that method to evaluate dose response data, statistical tests can be used to separate but other models (e.g. logit) should be mean responses among groups. Tests used if they provide a better fit to the should be designed with the biology of data (Robertson et al., 1994). These the insect in mind, and insects should analyses are used to compare radiotolerance always be tested in the commodity of among life stages or species, and to help interest if possible. For example, pupae identify a target dose for large-scale may be inherently more tolerant of testing. Covariance analysis is an irradiation than larvae but because they alternative to compare response among only occur at the surface of the fruit they stages or between species. Covariance may be easier to sterilize than larvae analysis requires the slopes of the that feed at the center of the fruit where regression lines fitted to each group to be hypoxic conditions exist (low oxygen can parallel, so the test of parallelism

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 4 (nonsignificant stage or species by dose 3:1. High DURs are the result of product interaction effect) is tested before comparing volume and density, not the size of the stage or species effects (e.g. Follett and irradiator. When using commercial irradiators Armstrong, 2004). for research applications, DURs can be As mentioned, the actual dose to minimized by presenting product of achieve quarantine security at a given minimal depth (e.g. individual fruits) and level of precision may exceed the dose irradiating the product in a forward then predicted from small-scale dose response reverse orientation. For example, Follett tests. For example, the dose predicted to and Armstrong (2004) irradiated fruit fly prevent emergence of adult melon flies larvae in papayas at a commercial x-ray treated in papaya from dose response facility using an electron linear accelerator data was 90 Gy (0 survivors in 900 tested (5 MeV, model TB-5/15, SureBeam Corp., insects) (Follett and Armstrong, 2004); San Diego, California). To minimize the however, subsequent large-scale testing DUR, infested fruit were placed upright at 120 Gy resulted in 1 survivor out of in plastic tubs in a single row perpendicular 50,000 treated third instars and several to the beam. Dose mapping demonstrated partially emerged pupae. Increasing the that doses were sometimes lower near the dose for large-scale testing to 150 Gy sides and floor of the metal carrier, so resulted in 0 survivors in 96,700 treated the tubs with fruit were elevated by insects and no partial pupal emergence placement on a cardboard box and (Follett and Armstrong, 2004). This positioned in the exact center of the demonstrates the need for large-scale carrier. Each carrier passes in front of testing to verify a dose. the beam in a forward then reverse Accurate dosimetry is critical to the orientation. DURs in this study were success of insect irradiation studies. The consistently < 1.2 (Follett and Armstrong, objective in research is to minimize the 2004). dose uniformity ratio (DUR) (also called the maximum:minimum ratio), thus reducing Probit 9 treatments variation in dose response tests. This The question always arises: How allows the researcher to more accurately many insects must be tested during pinpoint an efficacious dose without research to demonstrate that a treatment excessive overkill. The maximum dose provides quarantine security? Future trade measured during large-scale testing becomes between countries in a commodity that is the minimum dose for a treatment potentially infested by a quarantine pest (Heather, 2004). Dose rate decreases with can be slowed by the lack of a the square of the distance from the standardized research protocol for developing source (e.g. if distance from source is a quarantine treatment or system. The doubled, dose rate decreases by a factor exporting country must often initiate of 4). Small scale research irradiators research on a crop or quarantine pest such as the Gammacell 220 types (MDS without full knowledge of the commitment Nordion, Canada) have a small radiation of time and resources involved because chamber volume and hence all locations the importing country has not published in the product during irradiation are a or explicitly outlined a research protocol. short distance from the source and DURs Hence the number of insects to treat in can be minimized (typically < 1.2:1). It is validation tests and other research generally accepted that large-scale requirements can vary dramatically commercial irradiators are not useful for depending on the pest, the crop, and the conducting dose response research because country. of high DURs, sometimes in the range of In the U.S., post-harvest commodity

Irradiation for Postharvest Control of Quarantine Insects 5 treatments for pests requiring a high during quarantine treatment development if degree of quarantine security are the potential economic and environmental commonly referred to as probit 9 treatments. impact of the pest should it be introduced The reference originates from the statistical is low. For example, irradiation treatment method (probit analysis) used for deriving with a dose of 300 Gy was accepted for the dose-response relationship. A response the mango seed weevil, Sternochetus at the probit 9 level results in 99.9968% mangiferae (F.) by Animal and Plant efficacy. The required response may be Health Inspection Service, USDA (USDA- mortality, sterility, or prevention of maturity. APHIS, 2002), a monophagous pest of The United States Department of Agriculture mangos, based on evidence for the weevil’s (USDA) has used 99.9968% efficacy as the limited potential impact on U.S. agriculture basis for approving many quarantine (Follett and Gabbard, 2000), and cumulative treatments, particularly for tephritid fruit data from several studies with a few flies. A probit 9 treatment usually provides thousand insects showing prevention of adequate quarantine security, and developing adult emergence from the fruit at this the treatment frequently proves to be the dose and sterilization at lower doses (Seo quickest and most easily accepted method et al., 1974, Heather and Corcoran, 1992, for overcoming phytosanitary restrictions Follett, 2001). (Follett and Neven, 2006). Irradiation negatively affects commodity To achieve probit 9 mortality at the quality in some cases. Lowering the 95% confidence level, a minimum of irradiation dose may reduce the 93,613 insects must be tested with no undesirable effects on the commodity. survivors after exposure to the treatment. Landolt et al. (1984) pointed out that the Quantitative methods have been developed probit 9 standard may be too stringent to calculate the number of test insects for commodities that are rarely infested and confidence limits for other levels of or are poor hosts, and hence a less severe precision and treatment efficacy, with post-harvest treatment might still provide and without survivors (Couey and Chew, quarantine security. The less-than-probit 1986). Although probit 9 testing seems 9 or alternative treatment efficacy approach like a comfortable level of safety, given a measures risk as the probability of a highly-infested commodity or a high enough mating pair or reproductive individual volume of infested commodity imports, even surviving in a shipment. This will be a probit 9 security could be overwhelmed function of many biological, operational, (Mangan et al., 1997, Powell, 2003). Other and environmental factors (Vail et al., countries (Japan, Australia, New Zealand) 1993, Yamamura and Katsumata, 1999, accept quarantine treatment efficacy at Follett and Neven, 2006). The main 99.99% (at the 95% confidence level), which quantitative argument for deviating from is obtained by treating 29,956 insects with probit 9 treatment efficacy is low infestation no survivors (Couey and Chew, 1986). Japan rate of the commodity, resulting from requires a total of 30,000 individuals in poor host status, early harvesting, or 3-4 trials (Sproul, 1976), New Zealand effective pre-harvest pest suppression. requires three replicates of 10,000 test A number of quarantine pest-commodity insects, and Australia accepts a cumulative systems are amenable to the less-than- total of 30,000 treated insects with no probit 9 approach (Liquido et al., 1995, survivors (Heather and Corcoran, 1992). Follett and McQuate, 2001). For example, nectarines are an inherently poor host for Alternative approaches codling moth, Cydia pomonella (L.). Only In certain cases, less-than-probit 9 three live codling moths (larvae) were numbers of insects may be acceptable found infesting 326,625 packed nectarines

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 6 sampled from packinghouses in the San limited geographic area for distribution Joaquin Valley of California for an (i.e. to non-fruit fly supporting areas). infestation rate of 9.2 x 10-6 (Curtis et al., 1991). In an average shipment of 16,000 Generic irradiation doses kg (89,600 fruits), the probability of one A generic treatment, a single or more mating pairs surviving after a treatment that controls a broad group of probit 9-level quarantine treatment is 1.7 pests without affecting the quality of a x 10-10. The actual mortality level required wide range of commodities, is the ultimate from a quarantine treatment to prevent a discovery sought after by quarantine mating pair of codling moths in a single entomologists, albeit seldom found. Most shipment of nectarines with 95% confidence quarantine treatments are developed for is 77.74% (probit 5.65). Hypothetically, if one pest and one commodity at a time, 100 shipments arrived at the same and research may take several years. location the probability of one or more Generic treatments for broad groups of codling moth mating pairs surviving in pests and commodities accelerate the nectarines after a probit 9-level quarantine research, shorten treatment development, treatment is still extremely small (1.7 x and save resources. Irradiation is the 10-6). In this case, a probit-9 treatment ideal technology for developing generic provides a high level of overkill and a treatments because radiation– from an less severe treatment might be developed isotope source such as cobalt-60, or that provides adequate quarantine security x-rays– penetrates fruit easily and is while minimizing any negative effects of effective against insects at doses that the treatment on commodity quality. Low generally do not injure the commodity. infestation rate at harvest can also be the A generic treatment for a group of result of effective pest management insects could be applied at many before harvest and/or the harvest of taxonomic levels, e.g. to all Diptera (flies), climacteric fruit (those that continue to or to flies in the family Tephritidae (fruit ripen after harvest) at a less susceptible flies), or to tephritid fruit flies in the or non-preferred maturity stage. An genus Bactrocera. A generic irradiation additional advantage to use of the less- dose is recommended after information than-probit 9 approach is that fewer has accumulated on effective quarantine insects may be needed during research to irradiation doses for a wide range of develop quarantine treatments, which insects within the taxon or for the would make new treatments available on important economic pests within the a more timely basis (Follett and McQuate, taxon (Follett and Neven, 2006, Bakri 2001). and Hendrichs, 2004). The rationale is The less-than-probit 9 approach fits that related species are likely to be with the systems approach where multiple similar in their radio-tolerance, and therefore procedures are used to cumulatively provide data for a limited number of species can quarantine security while maintaining be extrapolated to other related species to quality in a commodity that is sensitive arrive at a generic dose. to a particular quarantine treatment Recently, generic irradiation treatments (Jang and Moffitt, 1994). For example, a were approved for the first time. On less-than-probit 9 irradiation dose for a January 27, 2006, USDA-APHIS approved fruit fly might be part of a systems generic doses of 150 Gy for tephritid fruit approach that included effective pest flies and 400 Gy for all insects except suppression in the crop, poor host status, pupa and adult Lepidoptera (USDA- fruit cutting and inspection, limited APHIS, 2006). The rule also included distribution period (winter months), and lower doses for a number of well-studied

Irradiation for Postharvest Control of Quarantine Insects 7 Table 2.! Irradiation doses approved for insects and insect groups by the USDA Scientific Name Common name Dose (Gy) Anastrepha ludens Mexican fruit fly 70 Anastrepha obliqua West Indian fruit fly 70 Anastrepha serpentina Sapote fruit fly 100 Anastrepha suspensa Caribbean fruit fly 70 Bactrocera jarvisi (none) 100 Bactrocera tryoni Queensland fruit fly 100 Brevipalpus chilensis False red spider mite 300 Conotrachelus nenuphar Plum curculio 92 Cryptophlebia ombrodelta Litchi fruit moth 250 Cryptophlebia illepida Koa seedworm 250 Cylas formicarius elegantulus Sweetpotato weevil 150 Cydia pomonella Codling moth 200 Euscepes postfasciatus West Indian sweetpotato weevil 150 Grapholita molesta Oriental fruit moth 200 anastomosalis Sweetpotato vine borer 150 Rhagoletis pomonella Apple maggot 60 Sternochetus mangiferae Mango seed weevil 300 Fruit flies in the family Tephritidae not listed above 150 Plant pests of the Insecta not listed above, except Lepidoptera pupae and adults 400 Source: Federal Register 2006

quarantine insect species (Table 2). The New Zealand prepared a rule to allow generic and specific irradiation doses import of tropical fruits from Australia apply to all agricultural commodities. using generic irradiation treatments of 150 The generic dose for tephritid fruit flies Gy for fruit flies, 250 Gy for other insects, of 150 Gy was based on data for 17 and 300 Gy for mites (Corcoran and species of Anastrepha, Bactrocera, Ceratitis, Waddell, 2003). Any country negotiating and Rhagoletis fruit flies (Hallman and trade in a fresh fruits and vegetables Loaharanu, 2002, Follett and Armstrong, with the U.S. can use the generic 2004). The default dose of 400 Gy for all irradiation treatments, and adoption of insects except pupae and adults of these or other generic irradiation doses Lepidoptera was recommended after for tephritid fruit flies and other insect critical analysis of the literature (Follett groups by other countries is anticipated. and Hallman unpublished report). The The generic irradiation doses can be default dose was first used for sweet lowered for specific pests and commodities potatoes exported from Hawaii to the if this is practical. For example, papayas U.S. mainland. With the default dose exported from Hawaii to the U.S. mainland approach, an irradiation dose is set at the are routinely irradiated at a minimum upper limit of what is believed to control dose of 400 Gy to control white peach the insect groups that infest a commodity scale (Pseudaulacaspis pentagona) in addition without specific data for the quarantine to fruit flies because no information was species. A default dose of 400 Gy was available the radiotolerance of this scale. used for Hawaii (USDA-APHIS, Recent studies demonstrated that white 2004) until research later demonstrated peach scale is controlled at 150 Gy that 150 Gy was sufficient (Follett, 2006a). (Follett, 2006b). Hence, an irradiation

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 8 treatment with a minimum absorbed dose studies published recently on pests of of 150 Gy should provide quarantine stored products, such as the cigarette security for white peach scale in addition beetle, Lasioderma serricorne (Hu et al., to fruit flies on exported papaya. Lowering 2002a), rice weevil, Sitophilus oryzae (Hu the dose will significantly reduce costs of et al., 2002b), maize weevil, S. zeamais treatment and increase capacity of the (Hu et al., 2003), and the carambola fruit treatment facility. borer, Eucosma notanthes (Lin et al. Theoretically, a universal irradiation 2003). dose could be set for all insects. The most The United States and Taiwan are radio-tolerant insect species reported to negotiating trade in Taiwan longan. The date is the Angoumois grain moth, a first step in the process is the stored product pest which successfully preparation of a pest risk assessment. reproduced after irradiation treatment at This document is a listing of all the a dose of 500 Gy but not at 600 Gy insect, disease and weed species associated (Ignatowicz, 2004). If this is indeed the with the commodity, and a risk rating for most tolerant insect, irradiation treatment each pest. This list is used to develop risk with a minimum absorbed dose of 600 Gy mitigation or control options for the pests should control any insect. A limiting so that the commodity can be exported. factor for the practical use of a generic The tentative list of high- and medium- treatment at 600 Gy in the U.S. is the risk pests that might occur in exported 1000 Gy (1 kGy) maximum allowed dose Taiwan longan is presented in Table 3 for fresh produce set by the Food and (USDA-APHIS personal communication). Drug Administration. With typical dose This is a relatively long list, consisting of uniformity ratios at commercial irradiation 5 high risk pests and 21 medium risk facilities of 1.5-3.0, treatment to achieve pests. By comparison, the pest risk a minimum absorbed dose of 600 Gy assessment for Hawaii’s longan exported without exceeding 1 kGy would be difficult. to the U.S had 4 high risk pests (B. Also, doses above 600 Gy adversely affect dorsalis, B. cucurbitae, and Ceratitis the quality of many fresh commodities capitata, and M. hisutus) and 3 medium (Morris and Jessup, 1994). Another approach risk pests (including Cryptophlebia would be to set the generic dose for ombrodelta). Typically, high-risk pests insects at a dose lower than 600 Gy and require a proven mitigation procedure exclude any species or insect groups such as a quarantine treatment, whereas found to tolerate a dose above this level medium-risk pests may not require a (Follett and Armstrong, 2004, Follett and quarantine treatment per se provided Griffin, 2006). infestations can be identified during inspection. Case study: Longan from Taiwan to The simplest and quickest risk mitigation the U.S. option for Taiwan longan is irradiation at One of the earliest published studies a dose of 400 Gy. The generic treatment examining the use of irradiation as a rule provides a treatment of 400 Gy to quarantine treatment was by Koidsumi control all insects except Lepidoptera (1930) in Taiwan (Formosa). He systematically (moths and butterflies) pupae and adults. tested the lethal effects of various If none of the Lepidoptera associated with dosages of X-ray to oriental fruit fly, Taiwan’s longan are associated with the Bactrocera dorsalis, and melon fly, B. fruit as pupae or adults, 400 Gy is a curcubitae, at different developmental ready-made treatment. Research has shown stages. Irradiation continues to be a topic that longan is tolerant of irradiation at of interest in Taiwan, with several 400 Gy, and irradiation is superior to an

Irradiation for Postharvest Control of Quarantine Insects 9 Table 3.! High- and medium-risk pests identified in a draft USDA-APHIS pest risk assessment for longan imported from Taiwan Species USDA-Approved Dose Suggested Dose Reference High risk Diptera Bactrocera cucurbitae 150 150 Follett and Armstrong 2004 Bactrocera dorsalis 150 150 Follett and Armstrong 2004 Lepidoptera Conogethes punctiferalis -- -- Cryptophlebia ombrodelta 250 250 Follett and Lower 2000 Thysanoptera Rhipiphorothrips cruentatus -- --

Medium risk Hemiptera Ceroplastes rubens 400 -- Coccus discrepans 400 -- Coccus formicarii 400 -- Coccus viridis 400 250 Hara et al. 2002 Drepanococcus chiton 400 -- Pulvinaria taiwana 400 -- Aulcaspis tubercularis 400 -- Fiorinia pinicola 400 -- Pseudaonidia trilobitiformis 400 -- Thyssanofiorinia nephelii 400 -- Kerria greeni 400 -- Kerria lacca 400 -- Icerya seychellarum 400 -- Maconellicoccus hirsutus 400 250 Jacobson and Hara 2003 Nipaecoccus viridis hirsutus 400 -- Planococcus lilacinus 400 -- Planococcus minor 400 -- Lepidoptera Conopomorpha litchiella 400 250 Hu et al. 1999 Deudorix epijarbas 400 -- Dichocrocis punctiferalis 400 -- Adoxophyes orana 400 -- Source: USDA APHIS Pest Epidemiological Risk Analysis Laboratory, Raleigh, North Carolina

alternative treatment, hot water immersion 150 and 250 Gy, respectively, but there (Follett and Sanxter, 2002). are no approved irradiation doses for It may be possible to reduce the Conogethes punctiferalis (yellow peach irradiation dose from 400 Gy if research moth) or Rhipiphorothrips cruentatus can show a lower dose is sufficient to (Table 3). Research should be initiated to control the high-risk pests. For longan, identify effective irradiation doses for approved doses for the two tephritid fruit these quarantine pests. The dose for an flies and Cryptophlebia ombrodelta are irradiation treatment for longan would be

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 10 the dose that controls the most tolerant Ahmed M. 2001. Infestation of stored high-risk species. Irradiation studies have grains, pulses, dried fruits and nuts, been conducted on only a few of the and other dried foods. p. 77-112. In: medium-risk pests on the list. Food Irradiation: Principles and Applications (Molins, R. A. ed.). John Conclusions Wiley & Sons, Inc., New York. Bakri, A., and J. Hendrichs. 2004. The availability of generic dose Radiation doses for sterilization and treatments makes irradiation an attractive disinfestations of tephritid fruit flies. option compared with other quarantine In: Barnes, B., ed. pp. 475-479. treatments. Developing irradiation treatments Proceedings of the 6th. International for taxonomic groups or guilds of insects Symposium on Fruit Flies of and groups of commodities rather than Economic Importance. Isteg Scientific for individual pests and commodities Publications, Irene, South Africa. helps avoid unnecessary research, and Bakri, A., N. Heather, J. Hendrichs, and I. regulatory and trade bottlenecks. An Ferris. 2005. 50 Years of radiation International Database of Insect biology in entomology: Lessons learned Disinfestation and Sterilization (IDIDAS, from IDIDAS. Ann. Entomol. Soc. 2005; Bakri et al., 2005) developed by the Am. 98: 1-12. International Atomic Energy Agency and Corcoran, R. J., and B. C. Waddell. 2003. the Food and Agriculture Organization of Ionizing energy treatments for the United Nations contains radiotolerance quarantine disinfestation. Horticulture information for many Coleoptera (79 Australia Limited. species, mainly curculionids), Lepidoptera Couey, H. M., and V. Chew. 1986. (72 species, mainly pyralids and tortricids), Confidence limits and sample size in and other pest groups. Information could quarantine research. J. Econ. Entomol. be gleaned from the database to set 79: 887-890. additional generic doses although the Curtis, C. E., J. D. Clark, and J. S. majority of the studies referenced in the Tebbetts. 1991. Incidence of codling database for individual species were not moth (Lepidoptera: Tortricidae) in designed for quarantine purposes and packed nectarines. J. Econ. Entomol. lack the large-scale tests needed to 84: 1686-1690. confirm the efficacy of an irradiation FAO (Food and Agriculture Organization). dose. Data for other important regulatory 2003. Guidelines for the use of arthropod groups such as Thysanoptera, irradiation as a phytosanitary measure. Hemiptera, and Acari are limited. Before International Plant Protection generic treatments below 400 Gy can be Convention, ISPM No. 18, Rome, recommended for a wider range of insect Italy. groups, information from coordinated Follett, P. A. 2001. Irradiation as a research projects and large-scale tests is quarantine treatment for mango seed needed on effective irradiation doses for weevil (Coleoptera: Curculionidae). key pests and under-represented taxa. Proc. Hawaiian Entomol. Soc. 35: Generic irradiation treatments will accelerate 95-100. the approval of irradiation quarantine Follett P. A. 2006a. Irradiation as a treatments for specific crops and expedite methyl bromide alternative for new trade in agricultural products. postharvest control of Omphisa anastomosalis (Lepidoptera: Pyralidae), References Euscepes postfasciatus and Cylas formicarius elegantulus (Coleoptera:

Irradiation for Postharvest Control of Quarantine Insects 11 Curculionidae) in sweet potatoes. J. J. Econ. Entomol. 96: 1399-1404. Econ. Entomol. 99: 32-37. Hallman, G. J. 2004. Irradiation disinfestation Follett, P. A. 2006b. Irradiation as a of apple maggot (Diptera: Tephritidae) phytosanitary treatment for white in hypoxic and low-temperature storage. peach scale (Homoptera: Diaspididae). J. Econ. Entomol. 97: 1245-1248. J. Econ. Entomol. 99: 1974-1978. Hallman, G. J., and P. Loaharanu. 2002. Follett, P. A., and J. W. Armstrong. 2004. Generic ionizing radiation quarantine Revised irradiation doses to control treatments against fruit flies (Diptera: melon fly, Mediterranean fruit fly Tephritidae) proposed. J. Econ. Entomol. and oriental fruit fly (Diptera: 95: 893-901. Tephritidae) and a generic dose for Hara, A. H., J. A. Yalemar, E. B. Jang, and tephritid fruit flies. J. Econ. Entomol. J. H. Moy. 2002. Irradiation as a 97: 1254-62. possible quarantine treatment for Follett, P. A., and Z. Gabbard. 2000. green scale Coccus viridis (Green) Effect of mango weevil (Coleoptera: (Homoptera: Coccidae). Postharvest Curculionidae) damage on mango Biol. Technol. 25: 349-358. seed viability. J. Econ. Entomol. 93: Heather, N. W. 2004. Generalized quarantine 1237-1240. disinfestation research protocol. p. Follett, P. A., and R. Griffin. 2006. 171-78. In: Irradiation as a Phytosanitary Irradiation as a phytosanitary treatment Treatment of Food and Agricultural for fresh horticultural commodities: Commodities. IAEA Techdoc 1427, Research and regulations, p. 143-168, Vienna, Austria. In: Sommers, C. H., and X. Fan, eds. Heather, N. W., and R. J. Corcoran. 1992. Food Irradiation Research and Effects of ionizing energy on fruit Technology. Ames: Blackwell. flies and seed weevil in Australian Follett, P. A., and R. Lower. 2000. mangoes. In: Proceedings: Final Irradiation to ensure quarantine Research Coordination Meeting on security for Cryptophlebia spp. Use of Irradiation as a Quarantine (Lepidoptera: Tortricidae) in sapindaceous Treatment of Food and Agricultural fruits from Hawaii. J. Econ. Entomol. Commodities, Kuala Lumpur, , 93: 1848-1854. pp. 43-52. International Atomic Energy Follett, P. A., and G. T. McQuate. 2001. Agency, Vienna, Austria. Accelerated development of quarantine Hu, M Y., X. Q. Liu, R. H. Hou, X. D. Li, Z. treatments for insects on poor hosts. W. Yao, X. M. Lou, and Q. F. Weng. J. Econ. Entomol. 94: 1005-1011. 1999. Disinfestation of litchi stem- Follett, P. A., and L. G. Neven. 2006. end borer Conopomorpha sinensis Current trends in quarantine entomology. Bradley with irradiation for export of Annu. Rev. Entomol. 51: 359-385. litchi fruit. p. 115-122, In: Proceedings Follett, P. A., and S. S. Sanxter. 2002. of the Final Research Co-ordination Longan quality after hot-water Meeting on Irradiation as a Quarantine immersion and x-ray irradiation Treatment of Arthropod Pests, IAEA- quarantine treatment. HortScience Techdoc-1082, International Atomic 36: 571-574. Energy Agency, Vienna, Austria. Hallman, G. J. 2000. Expanding radiation Hu, T., C. C. Chen, and W. K. Peng. 2002a. quarantine treatments beyond fruit The lethal effect of gamma radiation flies. Agr. Forest Entomol. 2: 85-95. on Lasioderma serricorne (Fabricius) Hallman, G. J. 2003. Ionizing irradiation (Coleoptera: Anobiidae). Formosan quarantine treatment against plum Entomol. 22: 157-162. (in Chinese curculio (Coleoptera: Curculionidae). with English abstract)

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 12 Hu, T., C. C. Chen, and W. K. Peng. 2002b. 2003. Effects of gamma radiation on Lethal effect of gamma radiation on survival and reproduction of the Sitophilus oryzae (L.) (Coleoptera: carambola fruit borer, Eucosma Curculionidae). Formosan Entomol. notanthes Meyrick (Lepidoptera: 22: 229-236. (in Chinese with English Tortricidae). Formosan Entomol. 23: abstract) 189-197. (in Chinese with English Hu, T., C. C. Chen, and W. K. Peng. 2003. abstract) Lethal effect of gamma radiation on Liquido, N. J., R. L. Griffin, and K. W. Vick. Sitophilus zeamais (L.) (Coleoptera: 1995. Quarantine security for Curculionidae). Formosan Entomol. commodities: current approaches and 23: 145-150. (in Chinese with English potential strategies. USDA Publication abstract) Series 1996-04. IDIDAS. 2005. International Database on Mangan, R. L., E. R. Frampton, D. B. Insect Disinfestation and Sterilization. Thomas, and D. S. Moreno. 1997. website: www-ididas.ieae.org/ididas/. Application of the maximum pest International Atomic Energy Agency, limit concept to quarantine security Vienna. standards for the Mexican fruit fly Ignatowicz, S. 2004. Irradiation as an (Diptera: Tephritidae). J. Econ. alternative to methyl bromide Entomol. 90: 1433-1440. fumigation of agricultural commodities Morris, S. C., and A. J. Jessup. 1994. infested with quarantine stored product Irradiation. p. 163-190. In: Paull, R. pests. In: Irradiation as a Phytosanitary E., and J. W. Armstrong, eds. Insect Treatment of Food and Agricultural Pests and Fresh Horticultural Products: Commodities, pp. 51-66. International Treatments and Responses. CAB Atomic Energy Agency TECDOC International, Wallingford, UK. 1427, Vienna. Paull, R. E. 1994. Response of tropical Jacobson, C. M., and A. H. Hara. 2003. horticultural commodities to insect Irradiation of Maconellicoccus hirsutus disinfestation treatments. HortScience (Homoptera: Pseudococcidae) for 29: 988-996. phytosanitation of agricultural Powell, M. R. 2003. Modeling the commodities. J. Econ. Entomol. 96: response of the Mediterranean fruit 1334-1339. fly (Diptera: Tephritidae) to cold Jang, E. B., and H. Moffitt. 1994. Systems treatment. J. Econ. Entomol. 96: approaches to achieving quarantine 300-310. security. p. 225-237. In: Sharp, J. L., Robertson, J. L, H. K. Preisler, E. R. and G. J. Hallman eds., Quarantine Frampton, and J. W. Armstrong. 1994. Treatments for Pests of Food Plants. Statistical analyses to estimate Westview Press, Boulder, Colorado. efficacy of disinfestations treatment. Koidsumi, K. 1930. Quantitative studies In: Sharp, J. L., and G. J. Hallman, on the lethal action of X-rays upon eds. Quarantine Treatments for Pests certain insects. J. Soc. Trop. Agric. of Food Plants, pp. 47-66. Boulder: (Japan) 2: 243-263. Westview. Landolt, P. J., D. L. Chambers, and V. Seo, S. T., R. M. Kobayashi, D. L. Chew. 1984. Alternative to the use of Chambers, D. M. Dollar, and M probit 9 mortality as a criterion for Hanaoka. 1974. Hawaiian fruit flies quarantine treatments of fruit fly in papaya, bell pepper, and eggplant: (Diptera: Tephritidae) infested fruit. J. quarantine treatment with gamma Econ. Entomol. 77: 285-287. irradiation. J. Econ. Entomol. 66: Lin, J. Y., S. B. Horng, and C. C. Hung. 937-939.

Irradiation for Postharvest Control of Quarantine Insects 13 Sproul, A. N. 1976. Disinfestation of USDA-APHIS. 2006. Treatments for fruits Western Australian Granny Smith and vegetables. Federal Register 71 apples by cold treatment against the (18): 4451-4464., June 26, 2006. Rules egg and larval stages of the and Regulations. Mediterranean fruit fly (Ceratitis Vail, P. V., J. S. Tebbetts, B. E. Mackey, capitata (Wied.)) Aust. J. Exp. Agric. and C. E. Curtis. 1993. Quarantine Anim. Husb. 16: 280-285. treatments: a biological approach to Thomas, P. 2001. Irradiation of fruits and decision making for selected hosts of vegetables. pp. 213-240., In: Molins, codling moth (Lepidoptera: Tortricidae). R., ed. Food Irradiation. Wiley and J. Econ. Entomol. 86: 70-75. Sons, New York. Yamamura, K., and H. Katsumata. 1999. USDA-APHIS. 2002. Irradiation Phytosanitary Estimation of the probability of an Treatment of Imported Fruits and insect pest introduction through Vegetables. Federal Register 67 (205): imported commodities. Res. in Pop. pp. 65016-65029. Rules and Regulations. Ecol. (Japan) 41: 275-282. USDA-APHIS. 2004. Irradiation of sweet potatoes from Hawaii. Federal Register Received: July 7, 2006 69 (32): pp. 7541-7547., February 18, Accepted: November 6, 2006 2004, Rules and Regulations.

ௐ˘ഇס˛˩˟ᖪௐٿέ៉ 14 ఍நޢᑭࠪचᖪ̝ଳٺᏬड໰ड

Peter A. Follett! U.S. Department of Agriculture, Agricultural Research Service, U.S. Pacific Basin Agricultural Research Center, Hilo, Hawaii 96720, U.S.A. ཱི ᖪጯր! έ̚ξ 402 ઼Ѝྮ 250ٿ໅તӻ! ྮЍິ*! ઼ϲ̚Ꮈ̂ጯ ᑭࠪ௡! έΔξ 100 ࢦᇉݑྮ˟߱ 51 ཱི 9 ሁۏࠪᑭࠪԊങ֨ۏౘ̄ઈ! Җ߆ੰྺຽ؎ࣶົજങ

ၡ!!ࢋ

ܕʑĄ̝ڱ఍ந͞۞ۏᏬड໰डĞirradiationğѝ̏జϡࠎໝੵྺயݡ˯ѣचϠ!! ,᜕̳ࡗĞThe International Plant Protection Conventionܲۏᅫങ઼ٺѐֽϤ ؠ˞ֹϡᏬड໰डซҖᑭࠪ఍நĞphytosanitary treatmentğ۞઼ᅫఢቑĂטIPPCğ Ч઼۞ࢦෛĄ˘ਠྺயݡགྷϤዋ༊۞Ꮼड໰ड጗ณĂӈΞд̙ᇆᜩזצՀֹܳ׎ు႙ Ğdisinfestation effectğĄᄃڍĂ၆кᇴचᖪĞ螨ğயϠ։р۞ໝੵड़˭ڶݡኳ۞ଐ ࠹ྵĂᏬड໰ड఍ந̙֭ͽϲӈ୭ѪचᖪĞ螨ğ۞͞ёֽቁܲᑭࠪڱ׎΁ᑭࠪ఍ந͞ щБّĄЯࠎགྷ࿅Ꮼड໰ड఍ந̝ྺயݡĂᔵ൒׎̚۞ᑭࠪचᖪĞ螨ğ̪Ξਕх߿Ă۞ ͼѪ˸۞Ăซ˾઼̙֭ᅮࢋГਈ෱ჟ˧ᑭෛιࣇߏӎхдĄܕҭιࣇ̏ߏ̙θ۞ٕߏ Հࢎؠ˞Ꮼड໰डઇࠎЧёྺயݡᑭࠪ఍ந۞В఼఍ந጗ณĞgenericعϫ઼݈࡚߆ ၁ᙀ۞В఼఍ந጗ณࠎ 150 GyĂ҃ੵសਂϫ۞ڍtreatment dosesğĂּтໝੵЧᙷ ᄃјᖪĞᅮགྷྵ੼۞጗ณ఍நğͽγĂ׎ιᑭࠪचᖪĞ螨ğ۞В఼఍ந጗ณࠎ 400ུ ତᏮˢĄᏬड໰डВ఼఍ۡޢGyĂ̯֭ధкีགྷѩඈ጗ณ఍ந̝ྺயݡགྷ࿅ᑭࠪᄮᙋ ந጗ณ۞ࢎؠĂ̙ҭΞΐిপؠྺயݡӀϡᏬड໰ड఍நͽ௑ЪᑭࠪࢋՐĂТॡϺΞ ΐి׎΁າྺயݡд઼ᅫξಞ۞ฟ٤ĂЯࠎາ۞ྺயݡ่ᅮֶѩૄ໤఍ந࿅ӈΞ఼࿅ ॡมĂ੫၆̙ТचᖪĞ螨ğซҖЧ჌̙Т۞ᑭࠪ఍நྏ۞ܜᑭࠪᄮᙋĂ̙ᅮГਈ෱̴ В఼఍நٺĂϤڱ׎ιᑭࠪ఍ந͞ٺរĂ̖Ξਕᒔ଀ซ˾઼۞ᑭࠪᄮᙋĄЯѩĂ࠹ྵ Ąڱ΃׎΁ᑭࠪ఍ந۞ആ΃͞פ጗ณ۞ቁϲĂֹ଀Ꮼड໰डјࠎ˘ีஎ׍ሕ˧ă֖ͽ

ᑭࠪ఍நăᑭࠪचᖪăprobit 9 ۞ᏴፄăВ఼఍ந጗ณĄۏᜰᗤຠȈᏬड໰डăങ

*ኢ͛ᓑᘭˠ Irradiation for Postharvest Control of Quarantine Insects 15 e-mail: [email protected]