Factors Affecting Ionizing Radiation Phytosanitary Treatments, and Implications for Research and Generic Treatments Author(S): Guy J

Factors Affecting Ionizing Radiation Phytosanitary Treatments, and Implications for Research and Generic Treatments Author(s): Guy J. Hallman, Nichole M. Levang-Brilz, J. Larry Zettler, and Ian C. Winborne Source: Journal of Economic Entomology, 103(6):1950-1963. 2010. Published By: Entomological Society of America DOI: 10.1603/EC10228 URL: http://www.bioone.org/doi/full/10.1603/EC10228

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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. FORUM Factors Affecting Ionizing Radiation Phytosanitary Treatments, and Implications for Research and Generic Treatments

1 2 3 2 GUY J. HALLMAN, NICHOLE M. LEVANG-BRILZ, J. LARRY ZETTLER, AND IAN C. WINBORNE

J. Econ. Entomol. 103(6): 1950Ð1963 (2010); DOI: 10.1603/EC10228 ABSTRACT Phytosanitary irradiation (PI) treatments are promising measures to overcome quarantine barriers to trade and are currently used in several countries. Although PI has advantages compared with other treatments one disadvantage bedevils research, approval, and application: organisms may remain alive after importation. Although this does not preclude their use as a phytosanitary treatment, it does leave the treatment without an independent veriÞcation of efÞcacy and places a greater burden for assuring quarantine security on the research supporting the treatment. This article analyses several factors that have been hypothesized to affect PI efÞcacy: low oxygen, pest stage, host, dose rate, and temperature. Of these factors, the Þrst is known to affect efÞcacy, whereas host and dose rate probably need more research. The International Plant Protection Convention considered several PI treatments for its international standard on phytosanitary treatments and did not approve some at Þrst because of perceived problems with the research or the presence of live adults after irradiation. Based on these concerns recommendations for research and dealing with the issue of live adults postirradiation are given. Generic PI treatments are suggested.

KEY WORDS quarantine, commodity treatment, irradiation, disinfestation

Ionizing radiation as a phytosanitary treatment is in- commodity or reinfested after treatment. Live pests creasing in commercial use because it possesses some are expected after irradiation, and Þnding them does advantages over other treatments, such as applicabil- not preclude entry of the consignment as long as ity to packed commodities and broad tolerance by treatment certiÞcation is veriÞed. fresh fruit (Heather and Hallman 2008). A major dis- The U.S. Animal and Plant Health Inspection Ser- advantage for plant protection organizations with vice (APHIS) has approved several PI treatments (Ta- phytosanitary irradiation (PI) compared with other ble 1). The International Plant Protection Convention treatments is that PI is the only commercially applied (IPPC) adopted eight in 2009 (FAO 2009b) and re- treatment that does not result in signiÞcant acute cently adopted three more at the Þfth meeting of the mortality, leaving phytosanitary inspectors with no Commission on Phytosanitary Measures (CPM) independent veriÞcation of efÞcacy. This shortfall is (FAO 2010), making 11 adopted PI treatments in total important because major phytosanitary treatments (Table 1). based on heat, cold, and methyl bromide fumigation All of the treatments approved by APHIS by 2006 have apparently failed, and the only way this was were considered for submission to the IPPC vetting known was by the discovery of live insects after treat- process; two were not proposed by APHIS and six ment (Heather and Hallman 2008). These treatments were eliminated during the process at different stages were based on accepted research, and there is no (FAO 2009c, 2010). The following section discusses reason to believe that irradiation could not fail as well the fate of these treatments in the submission and except in this case the failure might not be known. approval process. The measure of efÞcacy of PI is prevention of fur- APHIS did not propose the treatments for Brevi- ther development or successful reproduction (FAO palpus chilensis Baker and Sternochetus mangiferae 2003). If inspectors Þnd live quarantine pests for vir- (F.) (Table 1) because of insufÞcient numbers of tually every other treatment the consignment is re- organisms tested and poor performance of controls. jected or retreated regardless of certiÞcation of treat- The 300-gray (Gy) dose for B. chilensis was conÞrmed ment. It is assumed that the treatment was not with a total of 8,042 irradiated adults, which is not properly done or does not work as applied or that the considered sufÞcient for a mite that may be present in shipment was contaminated with nontreated, infested considerable numbers in regulated articles. Further- more, controls laid a mean of only 1.0 egg per female 1 Corresponding author: USDAÐARS, 2413 E. Hwy. 83, Weslaco, TX with only 33.2% of the eggs hatching (Castro et al. 78596 (e-mail: [email protected]). 2004). Also, 56.6% of irradiated mites were still alive 2 USDAÐAPHISÐPPQÐCPHST, 1730 Varsity Dr., Suite 400, Raleigh, NC 27606. when the experiments were terminated. To demon- 3 920 Rahn Station Rd., Rincon, GA 31326. strate failure of reproduction after irradiation the ir- December 2010 HALLMAN ET AL.: PHYTOSANITARY IRRADIATION 1951

Table 1. Radiation phytosanitary treatments approved by APHIS (2008a, 2010a,b) and the IPPC (FAO 2009b,c, 2010)

Dose (Gy) Species or group Order: Family APHIS IPPC Anastrepha ludens (Loew) Diptera: Tephritidae 70 70 Anastrepha obliqua (Macquart) Diptera: Tephritidae 70 70 Anastrepha serpentina (Wiedemann) Diptera: Tephritidae 100 100 Anastrepha suspensa (Loew) Diptera: Tephritidae 70 Aspidiotus destructor Signoreta Hemiptera: Diaspididae 150 Bactrocera jarvisi (Tryon) Diptera: Tephritidae 100 100 Bactrocera tryoni (Froggatt) Diptera: Tephritidae 100 100 Brevipalpus chilensis Baker Acari: Tenuipalpidae 300 Ceratitis capitata (Wiedemann)a Diptera: Tephritidae 100 Conotrachelus nenuphar (Herbst) Coleoptera: Curculionidae 92 92 Copitarsia decolora (Guene´e)a Lepidoptera: Noctuidae 100 Cryptophlebia ombrodelta (Lower) Lepidoptera: Tortricidae 250 Cryptophlebia illepida (Butler) Lepidoptera: Tortricidae 250 Cylas formicarius (F.) Coleoptera: Brentidae 150 Cydia pomonella (L.) Lepidoptera: Tortricidae 200 200 Euscepes postfasciatus (Fairmaire) Coleoptera: Curculionidae 150 Grapholita molesta (Busck) Lepidoptera: Tortricidae 200 232b Omphisa anastomosalis (Guene´e) Lepidoptera: Pyralidae 150 Pseudaulacaspis pentagona (Targioni-Tozzetti)a Hemiptera: Diaspididae 150 Rhagoletis pomonella (Walsh) Diptera: Tephritidae 60 60 Sternochetus mangiferae (F.) Coleoptera: Curculionidae 300 Tephritidae Diptera: Tephritidae 150 150 Insecta except pupa and adult of Lepidoptera Class Insecta 400

a These pests were not considered for inclusion in the IPPC ISPM #28 in 2006 because they were not approved by APHIS until later. b There are two treatments for G. molesta, in ambient and hypoxic atmospheres; although the dose is the same, the measures of efÞcacy are different. radiated organisms should be kept alive under favor- high as 232 Gy. This objection is a reasonable because able conditions for reproduction until they eventually the maximal dose recorded during research support- die. The APHIS-approved treatment for B. chilensis ing a treatment should become the minimal dose re- has not been used commercially. quired for commercial application. After considering a dose of 100 Gy for S. mangiferae, Two treatments were proposed for G. molesta: one APHIS set the dose at 300 Gy based on low conÞdence treatment for commodities stored in ambient atmo- in research supporting 100 Gy (APHIS 2002). The spheres and one treatment for low oxygen storage. dose of 300 Gy may be excessive and has not been used The effect of hypoxia on the efÞcacy of PI is discussed commercially. below. The measure of efÞcacy for PI in ambient The IPPC Technical Panel on Phytosanitary atmosphere is prevention of emergence of the adult Treatments (TPPT) rejected the proposed treat- when stages no more advanced than larvae are irra- ments for Anastrepha suspensa (Loew), Cryptophle- diated. At the same dose in a low oxygen atmosphere, bia ombrodelta (Lower), and C. illepida (Butler), the 5.3% of irradiated Þfth-instar G. molesta emerged as former species because the supporting research did normal-looking adults, although the females did not not seem to use the most resistant stage (third instar) lay eggs and died within 8 d (Hallman 2004a). How- present in shipped fruit (Gould and von Windeguth ever, the fact that some adults emerged concerned 1991) and the latter two species because the research some member countries because 1) no further meta- was done exclusively in diet without comparing efÞ- morphosis is needed for the insects to reach the re- cacy on a plant host (Follett and Lower 2000). productive stage; and 2) live, although nonreproduc- Fifteen treatments were proposed for adoption by ing, individuals might be found in survey traps the TPPT, and eight survived the initial vetting process triggering restrictive and costly regulatory responses. during member consultation where individual mem- In March 2010, the CPM met and adopted both G. ber countries (173 as of August 2010) and their plant molesta treatments at 232 Gy (FAO 2010). The CPM protection organizations review and comment on the concluded that although the treatment done in hy- proposed standard. When there are no objections or poxic atmospheres may result in the presence of live unresolved issues, the standard is submitted to the but irradiated adults, only a very small percentage of IPPC Commission on Phytosanitary Measures for adults are likely to emerge after irradiation and that adoption. These eight treatments were adopted in these adults are very unlikely to survive for Ͼ1 wk. 2009 (FAO 2009b,c). Three more were adopted after Both factors greatly reduce the likelihood of adults reexamination in March 2010 (FAO 2010). being found in monitoring traps in importing coun- A member country objected to setting the dose for tries. Grapholita molesta (Busck) at 200 Gy because Hall- A dose of 150 Gy was proposed for Omphisa anas- man (2004a) recorded maximum absorbed doses in tomosalis (Guene´e) based on research that allowed the large-scale tests conÞrming the treatment to be as for adult emergence from irradiated late pupae but not 1952 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 6

production of F1 adults (Follett 2006a). It is generally and which need further research in light of the fact not possible to prevent adult emergence from late that irradiation does not have an independent method pupae of any insect at a dose tolerated by fresh com- of verifying efÞcacy. The impact of these factors on PI modities, so the most likely measure of efÞcacy will be research and application to generic treatments is dis- prevention of reproduction. Member countries were cussed. concerned about adult O. anastomosalis being found in survey traps. In addition, the nonirradiated control did not reproduce as well as expected indicating that un- Phytosanitary Irradiation Variables known factor(s) in addition to irradiation were re- pressing reproduction. Several variables have been noted from the litera- A dose of 92 Gy was proposed for Conotrachelus ture to possibly affect PI efÞcacy (Hallman 2000, nenuphar (Herbst) based on research that allowed for 2001). The more compelling of these are examined in

F1 mid-instars to develop when adults were irradiated greater detail below. (Hallman 2003). In this case, adults were considered Effect of Low Oxygen on Efﬁcacy. Hypoxia during the most radiotolerant stage that could be present on irradiation was observed to reduce phytosanitary ef- transported fruit hosts and objection to the presence Þcacy for tephritids in vitro by Balock et al. (1963) and of live adults postirradiation was made. In March 2010, substantiated in a number of instances since then the CPM adopted the treatment concluding that, al- (Hallman and Hellmich 2010). Hallman (2004b) though the treatment may result in the presence of showed that the reduction is much less for tephritids live but irradiated adults, they are rarely (if ever) in fruit compared with in vitro probably because in present in shipped fruit and irradiated adults are very fruit the larvae are already in a low oxygen environ- unlikely to survive for Ͼ1 wk (FAO 2010). Both fac- ment. tors greatly reduce the likelihood of adults being International standards prohibit phytosanitary found in monitoring traps in importing countries. radiation to commodities from low oxygen storage Doses of 140 and 145 Gy, respectively, for Cylas except for product at risk of Rhagoletis pomonella formicarius (F.) and Euscepes postfasciatus (Fair- (Walsh), which was studied under hypoxic conditions maire) were based on exposure of adults to radiation (Hallman 2004b, FAO 2009b). However, APHIS with no F1 adults resulting (Follett 2006a). Objection (2010b) does not prohibit commercial irradiation of was made to the presence of live adults post irradiation product stored in low oxygen. and the uncertainty as to how far the F1 generation More research is needed to decide under what cir- would develop after irradiation. Prevention of the F1 cumstances low oxygen storage might be a detriment adult as the measure of efÞcacy of PI does not leave to phytosanitary radiation and how to regulate com- much of a margin of security. These two proposed modities stored as such. This is the most signiÞcant treatments have been forwarded to the IPPC Stan- recognized factor affecting efÞcacy of PI after dose dards Committee for further review. itself. Hypoxic conditions might occur under storage PI treatments have been applied generically with regimes that do not necessarily use low oxygen by regard to host and also pest to a very large extent. design, such as packaging restrictive of gas ßow. Low Irradiation treatments in the IPPC phytosanitary oxygen itself is a phytosanitary treatment but usually treatment standard (FAO 2009b) apply to all fruits and at levels that are lower than those in storage (Neven vegetables. APHIS (2010b) has approved irradiation et al. 2009). as a phytosanitary treatment for all admissible fresh Most Radiation Tolerant Stage. A phytosanitary fruits and vegetables from all countries. The IPPC has treatment should be demonstrated effective against approved a generic dose of 150 Gy for all Tephritidae the most tolerant stage present on the regulated article (FAO 2009c), whereas APHIS (2010b) has approved and it follows that it will be effective against the other the same dose for tephritids as well as a 400-Gy dose stages that might be present. Although it is generally for Insecta except pupae and adults of Lepidoptera, accepted that radiotolerance in insects increases as which may require higher doses. The generic dose of they develop and is frequently cited as such, this fact 400 Gy did not survive the IPPC vetting process be- has not been robustly summarized for the measures of cause it was considered excessive extrapolation for the efÞcacy used in PI. data that had been accumulated so far. Also, the pres- Table 2 presents relative radiotolerances of stages of ence of live adults among most quarantine pests in that organisms for measures of efÞcacy used in PI. We group (all Insecta except pupae and adults of Lepi- include all published studies where three or more doptera) was objectionable to some countries. Lim- stages can be compared, with stage being deÞned iting phytosanitary irradiation treatments to cases liberally as any speciÞc period of development. The where live adults will not be present after treatment studies support the hypothesis that radiotolerance in- would greatly restrict the applicability of this tech- creases as insects develop. There are several excep- nology to instances where tephritids and some Lepi- tions; some may be dismissed but some cannot, given doptera were the only quarantine pests that could be the information in the respective publication. Other present on transported commodities. studies not included in Table 2 report relative differ- The objective of this review is to examine several ences among only two stages or report differences in factors related to PI, determine which have sufÞcient a way not easily summarized (e.g., Hallman 2003). information to determine whether they affect efÞcacy Still, none of these other studies contradict the hy- eebr21 H 2010 December Table 2. Radiotolerances of different stages (where three or more stages can be compared) of arthropods to measures of efﬁcacy that are used as objectives for phytosanitary irradiation treatments

Measure of efÞcacy; Stages tested in order of development with least developed Order: Family Organism Reference prevention of Þrst (min. dose ͓Gy͔ to achieve near 100% efÞcacy)a Acari: Acarididae Acarus siro (L.) Adult Egg (Ͼ450); larva (450); Hypopus (1,000) Burkholder et al. (1966) Ͻ A. siro F1 adult Egg (250); larva (250); Hypopus (450); adult ( 450) Burkholder et al. (1966) Coleoptera: Anobiidae Lasioderma serricorne (F.) Adult Egg 1 d (10), 2 d (15), 3Ð4 d (Ͼ20); larva 5 d (25), 10 d (25), Harwalkar et al. (1995) 15d(Ͼ25) L. serricorne Adult Egg 1Ð2 d (50), 5Ð6 d (100); larva (100); pupa (Ͼ200) Imai et al. (2006) Coleoptera: Bostrichidae Rhyzopertha dominica (F.) Adult Egg 2Ð4 d (40); larva 14Ð16 d (80); pupa (ϾϾ200) Matin and Hooper (1974) R. dominica Reproduction Egg 2Ð4 d (30); larva 14Ð16 d (40); pupa (140); adult 4Ð7 d Matin and Hooper (1974) (115) Coleoptera: Bruchidae Callosobruchus maculatus (F.) Adult Egg 0Ð1 d (5), 2 d (10), 3 d (15); larva 1Ð10 d (20), 11 d Dongre et al. (1997) (100), 12 d (Ͼ150) C. maculatus Adult Egg (20); larva early (20), middle (30), late (60); pupa (140) Diop et al. (1997) Coleoptera: Curculionidae Anthonomus grandis Boheman Reproduction Instar 3 (19); pupa early (22), middle (Ͼ28), late (Ͼ28); Flint et al. (1966) adult (45) Sitophilus granarius (L.) Reproduction Egg (30), larva (30), pupa (70), Young adult (100), Old adult Aldryhim and Adam (1999) (70) Coleoptera: Tenebrionidae Palorus subdepressus (Wollaston) Adult Egg (50); larva (100); pupa (1000) Brower (1973a) AL ET ALLMAN Diptera: Tephritidae Anastrepha ludens (Lowe) Adult emergence Instar 3 feeding (16), postfeeding (16); Prepupa (14); pupa Hallman and Worley (1999) cryptocephalic (18), phanerocephalic 1 d (22), 2 d (25); adult pharate 1 d (35), 2 d (100), 3 d (250) Anastrepha obliqua (Macquart) Adult emergence Instar 3 (50); puparium 1 d (20), 10 d (300) Arthur et al. (1994) A. obliqua Adult emergence Instar 3 (14); Prepupa (14); pupa (14); adult pharate 1 d (20) Hallman and Worley (1999) b Ͼ Ͼ Ͼ Ͼ Bactrocera cucurbitae (Coquillett) Adult emergence Egg ( 33); larva1d( 46),2d( 45),3d( 50), 4 d Balock et al. (1963) P .: (Ͼ45),5d(Ͼ41); puparium1d(Ͼ32),2d(Ͼ42), 3 d (Ͼ61),4d(Ͼ270),5d(Ͼ450),6d(Ͼ665),7d(Ͼ830), HYTOSANITARY 8d(Ͼ1170),9d(Ͼ1215) Bactrocera dorsalis (Hendel)2 Puparia Egg1d(Ͼ120); larva1d(Ͼ280),2d(Ͼ470); instar 3 Balock et al. (1963) (Ͼ930) B. dorsalisb Adult emergence Egg (Ͼ26); larva1d(Ͼ27),2d(Ͼ25),3d(Ͼ32), 4 d Balock et al. (1963) (Ͼ34),5d(Ͼ35),6d(Ͼ33); puparium1d(Ͼ24), 2 d (Ͼ27),3d(Ͼ30),4d(Ͼ180),5d(Ͼ290),6d(Ͼ420), 7 d I (Ͼ570),8d(Ͼ680), 9d (Ͼ1100), 10 d (Ͼ1400) RRADIATION B. dorsalis Adult emergence Egg (25); instar 1 (25), 2 (25), 3 (Ͼ80) Vijaysegaran et al. (1992) Bactrocera tryoni (Froggatt) Adult emergence Egg (Ͻ50); larva young (50), old (75) Rigney and Wills 1983) B. tryoni Egg (Ͻ75); larva young (75), old (75) Jessup et al. (1992) Ceratitis capitata (Wiedemann) Adult emergence Egg 1Ð24 h (10), 48 h (20); larva 2Ð4 d (20), 8 d (40) Masour and Franz (1996) C. capitatab Adult emergence Egg1d(Ͼ14),2d(Ͼ22); larva1d(Ͼ18),2d(Ͼ20), 3 d Balock et al. (1963) (Ͼ22),4d(Ͼ23),5d(Ͼ25),6d(Ͼ25); puparium 1 d (Ͼ17),2d(Ͼ16),3d(Ͼ23),4d(Ͼ150),5d(Ͼ255), 6 d (Ͼ370),7d(Ͼ470),8d(Ͼ560), 9d (Ͼ840), 10 d (Ͼ980) C. capitata Pupariation Egg 2Ð4 h (10), 27Ð30 h (20), 45Ð49 h (240); larva 1 d (240), Sheta (1983) 3 d (360), 5 d (840), 7 d (1000) Hemiptera: Diaspididae Pseudaulacaspis pentagona Gravid F1 female Instar 2 (90); adult female (60), gravid female (120) Follett (2006c) (Targioni-Tozzetti) Hemiptera: Pentatomidae Nezara viridula (L.) Egg hatch Egg 0 d (5), 1 d (10), 2 d (10),3d(Ͼ10), 4 d (50), 5 d Mau et al. (1967) (Ͼ50) Hemiptera: Pseudococcidae Planococcus minor (Maskell) F1 egg hatch Egg (150); Nymph (150); adult (150) Ravuiwasa et al. (2009) Lepidoptera: Gelechiidae Phthorimaea operculella Zeller Adult Larva 1Ð1.5 d (100), 6Ð6.5 d (100), 12Ð12.5 d (125) Saour and Makee (2004) P. operculella Adult Instar 4 (120); pupa 1Ð3 d (400), 6Ð8 d (700) Al-Taweel et al. (2007) 1953 Sitotroga cerealella (Olivier) Adult Egg (175); larva (175); pupa (Ͼ1000) Cogburn et al. (1966) Table 2. Continued J 1954

Lepidoptera: Noctuidae Heliothis virescens (F.) Adult Larva1d(Ͻ100), 6 d (100),9d(Ͼ100), 15 d (Ͼ100) El Sayed and Graves (1969) Spodoptera litura (Fabr.) Pupation Egg3d(Ͻ200), 4 d (200); instar 3 (200), 5 (400) Dohino et al. (1996a) Lepidoptera: Pyralidae Anagasta kuehniella (Zeller) Adult Egg (200); larva 7 d (200); instar 5 (250) Ayvaz and Tunçbilek (2006) Ͼ A. kuehniella F1 egg production Egg (200); larva 7 d (200); instar 5 (150); pupa5d( 350); Ayvaz and Tunçbilek (2006) adult (Ͼ550) A. kuehniella F1 egg hatch Egg (150); instar 5 (250); pupa 5 d (300); adult (300) Ayvaz and Tunçbilek (2006) Cadra cautella (Walker) Adult Egg 3 d (300), instar 5 (200), pupa 3Ð4 d (1000) Cogburn et al. (1973) Corcyra cephalonica (Stainton) Adult Egg 0 d (10), 1 d (25), 2 d (75), 3 d (250), 4 d (250), instar 1 Huque (1971) (100), 5 (200) Plodia interpunctella (Hbner) Adult Egg (175); larva (132); pupa (Ͼ1000) Cogburn et al. (1966) Lepidoptera: Tortricidae Amorbia emigratella Busck Adult Instar 1 (90), 2Ð3 (120), 4Ð5 (Ͼ150); pupa (ϾϾ150) Follett (2008) Cryptophlebia illepida (Butler) Adult Egg 3 d (125); instar 1 (Ͻ250), 2Ð3 (125), 4Ð5 (Ͼ250); pupa Follett and Lower (2000) (Ͼ250)

C. illepida Reproductive Egg 3 d (62.5); instar 1 (125), 2Ð3 (62.5), 4Ð5 (125); pupa 1Ð5 Follett and Lower (2000) OF OURNAL females d (125), 7Ð8 d (Ͼ250) C. illepida Oviposition Instar 1 (125), 2Ð3 (62.5), 4Ð5 (125); pupa 1Ð5 d (125), 7Ð8 d Follett and Lower (2000) (Ͼ250) Ctenopseustis obliquana (Walker)c Pupation Egg 1 d (81), 5 d (159); instar 1 (193), 3 (192), 5 (215) Lester and Barrington (1997) C. obliquanac Adult Egg 1 d (42), 5 d (111); instar 1 (150), 3 (126), 5 (117) Lester and Barrington (1997) c E

C. obliquana Oviposition Egg 5 d (36); instar 1 (55), 3 (65), 5 (70) Lester and Barrington (1997) CONOMIC Ͼ Ͼ Ͼ Cydia pomonella (L.) F1 egg hatch Instar 1 (93); pupa early ( 70), mid ( 233), late ( 400); Proverbs and Newton (1962) adult (400) Thysanoptera: Thripidae Retithrips syriacus (Mayet) F1 adult Egg (100); larvae (100); pupae (150); adult (150) Bhuiya et al. (1999) R. syriacus Adult Egg (25); larvae (50); pre- and pupae (500) Majumder (2001) d E

R. syriacus Fertility Egg (25); larvae (25); pre- and pupae (50); adult (50) Majumder (2001) NTOMOLOGY R. syriacus Oviposition Larvae (25); pre- and pupae (50); adult (Ͼ500) Majumder (2001) Thrips palmi Karny Reproduction Egg (100); instar 2 (100); adult (Ͼ200) Dohino et al. (1996b) Thrips tabaci Lindeman Reproduction Egg (100); instar 2 (100); adult (Ͻ400) Dohino et al. (1996b)

a Doses are for relative comparisons within rows because they are nominal (dosimetry sometimes not reported) and other differences among studies caution against direct comparisons. b Estimates of 95 percentile (hence, “greater than” added to achieve 100%); actual data not given. c Estimates of 99 percentile; actual data not given. d Reported as “sterility” without identifying what was measured. o.13 o 6 no. 103, Vol. December 2010 HALLMAN ET AL.: PHYTOSANITARY IRRADIATION 1955 pothesis that insects increase in radiotolerance as they 2Ð3-d-old Plodia interpunctella (Hu¨ bner) eggs were develop for measures of efÞcacy used in PI. more tolerant than last instars (Cogburn et al. 1966). Several apparent exemptions to the rule that ra- Of these exceptions in Table 2 to the axiom that diotolerance increases as insects develop are dis- radiotolerance in insects increases as they develop, cussed below. In a daily analysis of radiotolerance of three that are not easily dismissed are C. illepida, P. two tephritids Balock et al. (1963) found that radiotol- pentagona, and P. interpunctella. However, in the Þrst erance did not increase steadily with increasing de- two cases the most developed stages that could be velopment, but increased in a somewhat zigzag man- present on transported commodity, Þfth instar and ner. Results are estimates for the 95th percentile and gravid female, respectively, are more tolerant than any not the actual data. Taken as distinct developmental of the other stages present, resulting in no increased stages, though, the ßies increase in radiotolerance as risk to quarantine security if they were truly excep- they develop. tions (Follett and Lower 2000, Follett 2006c). P. in- A reason Arthur et al. (1994) found the Anastrepha terpunctella is not a quarantine pest; however, as an obliqua (Macquart) prepupa to be more susceptible example of a pyralid, the measure of efÞcacy may be than the third instar (Table 2) may be that because prevention of reproduction by late pupae (pyralids they were irradiated in sealed tubes the more active often pupate in shipped commodity), which required larvae depleted the oxygen in the tube to a greater a higher dose for pupae than eggs or larvae (Cogburn extent than the prepupae, increasing radiotolerance of et al. 1966). the former. Hallman and Worley (1999) found no Some research demonstrates that, although ra- difference in radiotolerance in vitro between third diotolerance may increase as an insect develops, old instar and prepupal A. obliqua. adults may be more susceptible than young adults Lester and Barrington (1997) found that larval (e.g., Aldryhim and Adam 1999), indicating that ac- Ctenopseustis obliquana (Walker) (Tortricidae) de- tively reproducing adults should be used in phytosani- creased in radiotolerance as they developed when tary research and not adults past their prime repro- measured as prevention of adult emergence but not ductive age. when measured as prevention of pupation or ovipo- Cryptically-feeding Curculionidae that occur as im- sition (Table 2). These observations are 99th percen- matures inside the host plant represent a potentially special case regarding most radiotolerant stage. Im- tile estimates and not the actual data, and there is some matures may be in hypoxic atmospheres, possibly in- overlap in 95% conÞdence intervals. Follett and Lower creasing their radiotolerance in the same manner as (2000) found that mid-instar Cryptophlebia illepida occurs with tephritids (Hallman and Loaharanu 2002). (Butler) were more susceptible than Þrst instars re- It could be reasonable to hypothesize that adults gardless of the measure of efÞcacy (Table 2). treated in vitro could be more susceptible. However, Nymphal Pseudaulacaspis pentagona (Targioni-Toz- Hallman (2003) found that third-instar Conotrachelus zetti) were more radiotolerant than adults for pre- nenuphar (Herbst) cryptically infesting immature ap- vention of gravid F1 (Follett 2006c). Sixty gray applied ples (Malus spp.) were more susceptible than adults to second-stage nymphs (n ϭ 172) and pregravid ϭ outside of apples. adults (n 358) resulted in 237 and 0 gravid F1, Effect of Host on Efficacy. Another characteristic respectively. that has been largely accepted in radiation treatments We found four exceptions with stored product but that has not been adequately analyzed is that host pests. A higher dose was required to prevent repro- does not affect efÞcacy. International standards state duction in pupal Rhyzopertha dominica (F.) than adult that radiation treatments are valid for all fruits and (Matin and Hooper 1974). However, adults were ir- vegetables that are hosts for the given pests (FAO radiated with a different source (an X-ray therapy 2009b, 2010). APHIS (2005) states that “SpeciÞc char- unit) than immatures (gamma from cobalt 60); it is not acteristics of the fruits and vegetables being treated . . . clear that the same doses were being absorbed by are irrelevant to the effectiveness of irradiation as long adults versus immatures. A higher dose was required as the required minimum dose is absorbed.” to prevent egg stage Cadra cautella (Walker) from Gould and von Windeguth (1991) concluded that reaching the adult stage than Þfth instars (Cogburn et three different hosts of Anastrepha suspensa (Loew) al. 1973). However, this is probably an anomaly as only required different doses (50Ð150 Gy) to achieve the one egg reached the adult stage at 200 Gy, whereas at same level of quarantine security. Hallman and Loa- the next lowest dose (100 Gy), 0.8 and 10.9% eggs and haranu (2002) successfully argued that variations in larvae, respectively, reached the adult stage, showing the research allegedly supporting different doses the Þfth instar to be more tolerant than the egg stage. among these hosts do not in fact support different The Þfth (Þnal) instar Anagasta kuehniella (Zeller) doses and that 70 Gy is sufÞcient (Table 1). was more susceptible than a younger (7-d-old) larva Apparent differences in dose among various studies when measured as F1 egg production at a series of of Ceratitis capitata (Wiedemann) that could be hy- doses from 50 to 150 Gy (Ayvaz and Tunçbilek 2006). pothesized at least in part as due to host are not Fate of the eggs laid by irradiated 7-d-old larvae is not consistent (Torres-Rivera and Hallman 2007). For ex- reported. When measured as adult emergence, the ample, doses for orange range from 40 to Ͼ200 Gy and Þfth instar was more tolerant than 7-d-old larvae. doses for papaya range from 100 to 225 Gy. The wide When measured as development to the adult stage, variation in doses for C. capitata can more logically be 1956 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 6 explained by irregularities in some of the research, and a dose of 100 Gy should sufÞce (APHIS 2010a). A few studies directly compare hosts for measures of efÞcacy used in PI (acute mortality is not considered). When corrected for control emergence, adult emergence from Bactrocera tryoni (Froggatt) larvae irradiated with 40 Gy in meridic diet, orange, Citrus sinensis L., and apple, Malus domestica Borkh., was 0, 0.34, and 0.15%, respectively (Macfarlane 1966). Bac- trocera tryoni third instars infesting oranges and avo- cados, Persea americana Mill, responded to radiation dose equally (Rigney and Wills 1983). Jessup et al. (1992) report on disinfestation of six fruits of B. tryoni Fig. 1. Eclosion of T. urticae eggs irradiated when4dold third instars and found that 50 Gy prevented 98.6Ð (after Dohino et al. 1994). Dose rate for electron beam was 100% adult emergence except for mangoes, Mangifera several hundred times that for gamma ray. indica L. (87.1% adult emergence at 50 Gy). However, although these hosts were reported in the same article, it was a compilation of several years of research that Host does not seem to affect efÞcacy for the mea- may not have been done under the same circum- sures of efÞcacy used for PI treatments (prevention of stances. Regardless, all were disinfested at 75 Gy, al- development or reproduction). However, direct com- though sample size for mangoes was small (504 larvae parisons among hosts are few and comparisons of versus 2,891Ð220,328 for the others), yielding a low different studies sometimes yield quite variable results level of conÞdence that 75 Gy would provide com- which may or may not have anything to do with host. plete control in that fruit. Heather et al. (1991) dem- Also, there is considerable difference in efÞcacy of onstrated a high level of quarantine security against B. irradiation of tephritids in diet versus fruit, and the tryoni in mangoes with a dose of 74Ð101 Gy. The target reason for that difference should be examined as it dose was 75 Gy, but dosimetry showed some doses to may relate to host. Effect of Dose Rate on Efficacy. The possible effect be as high as 101 Gy. It is possible that dose reports of of dose rate on efÞcacy and commodity quality has not 75 Gy in Jessup et al. (1992) were targets and that both been considered when approving PI treatments. Hall- studies used the same irradiation facility, thus dem- man (2000) reviewed some articles on this subject onstrating that B. tryoni in mangoes are controlled which indicated that dose rate may be directly related with a dose not far from other fruits studied by Jessup to damage to pests and commodities. Results from et al. (1992). other articles follow. Bletchly (1961) reported no dif- There was no signiÞcant difference in completion of ference between two dose rates (0.5 and 11.5 Gy/min) development for irradiated eggs and larvae of Tribo- at doses (60Ð80 Gy) that prevented adult emergence lium confusum Jacquelin du Val reared on wheat from irradiated Anobium punctatum (De Geer) mid- (Triticum sp.); barley, Hordeum vulgare L.; and corn, dle-aged larvae. Gonen and Calderon (1973) found Zea mays L., ßour (Tunçbilek and Kansu 1966). Man- that dose rate was directly related to male reproduc- sour and Franz (1996) found no difference between C. tive sterility of E. cautella when the doseÐrate ratio was capitata larvae reared and irradiated in orange (Citrus as little as 3:1; egg hatch was 15 and 1% for the lower sp.) and peach, Prunus persica (L.) Batsch. and higher dose rates, respectively. Apparent differences between studies can often be Dohino et al. (1994) compared electron beam to explained by deÞciencies in research, although it may gamma ray (cobalt 60) for effect on eclosion of Tet- not be possible to prove. Tephritid larvae treated in ranychus urticae Koch eggs and found no signiÞcant open diet are controlled with lower doses than in fruit difference (Fig. 1). This example is an extreme exam- (Macfarlane 1966, Hallman and Loaharanu 2002). ple of dose rate differences because the entire radia- These differences may be due in part to differences in tion dose via electron beam is applied to a given spider atmospheric content in vitro versus in fruit. Some mite egg in a fraction of a second, whereas it takes tephritid research has been conducted by rearing several minutes to apply the same dose via cobalt 60. third instars in diet and inserting them in fruit Ϸ1d Given that a spider mite egg is Ϸ0.14 mm in diameter, before irradiation without comparing the results of and the speed of the electron beam conveyor is 3.0 this technique to more natural infestation (Mansour m/min, any given egg was irradiated in Ϸ0.17 s via and Franz 1996, Follett and Armstrong 2004). Such a electron beam, whereas cobalt required 15 min to comparison should be made before an unnatural in- deliver 1 kGy to any given egg. Therefore, at the festation technique is used to develop a phytosanitary largest dose (1 kGy), which resulted in Ϸ30% eclosion, treatment (Hallman and Thomas 2010). the dose rate for electron beam was 15.0 min (60 Differences in efÞcacy for diet versus a plant host s/min)/0.17 ϭϷ5,300 times the dose rate for cobalt were not found for the lepidopterans G. molesta or 60. However, the beam is not as narrow as the diameter Ostrinia nubilalis (Hu¨ bner) and insects reared on diet of a spider mite egg, so the dose via electron beam was were then used to develop treatments (Hallman probably delivered only several hundred times faster 2004a, Hallman and Hellmich 2009). than the dose via cobalt 60. December 2010 HALLMAN ET AL.: PHYTOSANITARY IRRADIATION 1957

Development of Callosobruchus maculatus (F.) ulation when irradiated as adults (Bartlett and Bell adults from irradiated larvae and pupae was com- 1962). At 50 Gy 2.3 and 10.4%, respectively, of eggs of pletely prevented with 25 Gy applied at a rate of 23.6 the large and normal-size populations hatched. Gy/min, whereas 100 Gy was required at 0.9 Gy/min Although Cornwell (1966) noted marked differ- (Fontes et al. 2003). ences in mortality among 35 irradiated strains of Sito- Hatch of eggs laid by irradiated (50 Gy) Tribolium philus granarius (L.), only insigniÞcant differences castaneum (Herbst) adults was 1.1 and 0% at 0.5 and were found for fertility. 23.3 Gy/min, respectively (Nair and Subramanyam Reproduction of two malathion-resistant and one 1963). susceptible strain of P. interpunctella was reduced sim- Until recently, most phytosanitary radiation re- ilarly (Ϸ44%) when irradiated with 50 Gy (Brower search was conducted using isotopic sources (cobalt 1973b). Likewise a strain of T. castaneum resistant to 60 and cesium 137) with slow to modest dose rates that DDT and malathion and a susceptible strain were both are usually exceeded by commercial application. In reduced to Ϸ31% of reproduction when irradiated that case, efÞcacy of a commercial application may with 20 Gy (Brower 1974). Phosphine-resistant T. cas- exceed the efÞcacy level used in the research. How- taneum was signiÞcantly more tolerant than a suscep- ever, in recent years research has been performed tible strain when measured as adult emergence from with machine sources with very high dose rates. If this irradiated larvae (Nakakita et al. 1985); there was no research is applied using slower commercial isotopic difference between the two strains regarding repro- sources, there is reason to hypothesize that the level duction of irradiated adults. of efÞcacy might be inferior in the isotopic commer- Chung et al. (1971) reported a difference in repro- cial application. Therefore, the effect of dose rate on duction between Þeld and laboratory-sourced chafers efÞcacy should be tested. Rhizotrogus majalis (Razoumowsky), although both Effect of Temperature on Efficacy. Cold may re- sources were collected close together in time in the duce the efÞcacy of sanitary applications of radiation same place and were most likely the same genotype, (Dickson 2001); however, that generally occurs when indicating other reasons than genetics for the differ- the product is frozen, which is never the case for ence. They suggest that the irradiated adults of both phytosanitary applications. Few and inconclusive sources were of different ages when irradiated, which studies addressed the effect of temperature on efÞ- could account for the difference. cacy of phytosanitary radiation when it was reviewed Hallman (2003) found that reproduction of dia- by Hallman (2000). Research done since then found pausing northern strain of Conotrachelus nenuphar that temperature did not affect efÞcacy for a tephritid (Herbst) was prevented with half the dose required and a crambid within the range used for cold storage for the nondiapausing southern strain. However, the of fresh commodities and ambient temperatures two strains are somewhat reproductively incompati- (Hallman 2004b, Hallman and Hellmich 2009). A few ble and possibly should be treated as different species. more studies are warranted before a deÞnite conclu- Also, insects in diapause may be more susceptible to sion should be made. radiation than ones not in diapause (Hallman 2000). Variability for Radiosusceptibility Among Popula- Twenty-Þve gray applied to cage (laboratory) and tions. In general, phytosanitary treatments have been Þeld-infested peaches, P. persica, resulted in 5.0 and considered efÞcacious against all populations of an 4.4%, respectively, C. capitata adult emergence in two approved species, and irradiation is no exception. separate studies done during the same time period However, because radiation treatments have no inde- with the same methodology (Arthur et al. 1993a,b). pendent veriÞcation of efÞcacy it would be more cru- Adult emergence for the cage-infested ßies should cial to know whether differences among populations probably be slightly lower as the percentage emerged exist for irradiation. Taken at face value, the literature is based on the number of puparia forming and not seems to indicate differences in radiotolerance among larvae irradiated, which is not given; this pair of studies populations of the same insects. Torres-Rivera and shows no difference between wild and laboratory C. Hallman (2007) examine studies that suggest control capitata. Follett and Armstrong (2004) found labora- doses for different populations of C. capitata infesting tory and wild strains of three species of tephritids the same fruit range from 40 to 200 Gy. However, (including C. capitata) to respond the same when because these studies were done by different re- measured as adult emergence from irradiated third searchers, factors other than genotype may be respon- instars. sible for apparent differences. The aggregate of studies where direct comparisons Several studies directly compared known popula- are made between genotypes of the same species does tions of the same species for radiotolerance. Because not support signiÞcant differences in response to ra- acute mortality is not a measure of efÞcacy for phyt- diation. A few more studies may be warranted because osanitary radiation, we ignore studies comparing mor- those done do not represent a broad range of taxa tality and instead report studies comparing metamor- (mainly tephritids and stored product pests from Co- phosis or reproduction, measures of efÞcacy for leoptera and Lepidoptera). phytosanitary radiation. Although increased tolerance to radiation has been Eggs laid by a population of T. castaneum selected bred in the laboratory (e.g., EnÞeld et al. 1983), this for increased pupal weight (2.5ϫ normal) were sig- increase would not likely happen for phytosanitary niÞcantly more radiosusceptible than the source pop- applications in nature because the dose used should 1958 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 6 leave essentially no survivors to reproduce and, even not tolerate the maximum dose that will be absorbed if it did, they would usually be exported and thus by the commodity when a minimum dose of 500 Gy is removed from the population. Also, the degree of sought, which could be at least twice that dose induced increase in radioresistance achieved has been (Heather and Hallman 2008). Therefore, viable ge- small compared with resistance to pesticides. neric doses for groups of quarantine pests that would Our conclusion is that variations among populations be Ͻ500 Gy should be sought. for resistance to radiation, if they exist, are probably A reduction in dose also can lead to savings in not signiÞcant. However, it may always be prudent to application time and costs. For example, Follett (2009) use wild material when researching phytosanitary reports that a reduction in treatment dose for Hawai- treatments, including irradiation. Populations that ian sweet potato, Ipomoea batatas (L.) Lam., from 400 show distinct biological differences, such as northern to 150 Gy resulted in a 60% reduction in cost of treat- and southern strains of C. nenuphar (Hallman 2003), ment. possibly should be treated as distinct species for phyt- Weevils. Cryptic feeders cannot be easily found and osanitary research purposes. culled upon inspection without damaging the fruit. Therefore they will usually require a treatment if there is more than a negligible risk of their presence. Cur- Generic Treatments culionidae and Brentidae form such a group of cryptic The generic phytosanitary treatment concept is that quarantine pests. Fresh commodity-infesting weevils one speciÞc treatment is used for a group of quaran- usually have narrow host ranges, thus most commod- tine pests and or commodities, although not all were ities are not hosts in most of their growing ranges, so tested for efÞcacy. Although it has been applied to they are not as omnipresent as Tephritidae in their various treatments, such as cold storage and fumiga- hosts. A generic treatment for these weevils could be tion, it is applied to a much broader degree with as low as 150 Gy (Heather and Hallman 2008). irradiation (Heather and Hallman 2008). A generic Three weevils discussed above (C. nenuphar, C. treatment should contain a margin of error to cover formicaries, and E. postfasciatus) have been studied to untested pests that might require higher doses than the degree required for phytosanitary treatments, but those for pests in the group that were tested. The only one weevil survived IPPC vetting so far. Before generic dose of 150 Gy for all Tephritidae was ac- a generic treatment for these weevils can be seriously cepted by APHIS in 2006 and the IPPC in 2009. Also, considered more species must be studied with large in 2006, APHIS accepted a generic dose of 400 Gy for numbers (tens of thousands) of individuals. Good can- all Insecta minus pupae and adults of Lepidoptera. didate species for research are those infesting fruits for Generic treatments should be developed for groups which irradiation at 400 Gy is presently applied: Cono- of pests for which it is feasible that they will be com- trachelus psidii Marshall and Conotrachelus dimidiatus mercially used. The generic dose of 150 Gy for Te- Champion in guava from Mexico, and Sternochetus phritidae is used for mangoes and citrus fruit exported frigidus (F.), Sternochetus mangiferae (F.), and Ster- from Mexico to the United States. In several other nochetus olivieri (Faust) in mango from India and cases (guavas from Mexico to the United States, man- Thailand. goes from India to the United States, dragon fruit, Lepidoptera Larvae. A generic treatment for Lep- Hylocereus undatus (Haworth) Britton & Rose, from idoptera that infest regulated articles only in the egg Vietnam to the United States, and several fruit from or larval stages would be useful. Although the larvae Thailand to the United States) the APHIS-approved leave feeding holes visible on the outside of a com- generic treatment of 400 Gy is used because insects modity in which they bore, they may not be effectively besides fruit ßies may be present. Australia sends man- eliminated by culling; thus, postharvest phytosanitary goes and litchi to New Zealand using a generic treat- treatments are often required. This group would in- ment of 250 Gy for Insecta (MAF 2009). clude the families Crambidae, Gracillariidae, Lycae- Virtually any small organism feeding on the part of nidae, Noctuidae, Pyralidae, and Tortricidae. The a commodity that is exported can be a quarantine pest measure of efÞcacy could be the same as for Tephriti- to any part of the world that does not have that or- dae: prevention of emergence of normal-looking ganism and where it could become established. Ad- adults from irradiated eggs and larvae. The Þnal instar ditional organisms may be found on commodities as is the most radiotolerant stage. Candidate species for Ôcontaminating pestsÕ that may be carried by a com- research are the following quarantine pests on commodity but do not feed on it (FAO 2009a). Two commodities already using PI at a dose of 400 Gy: Deanolis mon examples intercepted in the United States are the sublimbalis Snellen (Pyralidae) in mango from India; khapra beetle, Trogoderma granarium Everts, with Gymnandrosoma aurantianum Lima (Tortricidae) in brass items from Asia and terrestrial Gastropoda with guava from Mexico; Conopomorpha sinensis (Bradley) ceramic tiles from the European Union. (Gracillariidae), Cryptophlebia ombrodelta (Lower) Although a single generic dose for all invertebrate (Tortricidae) and Deudorix epijarbas (Moore) (Ly- quarantine pests would be useful, it would necessarily caenidae) in longan (Dimocarpus longan Lour.) and be set at the minimum absorbed dose required for the lychee (Litchi chinensis Sonn.) from Thailand; and most tolerant organism within that group, which could Conopomorpha cramerella (Snellen) (Gracillariidae) require at least 500 Gy (Hallman and Phillips 2008). in rambutan (Nephelium lappaceum L.) from Thai- Although many commodities tolerate 500 Gy they may land. A reasonable target for a generic dose for Lep- December 2010 HALLMAN ET AL.: PHYTOSANITARY IRRADIATION 1959 idoptera eggs and larvae is 250 Gy (Heather and Hall- Dosimetry. Although the IPPC accepted treatments man 2008). for which dosimetry was not reported, it was noted Those Lepidoptera that pupate in the transported that not only should dosimetry be done but the results commodity will not be included in this generic dose should be reported. Dosimeters should be placed in and may require higher doses. For example, Ͼ300 Gy areas of the load where extreme values are shown to was required to prevent F1 egg hatch from irradiated occur via prior dose mapping (Heather and Hallman Ostrinia nubilalis (Hu¨ bner) late pupae (Hallman and 2008). The highest doses absorbed during the large- Hellmich 2009). However, a lower dose could be used scale testing conÞrming dose efÞcacy become the if efÞcacy were measured later than F1 egg hatch. In minimum absorbed doses required for commercial the above-mentioned example prevention of F1 pu- use. pation was accomplished with Ͻ250 Gy. Live Adults Postirradiation. Rejection of the pres- Sternorrhyncha or Coccoidea. Hemipterans of ence of live adults threatens broad application of PI the families Aleyrodidae, Coccidae, Diaspididae, and because most quarantine pests will be present as adults Pseudococcidae are external feeders that may not be and they will not be killed rapidly by irradiation. This readily removed from commodities during the pack- problem was faced years ago by APHIS (1996) when ing process and may require postharvest phytosanitary they stated that it was desirable that live irradiated treatments. A generic treatment comprising at least quarantine pests could not emerge from the commod- these four families might be Ϸ250 Gy, although ity unless they could be demonstrated to have been Heather and Hallman (2008) suggest a dose for some irradiated and that live pests for which treatments non-Coccoidea in the Sternorrhyncha (Aleyrodidae were approved will presume to have been effectively and Aphididae) might be as low as 100 Gy. Many treated unless “evidence exists that the integrity of the aleyrodids, coccids, diaspidids, and pseudococcids are treatment was inadequate.” ISPM #18 also states that quarantine pests of commodities currently treated by it is preferable that live pests not emerge from the the APHIS generic dose of 400 Gy and would be prime commodity unless proof of irradiation was available candidates for research aimed at lowering the doses (FAO 2003). APHIS has not objected to live adults via applied to host commodities (APHIS 2006, 2007, a comprehensive process of validation and certiÞ- 2008b,c; BA 2008). The presence of live adults postir- cation of treatment facilities with monitoring of radiation must be broadly accepted for a generic treat- dosimetry and dose application during preclearance ment for this group to be viable. programs and safeguarding of regulated articles Acari. Plant-infesting Acari of the families Eriophyi- posttreatment. dae, Tarsonemidae, Tenuipalpidae, and Tetranychi- Although the presence of live parent generation dae are quarantine pests for which postharvest phyt- adults cannot reasonably be prohibited, postirradia- osanitary treatments are frequently required. The tion restrictions on development of the F1 generation dose for these pests could be at least 350 Gy (Heather should help instill conÞdence that the risk of an in- and Hallman 2008); therefore, a generic treatment festation by progeny of irradiated adults is negligible. including Acari would probably sufÞce for all Insecta A treatment for Aspidiotus destructor Signoret allows as well except for certain adults of Lepidoptera (Hall- for up to F1 adult development after irradiation (Fol- man and Phillips 2008). Adult Lepidoptera may rarely lett 2006b) and represents an extreme measure of be of quarantine importance in the normal pathways efÞcacy for an accepted treatment. Objectives of for agricultural commodities. treatments should ideally prevent signiÞcant F1 development. Eggs may be laid, hatch, and early instars appear, but they should be documented to stop de- veloping well before the F adult could be present. Phytosanitary Research 1 The use of speciÞc measures of efÞcacy that do not The experience with the IPPC vetting of PI treat- leave signiÞcant unknown periods in the developmen- ments provides some lessons for research. Even if tal process can help ensure that any progeny die well techniques for identifying irradiated organisms were before reaching the F1 adult. Almost all tephritid PI available, they would not, of course, identify instances research has been done without observing develop- where the research supporting the treatment was in- ment during the lengthy puparial stage where the adequate or other factors had changed, thus reducing insect develops from a larva to a pharate adult. Ex- efÞcacy of the treatment. Therefore, PI research bears ceptions are some research with diapausing tephritids a greater burden of providing quarantine security than and A. ludens that found that most development ceases does research with all other commercial phytosanitary before the irradiated third instar reaches the phan- treatments that have an independent method of ver- erocephalic pupal stage, leaving a considerable margin ifying efÞcacy. Furthermore, PI research requires of security between that stage and the emerged adult more expertise in rearing and organism-handling tech- (Hallman 2004b, Hallman and Thomas 2010). niques than other treatments because organisms must Research that allows for live adults to be present at be held under favorable conditions and monitored for least for a few days postirradiation should monitor the efÞcacy until they die, and controls must perform behavior of those adults until they die to estimate the within expected norms. The IPPC vetting process has likelihood of their detection by survey programs in identiÞed areas where increased attention to research importing countries. If it was determined that the pests is recommended. could be found by the trapping systems used, the PI 1960 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 6 treatment might not be permitted unless it could be Aldryhim, Y. N., and E. E. Adam. 1999. EfÞcacy of gamma determined that any adults found in survey traps were irradiation against Sitophilus granarius (L.) (Coleoptera: adequately irradiated. Curculionidae). J. Stored Prod. Res. 35: 225Ð232. Several techniques have been developed to identify [APHIS] Animal and Plant Health Inspection Service. 1996. irradiated organisms. They may not be very precise or The application of irradiation to phytosanitary problems. easy to apply and largely depend on holding the or- Fed. Reg. 61: 24433Ð24439. ganism for a while to track abnormal development [APHIS] Animal and Plant Health Inspection Service. 2002. Irradiation phytosanitary treatment of imported fruits (Heather and Hallman 2008). Thus, they are not gen- and vegetables. Fed. Reg. 67: 65016Ð65029. erally useful at points of inspection. Although having [APHIS] Animal and Plant Health Inspection Service. 2005. reliable techniques that could be quickly used at Treatments for fruits and vegetables. Fed. Reg. 70: 33857Ð points of inspection for validating treatment efÞcacy 33873. would be useful, the development of such techniques [APHIS] Animal and Plant Health Inspection Service. 2006. may not be generally feasible and should not delay use Importation of fresh Mangifera indica (mango) fruit from of irradiation as a phytosanitary treatment. The United India into the continental United States. (http://www.aphis. States and New Zealand (the only countries currently usda.gov/newsroom/hot_issues/indian_mango/download/ importing commodities irradiated for phytosanitary RMindmang.doc). purposes), the countries exporting these commodi- [APHIS] Animal and Plant Health Inspection Service. 2007. ties, and several other interested countries have ac- Importation of Litchi chinensis (litchi or lychee), Dimo- cepted this concept, but resistance by other countries carpus longan (longan), Mangifera indica (mango), Gar- has delayed or hindered the IPPC approval of some cinia mangostana L. (mangosteen), Nephelium lappaceum L. (rambutan), and Ananas comosus (pineapple) into the treatments. United States from Thailand. (http://www.aphis.usda. Infestation Techniques. Some PI treatments were gov/newsroom/hot_issues/thai_irradiated_fruit/download/ developed using artiÞcial infestation techniques with- Thailand_6_RMD.doc). out comparing the results with natural infestation. It [APHIS] Animal and Plant Health Inspection Service. has been known for years that tephritids may be con- 2008a. Interstate movement of fruit from Hawaii. Fed. trolled with much lower doses in vitro than in fruit, so Reg. 88: 24851Ð24856. any infestation technique that strays from the natural [APHIS] Animal and Plant Health Inspection Service. state should be tested before being used to develop 2008b. Importation of fresh guava (Psidium guajava) treatments. Although Hallman and Thomas (2010) fruit from Mexico into the United States treated with 400 noted in PI studies with C. capitata by using insertion Gy irradiation. (http://www.regulations.gov/search/Regs/ ϭ ϭ of third instars into fruit that adult emergence was contentSteamer?objectId 090000648062f2c9&disposition ϭ prevented with slightly lower doses than studies using attachment&contentType msw8). infestation via oviposition, they found no statistically [APHIS] Animal and Plant Health Inspection Service. 2008c. Importation of red dragon fruit (red pitaya) (Hylocereus spp.) signiÞcant difference between insertion of diet-reared from Vietnam into the continental United States. (http:// third instars in fruit 24 h before irradiation versus www.regulations.gov/search/Regs/contentSteamer? infestation by oviposition for A. ludens. In two studies objectIdϭ09000064805533e5&dispositionϭattachment& with Lepidoptera, diet-reared insects were no easier contentTypeϭpdf). to control than host-reared ones meaning that diet- [APHIS] Animal and Plant Health Inspection Service. reared ones could be used to develop PI treatments 2010a. Changes to treatments for sweet cherries from (Hallman 2004a, Hallman and Hellmich 2009). Australia and irradiation dose for Mediterranean fruit ßy. Controls. Some PI treatments were approved al- Fed. Reg. 75: 46901Ð46902. though the controls did not perform within the range [APHIS] Animal and Plant Health Inspection Service. of expectation, meaning that experimental conditions 2010b. Treatment manual. (http://www.aphis.usda.gov/ _ were not favorable for the organisms. Both control and import export/plants/manuals/ports/treatment.shtml). irradiated organisms should be held under conditions Arthur, V., C. Caceres, F. M. Wiendl, and J. A. Wiendl. favorable for development and reproduction until all 1993a. Controle da infestaçaõ natural de Ceratitis capitata (Wied., 1824) (Diptera, Tephritidae) em pessegos irradiated organisms die. ˆ (Prunus persica) atrave´s das radiaço˜es gama. Sci. Agric. Piracicaba 50: 329Ð332. Arthur, V., F. M. Wiendl, and J. A. Wiendl. 1993b. Controle Acknowledgments de Ceratitis capitata (Wied., 1824) (Diptera, Tephritidae) em peˆssegos (Prunus persica) infestados artiÞcialmente We thank Neil Heather (University of Queensland, atrave´s das radiaço˜es gama do cobalto-60. Rev. Agric., Queensland, Australia) and Carl Blackburn (Food Irradia- Piracicaba 68: 323Ð330. tion Specialist, International Atomic Energy Agency, Vienna, Arthur, V., F. M. Wiendl, J. A. Wiendl, and A. Correa da Silva. Austria) for reviewing an earlier draft of the manuscript. 1994. Inßueˆncia das das radiaço˜es gama do cobalto-60 em larvas e pupas de Anastrepha obliqua (Mac., 1835) (Diptera: Tephritidae). Rev. Agric. Piracicaba 69: 121Ð References Cited 128. Ayvaz, A., and A. çS. Tunçbilek. 2006. Effects of gamma Al-Taweel, A. A., H. K. Al-Ubaidy, and H. S. Al-Asaady. 2007. radiation on life stages of the Mediterranean ßour moth, Sensitivity of some stages of Phthorimaea operculella Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). J. 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radiaçaõ gama, Ph.D. dissertation. University of Saõ nean fruit ßy (Diptera: Tephritidae). Fla. Entomol. 90: Paulo, Saõ Paulo, Brazil. 343Ð346. Ravuiwasa, K. T., K.-H. Lu, T.-C. Chen, and S.-Y. Hwang. Tunçbilek, A. c`S., and I. A. Kansu. 1966. The inßuence of 2009. Effects of irradiation on Planococcus minor rearing medium on the irradiation sensitivity of eggs and (Hemiptera: Pseudococcidae). J. Econ. Entomol. 102: larvae of the ßour beetle, Tribolium confusum J. du Val. J. 1774Ð1780. Stored Prod. Res. 32: 1Ð6. Rigney, C. J., and P. A. Wills. 1983. EfÞcacy of gamma ir- Vijaysegaran, S., P. F. Lam, R. M. Yon, M.N.A. Karim, H. radiation as a quarantine treatment against Queensland Ramli, and N. Yusof. 1992. Gamma irradiation as a quar- fruit ßy, pp. 116Ð120. In J. H. Moy [ed.], Radiation dis- antine treatment for carambola, papaya, and mango, pp. infestation of food and agricultural products. University 53Ð76. In Use of irradiation as a quarantine treatment of of Hawaii, Honolulu. Saour, G., and H. Makee. 2004. Susceptibility of potato tu- food and agricultural commodities. International Atomic ber moth (Lepidoptera: Gelechiidae) to postharvest Energy Agency, Vienna, Austria. gamma irradiation. J. Econ. Entomol. 97: 711Ð714. Torres-Rivera, Z., and G. J. Hallman. 2007. Low-dose irradiation phytosanitary treatment against Mediterra- Received 17 June 2010; accepted 25 August 2010.