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έ៉‫ٿ‬ᖪ 27: 1-15 (2007)


Formosan Entomol. 27: 1-15 (2007)

Irradiation for Postharvest Control of Quarantine Insects


Peter A. Follett U.S. Department of Agriculture, Agricultural Research Service, U.S. Pacific Basin Agricultural
Research Center, Hilo, Hawaii 96720, U.S.A.
Man-Miao Yang, Kuang-Hui Lu* Department of Entomology, National Chung Hsing University, Taichung 402,
Taiwan
Tse-Wei Chen Plant Quarantine Division, Bureau of Animal 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 Lepidoptera
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: khlu@dragon.nchu.edu.tw! Irradiation for Postharvest Control of Quarantine Insects 1
regulatory pests in exported commodities 2006). For example, Japan, 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 insect 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 Arthropod 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 (moths
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 moth, 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

2 έ៉‫ٿ‬ᖪௐ˟˩˛‫ס‬ௐ˘ഇ
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

4 έ៉‫ٿ‬ᖪௐ˟˩˛‫ס‬ௐ˘ഇ
(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

6 έ៉‫ٿ‬ᖪௐ˟˩˛‫ס‬ௐ˘ഇ
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
Omphisa 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 sweet potato (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

8 έ៉‫ٿ‬ᖪௐ˟˩˛‫ס‬ௐ˘ഇ
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

10 έ៉‫ٿ‬ᖪௐ˟˩˛‫ס‬ௐ˘ഇ
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),
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97: 1254-62. possible quarantine treatment for
Follett, P. A., and Z. Gabbard. 2000. green scale Coccus viridis (Green)
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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
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Sitophilus oryzae (L.) (Coleoptera: carambola fruit borer, Eucosma
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Sproul, A. N. 1976. Disinfestation of USDA-APHIS. 2006. Treatments for fruits
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USDA-APHIS. 2002. Irradiation Phytosanitary Estimation of the probability of an
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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.

14 έ៉‫ٿ‬ᖪௐ˟˩˛‫ס‬ௐ˘ഇ
Ꮼड໰ड‫ٺ‬ᑭࠪचᖪ̝ଳ‫ޢ‬఍ந
Peter A. Follett! U.S. Department of Agriculture, Agricultural Research Service, U.S. Pacific Basin Agricultural
Research Center, Hilo, Hawaii 96720, U.S.A.
໅તӻ! ྮЍິ*! ઼ϲ̚Ꮈ̂ጯ‫ٿ‬ᖪጯր! έ̚ξ 402 ઼Ѝྮ 250 ཱི
ౘ̄ઈ! Җ߆ੰྺຽ؎ࣶົજങ‫ࠪ֨ۏ‬ᑭࠪԊങ‫ۏ‬ᑭࠪ௡! έΔξ 100 ࢦᇉ‫ ߱˟ྮݑ‬51 ཱི 9 ሁ

ၡ! ! ࢋ

! ! Ꮼड໰डĞirradiationğѝ̏జϡࠎໝੵྺய‫˯ݡ‬ѣचϠ‫۞ۏ‬఍ந͞‫̝ڱ‬ʑĄ‫ܕ‬
ѐֽϤ‫઼ٺ‬ᅫങ‫ܲۏ‬᜕̳ࡗĞThe International Plant Protection Convention,
IPPCğ‫ֹ˞ؠט‬ϡᏬड໰डซҖᑭࠪ఍நĞphytosanitary treatmentğ۞઼ᅫఢቑĂ
Հֹܳ‫׎‬ు႙‫זצ‬Ч઼۞ࢦෛĄ˘ਠྺய‫ݡ‬གྷϤዋ༊۞Ꮼड໰ड጗ณĂӈΞд̙ᇆᜩ
‫ݡ‬ኳ۞ଐ‫˭ڶ‬Ă၆кᇴचᖪĞ螨ğயϠ։р۞ໝੵड़‫ڍ‬Ğdisinfestation effectğĄᄃ
‫΁׎‬ᑭࠪ఍ந͞‫ྵ࠹ڱ‬ĂᏬड໰ड఍ந̙֭ͽϲӈ୭ѪचᖪĞ螨ğ۞͞ёֽቁܲᑭࠪ
۞щБّĄЯࠎགྷ࿅Ꮼड໰ड఍ந̝ྺய‫ݡ‬Ăᔵ൒‫۞̚׎‬ᑭࠪचᖪĞ螨ğ̪Ξਕх߿Ă
ҭιࣇ̏ߏ̙θ۞ٕߏ‫ͼܕ‬Ѫ˸۞Ăซ˾઼̙֭ᅮࢋГਈ෱ჟ˧ᑭෛιࣇߏӎхдĄ
ϫ઼݈࡚߆‫ع‬Հࢎ‫˞ؠ‬Ꮼड໰डઇࠎЧёྺய‫ݡ‬ᑭࠪ఍ந۞В఼఍ந጗ณĞgeneric
treatment dosesğĂּтໝੵЧᙷ‫ڍ‬၁ᙀ۞В఼఍ந጗ณࠎ 150 GyĂ҃ੵសਂϫ۞
ུᄃјᖪĞᅮགྷྵ੼۞጗ณ఍நğͽγĂ‫׎‬ιᑭࠪचᖪĞ螨ğ۞В఼఍ந጗ณࠎ 400
GyĂ̯֭ధкีགྷѩඈ጗ณ఍ந̝ྺய‫ݡ‬གྷ࿅ᑭࠪᄮᙋ‫ۡޢ‬ତᏮˢĄᏬड໰डВ఼఍
ந጗ณ۞ࢎ‫ؠ‬Ă̙ҭΞΐిপ‫ྺؠ‬ய‫ݡ‬ӀϡᏬड໰ड఍நͽ௑ЪᑭࠪࢋՐĂТॡϺΞ
ΐి‫΁׎‬າྺய‫ݡ‬д઼ᅫξಞ۞ฟ٤ĂЯࠎາ۞ྺய‫่ݡ‬ᅮֶѩૄ໤఍ந࿅ӈΞ఼࿅
ᑭࠪᄮᙋĂ̙ᅮГਈ෱̴‫۞ܜ‬ॡมĂ੫၆̙ТचᖪĞ螨ğซҖЧ჌̙Т۞ᑭࠪ఍நྏ
រĂ̖Ξਕᒔ଀ซ˾઼۞ᑭࠪᄮᙋĄЯѩĂ࠹ྵ‫׎ٺ‬ιᑭࠪ఍ந͞‫ڱ‬ĂϤ‫ٺ‬В఼఍ந
጗ณ۞ቁϲĂֹ଀Ꮼड໰डјࠎ˘ีஎ‫׍‬ሕ˧ă֖ͽ‫΁׎΃פ‬ᑭࠪ఍ந۞ആ΃͞‫ڱ‬Ą

ᜰᗤຠȈᏬड໰डăങ‫ۏ‬ᑭࠪ఍நăᑭࠪचᖪăprobit 9 ۞ᏴፄăВ఼఍ந጗ณĄ

*ኢ͛ᓑᘭˠ
Irradiation for Postharvest Control of Quarantine Insects 15
e-mail: khlu@dragon.nchu.edu.tw

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