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Physics » Biophysics » "Evolution of Ionizing Radiation Research", book edited by Mitsuru Nenoi, ISBN 978-953-51-2167-1, Published: September 17, 2015 under CC BY 3.0 license. © The Author(s).

Chapter 10

Ionizing Radiation Disinfestation Treatments against Pest Insects

By Abdurrahman Ayvaz and Semih Yilmaz
DOI: 10.5772/60923

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Ionizing Radiation Disinfestation Treatments against Pest Insects

Abdurrahman Ayvaz1 and Semih Yilmaz2

1. Introduction

Chemical pesticides have been the most widely used insect control methods, especially after the Second World War together with the invention of synthetic chemical pesticides. Pesticides are often considered a suitable solution for controlling pests. However, the use of chemicals is very costly and has polluted almost every part of our environment. Pesticide residues are found in soil, air, and ground water and they poses significant risks to the natural ecosystems and nontarget organisms.

There are two overriding problems facing insect controlling specialists. These concerns are the rapid development of resistance and environmental pollutions resulting from pesticide use. It was reported that irradiation could offer substantial and charming option for eliminating the export commodity fumigation uses for the undesirable effects of chemicals [1, 2]. In many countries, the direct control of stored product insects in wheat and wheat flour through radiation treatments is regarded as an approved method and would soon be approved for all grain products and other dry foods [3]. To this end, research is needed to continue for improving the methods. Although irradiation quarantine disinfestation treatment has been in progress for decades, it is not so common to use these tactics because radiation cannot kill the insects abruptly, and there are great concerns with regard to radiation applications among peoples. Due to the relationship with radioactivity and nuclear technology, consumers and industrial organizations have significant concerns about the radiation applications in food preservations, whereas even at the highest doses, radioactivity cannot be induced using these sources in food or insects exposed [4]. Accordingly, the development of radiation methods in controlling the agricultural products is so slow, and the adoption of these practices by the public and commercial organizations takes time. Informing the public awareness on the issue of the reliability of this method will enable more widespread use of these applications and will provide more acceptances by people. If safer and more secure products are obtained as a result of food irradiation and consumers are satisfied with the nutritional adequacy, their attitudes can be positive and they will buy the products without hesitation.

The superiority of irradiation in protecting agricultural products can be summarized as follows: it reduces product loss after harvesting. In terms of treating the products uniformly, it is more advantages over the fumigation treatments. It leaves no residues on the products and a best alternative to chemicals ensuring product quality standards in international trade [5]. It is also an important strategy for improving the hygienic quality of the agricultural products. The future inclination in quarantine measures against insect pests will mainly focus on the following issues: (1) determining specific doses for the insects resistant to radiation such as lepidopteran pests, (2) reducing radiation doses and abate treatment periods to maintain the product quality, (3) developing generic treatments lower than 400 Gy for important quarantine insects, and (4) developing information on value-added irradiated fresh products [6]. The standardized radiation treatments will facilitate safer trade between countries. The measures taken with radiation aim to prevent adult insect emergence. In this way, the risk of introducing exotic plant pest into new ecological areas during trade between countries can efficiently be prevented [6]. If there are eggs, larvae, and pupae in agricultural products, they are intended to be sterile. By examining numerous studies, these goals can be achieved with relatively lower doses for the pests belong to Diptera, Homoptera, and Coleoptera. Lepidopteran pests require higher doses than other groups. Radiation resistance of insects increase with advanced developmental stages. The tolerance of male insects is higher than that of females.

This review aims to provide information in presenting advances related to irradiation quarantine treatments against pest insects, assessing the worries in this field, discuss apprehensions with the applications, stressing the future trends, and explaining the mode of action of radiation on pest insects.

2. Ionizing radiation sources

Ionizing radiation has been classified into X-rays, γ-rays, α-rays, β-rays, and neutron radiation [7]. Nature and background are the main sources of ionizing radiation. Of these, cosmic radiation can be classified into various forms according to its origin, energy and type, and flux density of the particles. Tree main sources of cosmic rays are galactic cosmic radiation, solar cosmic radiation, and radiation from the earth’s radiation belts (Van Allen belts) [8]. Gamma radiations have the possibility to ionize the atoms but not affect the nucleus, so they cannot induce radioactivity on irradiated materials [9]. Among the ionizing radiation sources, gamma rays, high-energy electrons, and X-rays are the types used practically in sterile insect releasing programs [10-12]. However, α particles are not suitable for insect sterilization due to their high linear energy transfer and weak penetrability. On the other hand, neutrons are more effective in insect sterilizing, but their radioactivity induction in irradiated materials makes them impractical for sterile insect technique (SIT) programs [13-15]. It should be taken into consideration that for the fitness of insects, the acceptable level of energy for SIT applications is less than 5 MeV for Gamma rays (from 60Co and 137Cs) or X-rays and less than 10 MeV for electrons [4, 16-18]. Due to their similar relative biological effectiveness values, a different type of radiation source does not exert significant difference in their lethal effects on particular insects [4]. Cobalt-60 and cesium-137 radioisotopes are the most commonly used gamma radiation sources for SIT programs [8].

3. Comparison of irradiators

Irradiators with several hundreds to thousands of Curies of a high-energy gamma or beta emitter are large self-shielded devices. The basic components of an irradiation unit (gamma-ray or electron) are composed of the following: (1) the control systems related to radiation source are referred as “irradiators,” (2) a product transport system, and (3) a shielding for protecting human health and environment from radiation [4].

Two major types of irradiator are “self-contained” and “non-self-contained or panoramic.” In the former, primary beam is entirely shielded during use and storage conditions. In the latter, primary beam is not contained [19]. Irradiator design varies from small, which is suitable for radiation studies, to very large, which is convenient for hundreds of tons of product throughput daily. The activity level of the radiation source and the methods for the translocation of the products in the radiation field are the main differences between various irradiators [4].

Both cobalt and cesium are widely used as source rods in gamma irradiators [4]. Sterilization of insects is usually carried out with gamma rays from self-contained irradiators. In most self-contained irradiators, the position of irradiation is in the center of an annular array of long parallel pencils that include the encapsulated radiation source. Within this irradiation compartment, the doses are provided uniformly. Although self-contained irradiators provide a high-dose rate with a small irradiation volume (1–4 L), this design is suitable for small-scale programs that apply the SIT [4].

Panoramic irradiators are used efficiently for large-volume irradiation. In this design, the radiation source includes either several Co-60 rods lined up in a plane or a single rod that can be moved up and down into a wide chamber. Because gamma rays are emitted in all directions from isotopic sources, the high-energy utilization efficiency can be achieved through surrounding by insects, and irradiation can be applied to several containers at the same time [4]. Large-scale commercial irradiators are mostly not practical for practicing dosage-determining research due to differences between maximum and minimum absorbed doses received. Therefore, the determination of minimum absorbed dose required for an irradiation quarantine application is best performed using small irradiators [20].

Electrons and X-ray are the two modes of accelerator-generated radiation in electron and X-ray irradiators. The two characteristics of the principal electron-beam are the energy of particles (MeV), which affects the penetration of electrons, and the average current (in mA), which affects the rate of absorbed dose. Contrary to gamma rays, electron beams from accelerator-generated radiation are quite focused, and insects are continuously moved in conveyors through the beam. Due to the deeper penetration of X-rays compared to electrons, it allows the use of larger containers of insects for treatments [4].

Although sterilizing effects of electron and gamma rays are similar, the factors determining the source selection for SIT programs mostly depend on penetration, cost, product throughput, presence of experts, and safety factors [21]. Besides, gamma irradiators are normally cheaper and easier to run when compared with accelerators. However, due to their safety when switched off, the reliability and the public acceptance of electron accelerators are higher than gamma source [22-24]. The emission power of 100 kCi of Co-60 gamma-ray source is more or less equivalent to that of a 1.5-kW electron accelerator. The commercial accelerators have usually higher power capacities (5–10 MeV electrons), thus rendering them unsuitable for SIT applications. Although X-ray irradiators have the advantages over the gamma irradiators and accelerators, the effectiveness of transforming electrons into X-rays is nearly 7% for 5 MeV electrons. Thus, a great majority of the power is wasted while heating the converter [25]. When these conditions are all considered, gamma irradiators can be thought as mostly used in nearly all SIT programs [4].

4. Dosimetry

Dosimetry is the radiation absorbed dose for sterilizing and is of major importance for programs that comprise the release of sterile insects [26]. Dosimeters are frequently used in producing sterile insects for such tasks as absorbed-dose mapping, process control, and qualification of the irradiator [4]. Some of them are convenient for routine use at SIT programs [27]. Insects receiving very low doses may not adequately be sterile, and those that absorb very high may be uncompetitive. In such cases, the effectiveness of the program that requires a greater number of sterile insects to be released may essentially be decreased [28]. In executing the analysis, variation in both dose-dependent sterility and competitiveness data are required at the same time. For the competitiveness data to be realistic, the tests should be performed in field cages or open plots [26]. Given the importance of dosimetry in SIT programs, selecting a convenient dosimetry system has a critical importance [26]. Methods for calibrating regular dosimetry systems and for determining radiation fields for insect sterilization are described in periodically updated ISO/ASTM standards [27, 29-31] and in IAEA technical reports [9]. Gray (Gy) is used as the absorbed dose unit, which is equivalent to a joule of absorbed energy per kilogram of sample [9]. Therefore, in newly planned programs, dosimetry system needs to be established for adequately measuring the absorbed dose and estimating the associated confidence interval [27].

5. Doses achieve quarantine security

Irradiation is a quarantine treatment with the potential to disinfest a variety of fresh commodities of great number of quarantined pests. Many insect groups from the orders Diptera, Coleoptera, and Homoptera can be controlled with relatively low doses without damaging host plants of economic importance [20]. Other insects in Lepidoptera are controlled by moderate doses (0.2–0.3 kGy), which are tolerated by some major commodities, such as apples, cherries, and blueberries [20]. These doses need further evaluation using adequate numbers of insects to accomplish the degree of confidence required in quarantine treatments [20].

Moreover, because effective irradiation doses against most insects and mites do not affect the characteristics of commodities, this technology is ideal in developing “generic” treatments [32]. A generic quarantine treatment should provide quarantine security for large insect groups. For example, it can be applied to all pests belonging to Diptera, or to tephritid fruit flies in the genus Bactrocera. Before recommending generic treatments, effective irradiation doses should be evaluated in controlling the wide range of species belonging to a taxon [32] (Table 1).

Pest group Objective Dose (kGy)
Stored product mothsAdult sterilization0.1–1
Stored product beetlesAdult sterilization0.05–0.4
Pyralidae and TortricidaeLate-pupa sterilization0.2–0.3
Noctuidae and TortricidaePrevent adult emergence0.1–0.3
Scarab beetlesAdult sterilization0.05–0.15

Table 1.

Doses to achieve quarantine security for various pest insects [20]

6. Advantages of irradiation over other postharvest treatments

The advantages of irradiation in controlling agricultural products can be outlined as follows: It is an effective and important tactic in controlling postharvest food losses. It is more advantageous compared to fumigation treatments due to its uniform penetration in the products and also time saving. It does not leave residues in commodities and a best alternative over chemical pesticides ensuring product quality standards in international trade. It is also an important strategy for improving the hygienic quality of the agricultural products [5]. The penetration power and the dose uniformity of the radiation treatment to treat products of different sizes and shapes and also to prevent the formation of resistance make the radiation treatments superior to chemicals [33]. Besides, radiation can reach pathogen organisms in areas of fruits not accessible to chemicals [34].

Because of growing concerns related to health problems and environmental pollutions, chemical sanitizing treatments are faced with a lot of regulatory restrictions. Thus, irradiation offers the most viable alternative for eliminating these concerns [5]. It was also reported that the minimum dose (150 Gy) required for disinfestation of fruit fly to satisfy quarantine regulations (0.15 kGy) does not adversely affect the physicochemical and nutritional value of most fruits and vegetables [35]. If the application is done properly, the efficacy of the irradiation process is guaranteed. It does not cause a significant amount of temperature increase during application; radiation does not leave residues. It is safe and removes concerns that may arise in terms of human health and environment. It is possible to apply for packaged products. However, some other disinfestation methods such as heat, cold, and fumigation treatments can be used in controlling pest insects in the commodities. For controlling pest species, irradiation treatments should be developed irrespective of commodity. Most products can have tolerance to irradiation at doses killing the pest; however, other methods cannot guarantee quality of the host commodities [4].

7. A generic quarantine treatment

Introducing exotic pest insects through the improvement of international world trade in agricultural commodities becomes increasingly important problem day by day. This new problem will cause extra costs for control programs and quarantine restrictions [36]. A generic quarantine treatment is one that provides quarantine security for a broad group of pests [37]. The International Consultative Group on Food Irradiation (ICGFI) was the first group to formalize a recommendation for a generic treatment. In 1986, based on irradiation data for many tephritid fruit fly species and a limited number of other insect pests, ICGFI proposed a dose of 150 Gy for fruit flies and 300 Gy for other insects [38]. Before generic treatments can be recommended, information is needed on effective irradiation doses for a wide range of insects within a taxon [36]. Data from all available insects are used in developing generic treatments because they serve as representatives for their respective groups [39]. According to a rule published in the United States in 2006, a dose of 150 Gy generic radiation was determined for all tephritid fruit flies and 400 Gy for all other insects, except for pupae and adults of lepidopteran pests, which require higher doses [40].

Some other applications such as heat, cold, and fumigation are used to disinfest host commodities before exporting them to pest free area. However, the treatment process other than irradiation requires balancing between the adverse effects and killing the pest insects to preserve commodity quality [41] since radiation treatments target pest insects without damaging the fruit or vegetable host [36]. For example, radiation prevents the temperature increase in commodities. International standard institutes approved that radiation is valid for all fruits and vegetables that are hosts for the given pests [42, 43].

Expanding the application spectrum of the generic irradiation treatments in the family or order level in other taxa would be practical, would easily promote international trade in agricultural products, and would supply an alternative treatment for infested commodities in cross-country transportation [44].

8. Integrated pest management programs

The process of pest control is becoming more complex and requires new solutions in the course of time due to the emergence of new pest population, strict regulation in international trade, insecticide resistance, and residue problems. These new problems made it necessary to develop new and cleverly designed pest control techniques. Integrated pest management (IPM) is largely accepted as a powerful and environmentally sensitive method in managing pest insects that relies on a combination of commonsense practices [45]. In IPM strategies, comprehensive information on the life cycles of pests and their interaction with the environment is used. This method, in combination with available pest control tactics, is applied to manage pest population damage with the least possible hazard to people, property, and environment [45].

As a part of an area-wide integrated pest management (AW-IPM) approach, the sterile insect technique (SIT) is regarded as a vigorous control strategy for establishing pest free areas. The development of more competitive moths may improve the effectiveness of AW-IPM programs integrated with SIT technique [46, 47]. Species-specific nature and compatibility with existing control methods (biological control, mating disruption, cultural control, and use of biorational pesticides) make SIT an indispensable part of AW-IPM application and also make it superior to other control methods [48-50]. There are a number of successful models in terms of integrating the SIT in AW-IPM programs against many important lepidopteran pests [51, 52].

Based on herein and other numerous literature, it may be said that SIT is a very convenient method as part of AW-IPM programs and can be further developed by decreasing the production costs, improving the effectiveness of released sterile moths and combining to other effective control tactics [53] .

9. Principles and practices of sterile insect technique

The idea that populations of economically important insect species might be controlled, managed, or eradicated through genetic manipulation was supposed by Knipling in 1930s. A similar concept was published independently by Serebrovsky [54]. In the late 1930s, Knipling recommended that if there could be a way to genetically sterilize male insects without affecting their ability to mate and competitiveness, then subsequent to their release and mating with wild females, the fertility of a target population could be reduced. The sterile insect technique is an environmentally innocuous and target-specific control tactic in suppressing the pest population [49]. With the development of modern genetic methods, this method will become a promising technique in the near future in controlling many important pest populations [55, 56].

The first applications were performed on the New World screwworm Cochliomyia hominivorax to evaluate this procedure [57]. The induction of sterility in this species by X-rays was the first small step on the way to the eradication of the serious livestock pest from Southern America and now from most countries of Central America [57]. This long-term and successful program has demonstrated that radiation-induced mutations can play an important role in developing environmentally acceptable, area-wide, and pest intervention strategies.

Although open to scientific criticism, the eradication process has been processed across the southern parts of the United States. With the help of this program, which began in Florida in 1957, the entire population of the pest is eradicated in the United States within a period of 10 years. Due to the reinfestations of migrating flies from neighboring Mexico, the program has been compromised, and the United States–Mexico joint program has become a necessity in 1972. With the success of the program, Mexico in 1991, Belize and Guatemala in 1994, and El Salvador in 1995 officially declared that they are free of screwworms. Because no flies have been detected since January 1995, Honduras was technically considered as free of screwworms. Eventually, the United States–Central America project proposed to maintain a sterile insect barrier at the Darien Gap in Panama starting in 1997. By the implementation of this program, billions of dollars was saved in livestock and wildlife loses [57]. Screwworm is an obligatory parasite of warm-blooded animals infesting livestock and mammals, including humans. Female flies lay their eggs on the wounded inflammatory region of the body. Larvae hatching from the eggs feed on the flesh. Because these flies were easy to rear, the program was composed of a small-scale wild adult population. The flies tend to mate only once the screwworm was a good candidate for SIT program. These factors were optimum to achieve high sterile/fertile ratios fort this pest [58].

Although not as successful as the screwworm eradication program, SIT has been implemented for some other pest populations such as the tephritid fruit flies, including Ceratitis capitata Wiedemann, Pectinophora gossypiella Saunders, and Cydia pomonella L. in many parts of the world [59].

Pests of agricultural, veterinary, and medical importance can be specifically controlled using the SIT method, the integral component of AW-IPM. The sterile insect technique (SIT) is a specific control method that may be applied in the area-wide integrated pest management of insects. It is important to release only the sterile males to implement this method effectively [60]. As the next generation is to be established by wild females, the removal of wild males is essential for reducing the size of target population [61]. Infertility in the wild population can only be achieved with the help of sterile males. Thus, this method was initially named as the sterile-male method [62]. At the first application, both sexes were released in controlling the New World screwworm C. hominivorax. However, the benefit of this bisexual releases was determined to be limited for the Mediterranean fruit fly [63-65]. In such a design, released sterile males and females tend to mate with each other. This inclination reduces the mating potential of sterile males with wild females, and less sterility is introduced into the wild population. Only sterile male release reduces mass rearing costs for both production and postproduction stages. In the postproduction stage, considerable reductions can be achieved in the cost of workload, marking, irradiation, transport, release, and monitoring [66]. In many cases, releasing sterile females is not an easy process and brings about further negative effects. For example, females of fruit fly may cause extra damage in some fruits, females of biting flies result in reducing livestock meat production, and females of blood-sucking species may transmit disease [67]. However, it is not easy to make sex separation in such large populations. Therefore, to overcome this problem, it is obligatory to develop new specific strains. To date, Mendelian genetics, chromosome rearrangements, and specific mutations can successfully be used to develop new strains. When the sterile insect technique is compared with pathogenic biological entities and toxic chemicals, it is noninvasive. Therefore, the environmental risks of SIT application are exceptionally very low [68, 69]. This method is also compatible with the food chain in terms of integrating ecosystems with living but nonreproductive organisms. When considering all these situations, the hazard of the SIT to the environment is negligible.

There are some components that make the sterilization techniques successful [70], and the principles of sterility have not changed significantly since E. F. Knipling’s formulation:

  1. Mass rearing of target insects should be easy and applicable (rearing component).

  2. Large numbers of the target insect should be possible to sterilize (treatment component).

  3. Following sterilization, fairly competitive insects should be released (competitiveness component).

  4. Release and distribution of sterile insects into fields should be cost effective (release component).

  5. Before and after the release of the treated insects, population should be assessed accurately by using special tools (evaluation component).

  6. The treated area should be well isolated to prevent inseminated females from entering the field (reinfestation component).

10. Improvement of the sterile insect technique thorough genetic engineering technology

The sterile insect techniques (SIT) are considered as releasing sterile males in area-wide pest management. In this context, with the use of genetic methods, infertile matings were enhanced utilizing the release of mass-reared sterile insects [49, 71-73]. Therefore, by genetic means, new insect strains developed for improving SIT activity or avoiding potential adverse effects of such releases. Two categories of genetic methods for strain development are considered as conventional genetics and transgenesis [74, 75]. Using these methods, the development of an efficient and cost-effective SIT program would have a great importance in eliminating females from the released population. In this respect, the sterile insect technique may possibly be improved and extended using modern molecular tools. For example, SIT programs are improved by releasing unirradiated but instead homozygous insects with dominant lethal (RIDLs) constructs that are repressible during mass production [56, 76, 77].

A female-lethal version of RIDL, with insects homozygous for one or more female-specific dominant lethal genetic constructs, has been created in C. capitata and offered for many other species [78] . This approach is also known as autocidal biological control [79]. The identification of alternative and more promiscuous transposable elements as hermes, hobo, minos, mosI, and piggyBac and novel gene delivery systems such as microinjection, electroporation, sonoporation, lipofection, and biolistics prompted studies on genetic manipulation of many insects of agricultural importance for various purposes [76, 80, 81].

The nature and timing of lethality is one of the most important potential advantages of genetic methods over radiation-based SIT programs. The transmission of transgenic SIT methods to insects of agricultural importance is now applicable through the development of sophisticated vectors incorporating the piggyBac transposable element [82, 83] and transformation markers based on improved green fluorescent protein (EGFP) variants [84, 85]. This technology was supposed to facilitate the development of transgenic insects for sustainable tactics to control pest populations or disease vectors [86, 87]. In addition, the use of systems for marking transgenic sperm in SIT programs is one of the other significant improvements for addressing the lack of efficient and reliable methods in field monitoring of insects. In SIT programs, producing male-only sexing strains for converting female insects into males thorough genetic manipulations in sex determining pathways can be another strategy [88, 89]. In the medfly, such a phenomenon has been shown to conditionally express a transgene that interferes with the expression of female-specific tra gene expression. The resulting population was reported to comprise 95% males and 5% intersexes [89].

11. Radiation-induced F1 sterility in lepidopteran pests

If the parental generation of these insects was irradiated with substerilizing doses of gamma radiation, the degree of sterility would be higher than that of parental generation, and this circumstance is known as radiation-induced F1 sterility [15, 90]. Because the pest insects from Lepidoptera are radioresistant species, high doses are required to achieve complete sterility when compared to other pest insects from different orders [4, 91]. Despite continued for several generations, radiation-induced detrimental effects are most pronounced in the F1 generation. Inherited sterility is also referred as inherited partial sterility, partial sterility, delayed sterility, semisterility, and F1 sterility [52]. Mutagenic chemical substances (chemosterilants) can be used to induce sterility as an alternative to radiation, but due to human health and environmental concerns, chemicals are not preferable for obtaining sterilized mass-reared insects today [92, 93].

Inherited sterility has been shown for the first time on silkworm Bombyx mori (L.) [94]. Early investigations related to this topic were revised and discussed in terms of its pest control potential and genetic aspects [15, 90]. Experiments of the Proverb [95] showed that the F1 generation of insects was sterile when their parents irradiated with gamma radiation. This first application has opened up new horizons and given impetus to research on F1 sterility [96]. Knipling [97] and LaChance [90] recommended the use of F1 sterility as the potential component of area-wide integrated management of lepidopteran pests. The validity and efficacy of the method has been indicated on various pests in a number of laboratory studies [90]. However, a high dose of radiation adversely affects some important traits of the pest population as mating ability and longevity and causes reduction in the competitiveness of the sterile insects against the wild population [98]. This control tactic represents an environmentally friendly alternative and provides facilities for control of many important pest species. The superiority of this method over the completely sterile insect is discussed by many authors [52, 99-102].

For the high radio resistance in lepidopteran insects, the presence of possible DNA repair mechanisms and an inducible cell recovery system was proposed [91]. The radio-tolerant talent of these insects has also been attributed to the holokinetic nature of their chromosomes [103]. Radiation-induced sterility is generally a result of dominant lethal mutations (DLMs) in insects other than lepidopterans and is expressed during early cell proliferation in embryogenesis [52, 104]. However, the frequency of DLMs is much lower in Lepidoptera than that of other pest orders and is seen toward the end of embryonic development [105].

Since sterile F1 progeny are produced under field conditions, releasing partially sterile males with fully sterile females is more compatible with other tactics [106]. A significant amount of the unfertilized eggs or early embryonic mortality was observed for different lepidopteran pests in treated males mated with the females as in the case of Manduca sexta (L.), Ephestia kuehniella Zeller, and Spodoptera litura (F.) [107-109]. It can be inferred that the most important cause of male sterility results from physiological impairments, including failed mating and inability to complete sperm transfer [52].

Males of Lepidoptera are more radio resistant than females. Several authors indicated that in different species of Lepidoptera, the sex ratio was biased toward the males [15, 108-111]. This difference is attributed to the gametes at the time of irradiation. Radiation is generally applied to mature pupa or newly emerged adults of Lepidoptera. Euprene sperm production is completed at the time of irradiation, and dividing cell reaches to interphase. However, the oocytes are stalled in metaphase I, and the process could not be completed up to the oviposition [112]. Thus, radiation disrupts the normal course of meiosis. The secondary harmful effect seen in the oocytes is the degradation of the cytoplasmic components. The treated oocytes have large amounts of cytoplasm than that of cytoplasm-free sperm, and this cytoplasm contains many components required for embryogenesis [52].

The higher sterility level in F1 male progeny was attributed to three factors by Tothová and Marec [113]:

  1. Despite large inherited chromosomal breaks, F1 males continue to survive, and the frequency of the chromosome breaks indicates a positive correlation depending on increasing doses. However, this correlation is not seen in F1 females. The differences result from the large number of chromosomal breaks inherited by F1, and higher radiation doses might cause increasing damage rate on sex chromosome (Z). F1 females might be affected of recessive lethal mutations, but not males.

  2. Crossing-over process during spermatogenesis

  3. Radiation-induced deleterious effects on the fertility of F1 males

Genetic sexing system was suggested to introduce lethal mutations in the wild population firstly in Bombix mori by Strunnikov [114] and subsequently developed in Mediterranean flour moth E. kuehniella by Marec [115], Marec and Mirchi [116], and Marec [117]. Almost all F1 generations consist of male progeny due to the inheritance of one of the lethal mutations from their father when BL-2 males are mated to wild-type females. Females are hemizygous with regard to sex-linked recessive mutations (sl-2 and sl-15) and die during embryogenesis. For introducing lethal mutations into the wild population, balanced BL-2 males could be released directly into nature or could be reared in laboratory conditions to generate male mutant strains [108, 118]. The combination of F1 sterility with male-only colonies would be useful for reducing rearing costs and enhancing population suppression. Despite these advantages of genetic sexing system in F1 sterility applications against lepidopteran pests, lack of suitable markers for constructing mutant strains, difficulties in sex separation under mass-rearing conditions, and constantly checking requirements of mutant strains to keep its genetic structure through genetic recombination or colony contamination are some of the significant drawbacks that still need to be overcome [52, 119].

F1 sterility can effectively be combined with other control tactics, such as pheromone disruption [120-123], host plant resistance [122], and natural enemies [123]. The production of sterile F1 larvae should be considered as an opportunity for producing natural enemies and sterile moths in field conditions [124]. This would be an additional advantage ensured from this method. The extra eggs of sterile population will constitute additional host material for the egg parasitoids [111, 125]. These sterile eggs do not affect parasitoid preference adversely [126], and this tactic could also be a suitable way for combining SIT and augmentative release.

The benefits of the radiation-induced F1 sterility can be summarized as follows.

  • Reduced egg hatch and highly sterile and predominant F1 male progeny

  • Lower doses are adequate to induce F1 sterility and hence to increase the quality and competitiveness of the released insects [15]

  • Dispersal ability improvement following release [120]

  • Increase in mating competitiveness [127]

  • Improved sperm competitiveness [127]

  • Sterile F1 progeny production in the field

  • Supplementing extra host material for the egg parasitoids [111, 125]

  • For increasing the natural enemy population, F1 eggs, larvae, and pupae of the pest insects can also be used as host [128]

12. International database on insect disinfestation and sterilization (IDIDAS)

The International Database on Insect Disinfestation and Sterilization (IDIDAS) is a data bank collecting the radiation doses applied to important pest arthropods, which are important in terms of veterinary, medicine, and agriculture. Data collection and share about radiation doses are the main purpose of this database for disinfesting and reproducing sterile pests by comparative analysis and quality check [129]. This data bank can be accessed from the website of IDIDAS [21].

13. Conclusions and recommendations for future research

The future trends in controlling important pest population would predominantly be directed to biological control methods as SIT treatments. As an integrated part of area-wide pest management programs, the applications of SIT treatments will continue to increase and be desired by all sectors as farmers, commercial companies, and consumers. Cooperation and contributions of all stakeholders are essential to ensure effective implementation of these technologies. The development and the applicability of the proposed methods are required to be inexpensive and environmentally sensitive. For the mass rearing of biological control agents and improving their transport facilities, various studies are carried out with great efforts. In this respect, with the utility of novel and innovative methods, the cost-effective augmentation of natural enemies in field conditions will be possible. The use of modern biotechnology and molecular methods for the manipulation of many insects of agricultural importance for increasing the competitiveness of released male-only population in the field, release of insects carrying a dominant lethal, and timing of lethality will contribute to radiation-induced sterility. Thus, sterile insect populations with highly competitive and desired properties can be achieved for protective purposes.


1 - Ahmed MSH. Irradiation disinfestation and packaging of dates. Insect disinfestation of food and agricultural products by irradiation. Proceedings of the final research co-ordination meeting; 25-29 MAY 1987; Beijing. China. Vienna: IAEA;1991. p. 7-26
2 - Marcotte M: United Nations Environment programme Methyl Bromide Technical Options Committee. Food Irrad. Newslett. 1993; 17: 27- 32
3 - Brower JH, Tilton EW. The potential of irradiation as commodities. In: Proceedings of Radiation disinfestation of food an agricultural products conference; Hawaii: Institute of Tropical Agricultural and Human Research, University of Hawaii, 1983. p. 75-86
4 - Bakri A, Mehta K, Lance DR. Sterilizing insects with ionizing radiation. In: Dyck VA, Hendrichs J, Robinson AS., editors. Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. p. 233–-268.
5 - Loaharanu P, Mainuddin A. Advantages and disadvantages of the use of irradiation for food preservation. Journal of Agricultural and Environmental Ethics. 1991; 4(1):14-30.
6 - Follett PA, Wall MM. Phytosanitary irradiation for export of fresh produce: commercial adoption in Hawaii and current issues. J Radioanal Nucl Chem. 2013; 296:517-522
7 - Wikilectures, [Internet]. Available from Radiation
8 - UNSCEAR 2010. Sources and effects of ionising radiation. United Nations Scientific Committee on the effects of Atomic Radiation. UNSCEAR 2008 Report to the general assembly with scientific annexes. Volume I. United Nations, New York 2010
9 - International Atomic Energy Agency. Natural and Induced Radioactivity in Food. IAEA-TECDOC-1287. IAEA, Vienna, Austria; 2002b
10 - Bushland RC, Hopkins DE. Sterilization of screw-worm flies with X-rays and gamma rays. Journal of Economic Entomology. 1953; 46(4):648–656
11 - Lindquist AW The use of gamma radiation for the control or eradication of the screwworm Journal of Economic Entomology 1955; 48(4):467–469
12 - Baumhover AH, Graham AJ, Bitter BA, Hopkins DE, New WD, Dudley FH, Bushland RC. Screwworm control through release of sterilized flies. Journal of Economic Entomology. 1955;48(4):462–466
13 - Hooper GHS. Sterilization and competitiveness of the Mediterranean fruit fly after irradiation of pupae with fast neutrons. Journal of Economic Entomology. 1971; 64(6):1369–1372
14 - Offori ED, Czock KH. The use of ‘fast’ neutrons and gamma radiation to sterilize the tsetse fly Glossina tachinoides Westw. The International Journal of Applied Radiation and Isotopes. 1975;26 (5):257–260
15 - North DT Inherited sterility in Lepidoptera Annual Review of Entomology197520167–182
16 - Elias PS, Cohen AJ, editors. Radiation chemistry of major food components: its relevance to the assessment of the wholesomeness of irradiated foods. Amsterdam, The Netherlands: Elsevier; 1977. 220 p
17 - FAO/IAEA/WHO, Food and Agriculture Organization of the United Nations/International Atomic Energy Agency/World Health Organization. 1999. High-dose irradiation: wholesomeness of food irradiated with doses above 10 kGy. Joint FAO/IAEA/WHO Study Group, Technical Report Series 890. World Health Organization, Geneva, Switzerland
18 - International Atomic Energy Agency, Dosimetry for Food Irradiation. International Atomic Energy Agency. Technical Reports Series Number 409. IAEA, Vienna, Austria; 2002a
19 - [Internet]. Available from
20 - Hallman GJ. Ionizing radiation quarantine treatments. Anais da Sociedade Entomológica do Brasil. 1998; 27(3):313-323
21 - IDIDAS. [Internet]. 2004. Available from: [Accessed: 2015-03-08]
22 - Cavallaro R, Delrio G. Sterilization of Dacus oleae Gmel. and Ceratitis capitata Wied with gamma rays and fast neutrons. Redia. 1974; 55(3):373–392
23 - Smittle BJ. Irradiation of Anastrepha suspensa (Diptera: Tephritidae): new irradiation facility. Florida Entomologist. 1993; 76(2):224–227
24 - EBFRF. Electron Beam Food Research Facility. Institute of Food Science and Engineering, Texas A&M University [Internet]. 2004. Available from:
25 - Farrell JP, Seltzer SM, Sillverman J. Bremsstrahlung generators for radiation processing. Radiation Physics and Chemistry. 1983; 22(3-5):469–478
26 - Parker A, Mehta K. Sterile insect technique: A model for dose optimization for improved sterile insect quality. Florida Entomologist. 2007; 90(1):88-95
27 - International Organization for Standardization/American Society for Testing and Materials (ISO/ASTM). (2004a). Standard guide for dosimetry for sterile insect release programs, ISO/ASTM 51940. Annual book of ASTM standards 12.02. ASTM International, Philadelphia, PA, USA
28 - Robinson AS. Mutations and their use in insect control. Mutation Research. 2002; 511(2):113–132
29 - International Organization for Standardization/American Society for Testing and Materials (ISO/ASTM). (2004b). Standard guide for selection and calibration of dosimetry systems for radiation processing. ISO/ASTM 51261. Annual book of ASTM standards 12.02. ASTM International, Philadelphia, PA, USA
30 - International Organization for Standardization/American Society for Testing and Materials (ISO/ASTM). (2004c). Standard guide for dosimetry in radiation research on food and agricultural products. ISO/ASTM 51900. Annual book of ASTM standards 12.02. ASTM International, Philadelphia, PA, USA
31 - International Organization for Standardization/American Society for Testing and Materials (ISO/ASTM). (2004d). Standard practice for dosimetry for a self-contained dry-storage gamma-ray irradiator. ISO/ASTM 52116. Annual book of ASTM standards 12.02. ASTM International, Philadelphia, PA, USA
32 - International Atomic Energy Agency. Irradiation as a phytosanitary treatment of food and agricultural commodities: proceedings of a final research coordination meeting organized by the Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture 2002. Vienna, Austria: International Atomic Energy Agency (IAEA); 2004. 181 p
33 - Jarrett RD. (1982). Isotope radiation sources. In: Josephson, E.S., Peterson, M.S.(Eds) Preservation of Food by Ionizing Radiation. CRC Press, Boca rato´ n. pp. 137-163
34 - Tiryaki O. Inhibition of Penicilllium expansum, Botrytis cinerea, Rhizopus stolonifer, and Alternaria tenuissima, which were isolated from Ankara pears, by gamma irradiation. The Journal of Turkish Phytopathology. 1990; 19(3):133-140
35 - IAEA, International Atomic Energy Agency. 1986. Report of a Task Force Meeting on Irradiation as a Quarantine Treatment, Chiang Mai, Thailand, 17-28 February 1986. Vienna: International Atomic Energy Agency
36 - Follett PA: Generic Radiation Quarantine Treatments: The Next Steps J. Econ. Entomol. 2009; 102(4):1399-1406
37 - Hallman GJ, Levang-Brilz NM, Zettler JL, Winborne IC. Factors affecting ionizing radiation phytosanitary treatments, and implications for research and generic treatments. Journal of Economic Entomology. 2010; 103(6):1950-1963
38 - International Consultative Group on Food Irradiation (ICGFI). 1991. Irradiation as a quarantine treatment of fresh fruits and vegetables. ICGFI Document 13. International Atomic Energy Agency, Vienna, Austria
39 - Hallman GJ. Control of stored product pests by ionizing radiation. Journal of Stored Products Research. 2013; 52:36-41
40 - Follett PA, Weinert ED. Comparative radiation dose mapping of single fruit type and mixed-fruit boxes for export from Hawaii. J. Food Process. Preserv. 2009; 33:231–244
41 - Paull RE: Response of tropical horticultural commodities to insect disinfestation treatments. Hort Science. 1994; 29:988-996
42 - Food and Agricultural Organization (FAO). 2000. Phytosanitary treatments for regulated pests. ISPM #28. Food and Agricultural Organization, Rome, Italy
43 - Food and Agricultural Organization. 2010. Report of the 5th session of the Commission on Phytosanitary Measures. Food and Agricultural Organization, Rome, Italy
44 - Follett P, Armstrong JW. Revised irradiation doses to control melon fly, mediterranean fruit fly, and oriental fruit fly (Diptera: Tephritidae) and a generic dose for Tephritid Fruit Flies. Journal of Economic Entomology. 2004; 97(4):1254-1262
45 - EPA [Intrnet].2007. Available from: [Accessed: 2015-03-08]
46 - Hendrichs J, Kenmore P, Robinson AS, Vreysen MJB. Area-wide integrated pest management (AW-IPM): principles, practice and prospects. In: Vreysen MJB, Robinson AS, Hendrichs J, editors. Areawide Control of Insect Pests. from Research to Field. Dordrecht, The Netherlands: Springer; 2007. p. 3–33
47 - Pimentel D. Area-wide pest management: environmental, economic and food issues. In: Vreysen MJB, Robinson AS, Hendrichs J, editors. Area-Wide Control of Insect Pests. from Research to Field Implementation. Dordrecht, The Netherlands: Springer; 2007. p. 35–47
48 - Carpenter JE. Area-wide integration of lepidopteran F1 sterility and augmentative biological control. In: Area-wide control of fruit flies and other insect pests. In: Tan KH, editor. Proceedings International Conference on AreaWide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance; 28 May-5 June 1998; Penang, Malaysia. Pulau Pinang, Malaysia: Penerbit Universiti Sains; 2000. p. 193–200
49 - Dyck VA, Hendrichs J, Robinson AS, editors. Sterile Insect Technique. In: Principles And Practice In Area Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. 723 p
50 - Schuster DJ, Stansly PA. Biorational insecticides for integrated pest management in tomatoes. Crop Protection. 2005; 64:88-92. DOI: doi:10.1016/j.cropro.2014.06.011
51 - Bloem KA, Bloem S, Carpenter JE. Impact of moth suppression/eradication programmes using the sterile insect technique or inherited sterility. In: Dyck VA, Hendrichs J, Robinson AS, editors. Sterile Insect Technique. Principles And Practice In Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. p. 677–700
52 - Carpenter JE, Bloem S, Marec F. Inherited sterility in insects. In: Sterile Insect Technique. Principles And Practice In Area-Wide Integrated Pest Management. Dyck VA, Hendrichs J, Robinson AS ed. Dordrecht, The Netherlands: Springer; 2005. p. 115–146
53 - Simmons GS, Suckling DM, Carpenter JE, Addison MF, Dyck VA, Vreysen MJB. Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests. Journal of Applied Entomology. 2010; 134(3):261–273. DOI: DOI: 10.1111/j.1439-0418.2009.01438.x
54 - Serebrovsky AS. On the possibility of a new method for the control of insect pests.. Zoologichesky Zhurnal. 1940; 19:618-630
55 - Gong P, Epton M, Fu G, Scaife S, Hiscox A, Condon K, Condon G, Morrison N, Kelly D, Dafa’alla T, Coleman P, Alphey L. A dominant lethal genetic system for autocidal control of the Mediterranean fruitfly. Nature Biotechnology. 2005; 23(4):453-456
56 - Alphey L. Engineering insects for the sterile insect technique. In: Vreysen, M., editors. Area-Wide Control of Insect Pests: from Research to Field Implementation.. Dordrecht, The Netherlands: Springer; 2007. p. 51–60
57 - Wyss JH. 2000. Screw-worm eradication in the Americas — overview, pp. 79–86. In K. H. Tan (ed.), Proceedings: Area-Wide Control of Fruit Flies and Other Insect Pests. International Conference on Area-Wide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia. Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia
58 - Bushland RC, Hopkins DE. Experiments with screwworm flies sterilized by X-rays. Journal of Economic Entomology. 1951; 44(5):725–731
59 - Alphey L, Benedict M, Bellini R, Clark GG, Dame DA, Service MV, Dobson SL. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector-Borne and Zoonotic Diseases. 2010; 10(3):295-311
60 - Franz G. Genetic sexing strains in Mediterranean Fruit Fly, an example for other species amenable to large-scale rearing for the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS, editors. Sterile Insect Technique: Principles And Practice In Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. p. 427-449
61 - Koyama J, Teruya T, Tanaka K: Eradication of the oriental fruit fly (Diptera: Tephritidae) from the Okinawa Islands by a male annihilation method. Journal of Economic Entomology. 1984; 77:468-472
62 - Knipling EF: Sterile-male method of population control. Science. 1959; 130:902-904
63 - McInnis DO, Tam S, Grace C, Miyashita D: Population suppression and sterility rates induced by variable sex ratio, sterile insect releases of Ceratitis capitata (Diptera: Tephritidae). Annals of the Entomological Society of America. 1994; 87:231-240
64 - Rendón P, McInnis D, Lance D, Stewart J. 2000. Comparison of medfly male-only and bisexual releases in large scale field trials, pp. 517–525. In K. H. Tan (ed.), Proceedings: Area-Wide Control of Fruit Flies and Other Insect Pests. International Conference on Area-Wide Control of Insect Pests, and the 5th International Symposium on Fruit Flies of Economic Importance, 28 May–5 June 1998, Penang, Malaysia. Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia
65 - Rendón P, McInnis D, Lance D, Stewart J. Medfly (Diptera: Tephritidae) genetic sexing: large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. Journal of Economic Entomology. 2004; 97: 1547–1553
66 - Epsky ND, Hendrichs J, Katsoyannos BI, Vasquez LA, Ros JP, Zumreoglu A, Pereira R, Bakri A, Seewooruthun SI, Heath RR: Field evaluation of female targeted trapping systems for Ceratitis capitata (Diptera: Tephritidae) in seven countries. Journal of Economic Entomology. 1999; 92:156–164
67 - Lance DR, McInnis DO. Biological Basis of the Sterile Insect Technique. In: Dyck VA, Hendrichs J, Robinson AS, editors. Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. p. 69-85
68 - Müller P, and Nagel P: Tsetse fly eradication on Zanzibar Island; environmental surveys. End of Mission Report, URT/5/016-07-01. International Atomic Energy Agency, Vienna, Austria. 1994. Institut für Biogeographie, Universität des Saarlandes, Saarbrücken, Germany
69 - Hendrichs J. The sterile insect technique world wide. In: Proceedings of Seminar, Madeira Med: Sterile Insect Technique as an Environmentally Friendly and Effective Insect Control System. Região Autónoma da Madeira and European Union; 12-13 November 1999; Funchal, Madeira. Madeira Regional Direction of Agriculture, Portugal; 2001. p. 25-53
70 - Bartlett, AC.. Insect sterility, insect genetics, and insect control. In: D. Pimentel, editor. CRC Handbook of Pest Management in Agriculture, Vol. II. Boca Raton, FL: CRC Press; 1990. p. 279-287
71 - Knipling EF. Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology. 1955; 48:459–462
72 - Krafsur ES. Sterile insect technique for suppressing and eradicating insect population: 55 years and counting. Journal of Agricultural Entomology. 1998; 15(4):303–317
73 - Klassen W, Curtis CF. History of the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS, editors. Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. p. 3–36
74 - Alphey L, Baker P, Burton RS, Condon GC, Condon KC, Dafa’alla TH, Epton MJ, Fu G, Gong P, Jin L, Labbé G, Morrison NI, Nimmo DD, O’Connell S, Phillips CE, Plackett A, Scaife S, Woods A.. Genetic technologies to enhance the Sterile Insect Technique (SIT). In: Proceedings of the 7th International Symposium on Fruit Flies of Economic Importance; 10-15 September 2006; Salvador, Brazil. p. 319-326
75 - Morrison NI, Franz G, Koukidou M, Miller TA, Saccone G, Alphey LS, Beech CJ, Nagaraju J, Simmons GS, Polito LC. Genetic improvements to the sterile insect technique for agricultural pests. Asia-Pacific Journal of Molecular Biology and Biotechnology. 2010; 18(2):275-295
76 - Thomas DD, Donnelly CA, Wood RJ, Alphey LS. Insect population control using a dominant, repressible, lethal genetic system. Science. 2000; 287(5462):2474–2476. DOI: DOI: 10.1126/science.287.5462.2474
77 - Alphey L, Nimmo D, O’Connell S, Alphey N.. Insect population suppression using engineered insects.. In: Aksoy S., editor. Transgenesis and the Management of Vector-Borne Disease. Austin, Texas: Landes Bioscience; 2007a
78 - Fu G, Condon KC, Epton MJ, Gong P, Jin L, Condon GC, Morrison NI, Dafa’Alla TH, Alphey L. Female-specific insect lethality engineered using alter- native splicing. Nature Biotechnology. 2007; 25(3):353–357
79 - Fryxell KJ, Miller TA. Autocidal biological control: a general strategy for insect control based on genetic transformation with a highly conserved gene. Journal of Economic Entomology. 1995; 88(5):1221–1232
80 - Swartz M, Eberhart J, Mastick GS, Krull CE: Sparking new frontiers: using in vivo electroporation for genetic manipulations. Dev Biol. 2001; 233, 13-21
81 - Asokan R: Genetic engineering of insects. Resonance. 2007; 21: 47-56
82 - Handler AM, Harrel RA. Germline transformation of Drosophila melanogaster with the piggybac transposon vector. Insect Molecular Biology. 1999; 8(4):449-457
83 - Handler AM, Harrel RA. Transformation of the Caribbean fruit fly, Anastrepha suspensa, with a piggybac vector marked with polyubiquitin-regulated GFP. Insect Biochemistry and Molecular Biology. 2001; 31(2):199-205
84 - Horn C, Jaunich B, Wimmer EA. Highly sensitive, fluorescent transformation marker for Drosophila transgenesis. Development Genes and Evolution. 2000; 210(12):623-629
85 - Horn C, Schmid BGM, Pogoda FS, Wimmer EA. Fluorescent transformation markers for insect transgenesis. Insect Biochemistry and Molecular Biology. 2002; 32(10):1221-1235
86 - O’Brochta DA, Atkinson PW: Building the better bug. Sci Am.1998; 279:90-95
87 - Schetelig MF, Wimmer EA. Insect transgenesis and the sterile insect technique. In: Vilcinskas A, editor. Insect Biotechnology, Biologically-Inspired Systems 2. Springer Science+Business Media B.V; 2011. p. 169-194. DOI: DOI 10.1007/978-90-481-9641-8
88 - Pane A, Salvemini M, Bovi PD, Polito LC, Saccone G. The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development. 2002; 129(15):3715-3725
89 - Saccone G, Pane A, De Simone A, Salvemini M, Milano A. New sexing strains for Mediterranean fruit fly Ceratitis capitata: transforming females into males. In: Vreysen MJB, Robinson AS, Hendrichs J, editors. Area-wide Control of Insect Pests. From Research to Field Implementation. Dordrecht, The Netherlands: Springer; 2007. p. 95-102
90 - LaChance LE. (1985). Genetic Methods fort he control of lepidopteran species: status and potential, ARS-28. USDA, Washington, DC, USA
91 - LaChance LE, Graham CK. Insect radiosensitivity: dose curves and dose-fractionation studies of dominant lethal mutations in the mature sperm of 4 insect species. Mutation Research. 1984; 127(1):49–59
92 - Knipling EF. The Basic Principles of Insect Population Suppression and Management. Washington, D. C: U.S. Dept. of Agriculture; 1979. 659 p
93 - Bartlett AC, Staten RT.. The sterile insect release method and other genetic control strategies. [Internet]. 1996. Available from:
94 - Astaurov BI, Frolova SL.. Artificial mutations in the silkworm (Bombyx mori L.). V.Sterility and spermatogenic anomalies in the progeny of irradiated moths concerning some questions of general biological and mutagenic action of X-rays. Biologicheskii Zhurnal. 1935; 4:861–894
95 - Proverbs, M. D. Some effects of gamma radiation on the reproductive potential of the codling moth, Carpocapsa pomonella (L.) (Lepidoptera: Olethreutidae). Canadian Entomologist 1962; 94:1162–1170
96 - Genchev NP, Gencheva EM. Inheritance of radiation induced sterility in males of the oriental fruit moth, Grapholitha Molesta Busck., (Lepidoptera: Tortricidae). Bulgarian Journal of Agricultural Science. 2006; 12:489-499
97 - Knipling EF: Suppression of pest Lepidoptera by releasing partially sterile males: a theoretical appraisal. BioScience. 1970; 20:456-4
98 - Suckling DM, Stringer LD, Mitchell VJ, Sullivan TES, Barrington AM, El-Sayed AM: Comparative Ştness of irradiated sterile light brown apple moths (Lepidoptera: Tortricidae) in a wind tunnel, hedgerow and vineyard. J. Econ. Entomol. 2011; 104: 1301-1308
99 - Makee H, Saour G. Efficiency of inherited sterility technique against Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae) as affected by irradiation of females. Journal of Vegetable Crop Production. 2004; 10(1):11–22
100 - Tate CD, Carpenter JE, Bloem S. Influence of radiation dose on the level of F1 sterility in the cactus moth, Cactoblastis cactorum (Lepidoptera: Pyralidae).. Florida Entomologist. 2007; 90(3):537–544. DOI:[537:IORDOT]2.0.CO;2
101 - Soopaya R, Stringer LD, Woods B, Stephens AEA, Butler RC, Lacey I, Kaur A, Suckling DM. Radiation biology and inherited sterility of light brown apple moth (Lepidoptera: Tortricidae): developing a sterile insect release program. Journal of Economic Entomology. 2011; 104(6):1999–2008. DOI:
102 - Jang EB, McInnis DO, Kurashima R, Woods B, Suckling DM. Irradiation of adult Epiphyas postvittana (Lepidoptera: Tortricidae): egg sterility in parental and F1 generations. Journal of Economic Entomology. 2012; 105(1):54–61
103 - LaChance LE, Schmidt CH, Bushland RC. Radiation induced sterilization. In: Kilgore WW, Doutt RL, editors. Pest Control: Biological, Physical and Selected Chemical Methods. New York, NY, USA: New York Academic Press; 1967. p. 147–196
104 - LaChance LE. The induction of dominant lethal mutations in insects by ionizing radiation and chemicals - as related to the sterile-male technique of insect control. In: Wright JW, Pal R, editors. Genetics of Insect Vectors of Disease. Amsterdam, The Netherlands: Elsevier; 1967. p. 617–650
105 - LaChance LE. Dominant lethal mutations in insects with holokinetic chromosomes. 2. irradiation of sperm of cabbage looper. Annals of the Entomological Society of America. 1974; 67(1):35-39
106 - Carpenter JE, Layton RC. Computer model for predicting the effect of inheritedsterility on population growth. In: Proceedings: Radiation Induced F1 Sterility in Lepidoptera for Area-Wide Control. Final Research Co-ordination Meeting, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture; 9–13 September 1991; Phoenix, AZ, USA. Vienna, Austria: IAEA; 1993. p. 49–55
107 - Seth RK, Reynolds SE: Induction of inherited sterility in the tobacco hornworm Manduca sexta (Lepidoptera: Sphingidae) by substerilizing doses of ionizing radiation. Bulletin of Entomological Research. 1993; 83:227-235
108 - Marec F, Kollárová I, Pavelka J. Radiation induced inherited sterility combined with a genetic sexing system in Ephestia kuehniella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America. 1999; 92(2):250–259
109 - Seth RK, Sharma VP. Inherited sterility by substerilizing radiation in Spodoptera litura (Lepidoptera: Noctuidae): bio-efficacy and potential for pest suppression. Florida Entomologist. 2001; 84(2):183–193
110 - Brower JH. Reproductive performance of inbred or outbred F1 and F2 progeny of Indian meal moth females or males x females partially sterilized by gamma radiation. Annals of the Entomological Society of America. 1981; 74(1):108–113
111 - Ayvaz A, Albayrak S, Tuncbilek AS.. Inherited sterility in Mediterranean flour moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae): Effect of gamma radiation doses on insect fecundity fertility and developmental period. Journal of Stored Product Research. 2007; 43:234–239
112 - Traut W. A study of recombination, formation of chiasmata and synaptonemal complexes in female and male meiosis of Ephestia kuehniella (Lepidoptera). Genetica. 1977; 47(2):135–142
113 - Tothová A, Marec F: Chromosomal principle of radiation-induced F1 sterility in Ephestia kuehniella (Lepidoptera: Pyralidae). Genome. 2001; 44:172-184
114 - Strunnikov VA: Sex control in silkworms. Nature (Lond.). 1975; 255:111-113
115 - Marec F: Genetic control of pest Lepidoptera: induction of sex-linked recessive lethal mutations in Ephestia kuehniella (Pyralidae). Acta Entomologica Bohemoslovaca. 1990; 87:445-458
116 - Marec F, Mirchi R: Genetic control of the pest Lepidoptera: gamma-ray induction of translocations between sex chromosomes of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Journal of Stored Products Research. 1990; 26:109-116
117 - Marec F. Genetic control of pest Lepidoptera: construction of a balanced lethal strain in Ephestia kuehniella. Entomologia Experimentalis et Applicata. 1991; 61(3):271–283
118 - Marec F: Synaptonemal complexes in insects. International Journal of Insect Morphology and Embryology. 1996; 25:205-233
119 - Marec F. Genetic control of pest Lepidoptera: construction of a balanced lethal strain in Ephestia kuehniella. Entomologia Experimentalis et Applicata. 1991; 61(3):271–283
120 - Bloem S, Carpenter JE. Evaluation of population suppression by irradiated pidoptera and their progeny. Florida Entomologist. 2001; 84(2):165–171
121 - Hamm JJ, Carpenter JE. Compatibility of nuclear polyhedrosis viruses and inherited sterility for control of corn earworm and fall armyworm (Lepidoptera: Noctuidae). Journal of Entomological Science. 1997; 32(2):48–53
122 - Carpenter JE, Wiseman BR. Spodoptera frugiperda (Lepidoptera: Noctuidae) development and damage potential as affected by inherited sterility and host plant resistance. Environmental Entomology. 1992; 21(1):57-60
123 - Carpenter JE, Young JR, Sparks AN. Fall armyworm (Lepidoptera: Noctuidae): comparison of inherited deleterious effects in progeny from irradiated males and females. Journal of Economic Entomology. 1986; 79(1):47–49
124 - Carpenter JE, Bloem S, Marec F. Inherited sterility in insects. In: Sterile Insect Technique. Principles And Practice In Area-Wide Integrated Pest Management. Dyck VA, Hendrichs J, Robinson AS ed. Dordrecht, The Netherlands: Springer; 2005. p. 115–146
125 - Bloem S, Carpenter JE, Hofmeyr JH. Radiation biology and inherited sterility in false codling moth (Lepidoptera: Tortricidae). Journal of Economic Entomology. 2003; 96(6):1724– 1731
126 - Ayvaz A, Karasu E, Karabörklü S, Tunçbilek AS.. Effects of cold storage, rearing temperature, parasitoid age and irradiation on the performance of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Journal of Stored Products Research. 2008; 44:232-240
127 - Carpenter JE, Sparks AN, HL Cromroy: Corn earworm (Lepidoptera. Noctuidae): influence of irradiation and mating history on the mating propensity of females. J. Econ. Entomol. 1987; 80:1233-1237
128 - Proshold FI, Gross HR, Carpenter JE. Inundative release of Archytas marmoratus (Diptera: Tachinidae) against the corn earworm and fall armyworm (Lepidoptera: Noctuidae) in whorl-stage corn. Journal of Entomological Science. 1998; 33:241–255
129 - Bakri A, Mehta K, Lance DR.. Sterilizing Insects With Ionizing Radiation. In: Dyck VA, Hendrichs J, Robinson AS., editors. Sterile Insect Technique: Principles And Practice In Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer; 2005. p. 233-268