Potential for controlling codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) in Argentina using the sterile insect technique and egg parasitoids

Codling moth is the main pest affecting apples and pears worldwide. Most pest control strategies used against this insect have relied on the use of broad‐spectrum insecticides which have led to non‐desirable effects like pesticide resistance, residues in the environment, human health concerns and the reduction of access to international markets. Therefore, alternative pest control strategies that would result in sustainable fruit production systems while taking care of the environment are strongly promoted. The use of the sterile insect technique has proven to be a valuable pest control tactic within area‐wide integrated pest management strategies, and its synergistic effect for Lepidoptera pests when combined with other biological control tactics such as parasitoids has been documented. The purposes of this research were to evaluate the response of an Argentinean codling moth strain to a sub‐sterilizing radiation dose of 100 Gy and to assess the acceptability and suitability of sterile codling moth eggs by the egg parasitoids, Trichogramma cacoeciae (Marchal) and Trichogramma nerudai (Pintureau and Gerding). Irradiated female moths survived better than irradiated male moths and non‐irradiated male and female moths. Also, the fecundity of irradiated female moths was reduced by more than 30% as compared to non‐irradiated ones whereas their fertility was close to zero. The F₁ generation was male biased with a lower fertility (inherited sterility) than the parental generation. Trichogramma cacoeciae and T. nerudai parasitized both fertile and sterile eggs. However, there was a significant reduction in acceptability for sterile eggs. Trichogramma nerudai parasitized more eggs than T. cacoeciae, but egg acceptability for this species was proportionally lower than for T. cacoeciae especially on eggs oviposited by irradiated females. Development to adult of both parasitoids species was not substantially affected by the origin of the eggs and the wasps had acceptable levels of adult emergence, survival and fecundity. These results provided useful information on the potential for controlling the codling moth using egg parasitoids and the sterile insect technique in Argentina.     

Cold treatment enhances low‐temperature flight performance in false codling moth,Thaumatotibia leucotreta (Lepidoptera: Tortricidae)

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Impact of mass rearing and gamma irradiation on thermal tolerance of Eldana saccharina

Mating ability, survival, and fitness of mass‐produced sterile insects when released into the wild, are critical to the success of the sterile insect technique (SIT) as a pest management strategy, but their field performance remains one of the greatest challenges. Thermal stress tolerance by irradiated insects is a determinant of sterile insect quality, hence knowledge of their physiological competitiveness is essential for developing the SIT. Here, we report the results of experiments investigating effects of laboratory rearing and increasing radiation dosage on thermal limits to activity of the adult stage of Eldana saccharina Walker (Lepidoptera: Pyralidae). The critical thermal maximum (CTmax) and critical thermal minimum (CTmin) were assayed using a dynamic method on both sexes of E. saccharina moths in laboratory vs. wild populations (to determine effect of rearing history). Furthermore, the laboratory population was exposed to 150, 200, and 250 Gy, to determine the effect of radiation dose. Laboratory‐reared E. saccharina were more heat tolerant compared to wild moths for both sexes (CTmax = 44.5 vs. 44.3 °C), whereas in the case of CTmin (3.7 vs. 4.4 °C), wild moths were more cold tolerant than their laboratory‐reared counterparts. Irradiation had a negative effect on both CTmax and CTmin. Moths treated at the lowest radiation dose were more cold and heat tolerant than those treated at the highest dosages (CTmin = 4.5 vs. 6.2 °C; CTmax = 43.9 vs. 43.5 °C), thereby reinforcing the importance of lower dosages rather than those that induce full sterility against E. saccharina. In general, sex had no influence on critical thermal limits in all moth treatments except for those irradiated at 150 Gy. The data presented in this article provide evidence that increasing radiation dose impacts on fitness of laboratory‐produced moths relative to their wild counterparts, which in turn could affect the effectiveness of the SIT programme.     

Thaumatotibia leucotreta and the Navel orange: ovipositional preferences and host susceptibility

False codling moth, Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae), presents a significant threat to the South African citrus industry. To limit income loss due to direct larval damage or from fruit rejection due to the phytosanitary status of this pest, additional pre‐harvest control techniques are required for Navel oranges, which are known to be susceptible to T. leucotreta damage. A number of Navel orange cultivars have been developed, and differences in female T. leucotreta ovipositional preference and susceptibility of cultivars to larval penetration are known to exist. Navel orange cultivars were grouped according to time of maturity (early, mid‐ and late season). Female T. leucotreta were subjected to choice and no‐choice tests with these cultivars, measured by oviposition. Host susceptibility was tested by allowing neonate T. leucotreta larvae to penetrate the different Navel cultivars. In the early maturing group, Fischer Navels were least preferred for oviposition and the least susceptible to larval penetration. The mid‐ and late season maturing groupings showed limited differences in oviposition preference, although host susceptibility did appear to be an important factor in assessing the vulnerability of fruit to T. leucotreta. Despite being widely planted in South Africa, the mid‐season Palmer Navels were highly susceptible to larval penetration, while for the late season cultivars, Cambria and Glen Ora Late were the least susceptible to T. leucotreta. As a result of these laboratory trials, it is recommended that farmers increase cultivation of Fischer Navels as the principal early season cultivar, avoid Palmer Navels in favour of other mid‐season maturing cultivars and give preference to the late maturing Cambria and Glen Ora Late cultivars, to limit T. leucotreta damage.     

Modelling the effects of inherited sterility for the application of the sterile insect technique

1 The sterile insect technique (SIT) involves the release of large numbers of sterile or partially‐sterile insects into a wild pest population to dilute the number of successful wild matings, with the eventual aim of eradication or area‐wide suppression. General population models, encompassing a wide range of SIT types, were used to derive principles for optimizing the success of SIT, with particular emphasis on the application of partial sterility leading to inherited sterility in the F₁ population. 2 The models show that inherited sterility can only be guaranteed to be more effective than complete sterility if matings between irradiated‐lineage partners are unsuccessful. This is widely assumed but rarely examined experimentally. 3 The models allow the critical overflooding ratio, φ_c, to be calculated for a particular target species, suggesting the release rate required to prevent population increase. Successful eradication using SIT alone should aim for a substantially higher release rate than suggested by φ_c. 4 The models show that pest populations may continue to increase in the first few generations of SIT releases, regardless of release rate, as irradiated‐lineage individuals infiltrate the population. This does not necessarily imply that the SIT programme will be unsuccessful in the longer term. 5For pests with overlapping generations, the models suggest that frequent small releases may be more effective than less frequent large releases, particularly when the average release rate is close to the critical threshold for success.     

Seasonal variation of the capture and field distribution of sterile Anastrepha ludens in Tamaulipas,Mexico

Anastrepha ludens (Loew) (Diptera: Tephritidae) is one of the most important citrus pest in Mexico. The sterile insect technique (SIT) is used against pest populations of fruit flies for suppression, eradication, containment and prevention to reduce damages in fruit‐growing areas. In this study, we analyzed the seasonal variation of captures and field distribution of sterile A. ludens released in different seasons of the year in north‐eastern Mexico. Chilled releases were conducted by air at constant densities per ha on a citrus area for a period of 32 weeks that included the coldest and warmest seasons that is winter, spring and summer. Multilure traps baited with torula yeast pellets were used to capture sterile flies. Fly capture data were compared over the three seasons and correlated with climate. The lowest number of captures of the sterile insect occurred in the summer and the highest in winter and spring. High and low temperatures were negatively correlated with fly captures. Field distribution was also negatively correlated with high temperatures in summer, but no relationships were observed in winter and spring. No relationships were observed between rainfall with capture and field distribution of sterile flies. These results indicate that summer is a season involving agro‐ecological and environmental constraints for the capture and field distribution of sterile flies. This study may be useful for enhancing release strategies and optimizing economic resources in north‐eastern Mexico. Further research on the behaviour of sterile flies under stressful environments is suggested.     

Attractiveness and competitiveness of irradiated light brown apple moths

The sterile insect technique (SIT) potentially provides a socially acceptable approach for insect eradication of new pest incursions. The light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), was discovered in Berkeley (CA, USA) in 2006, leading to an incursion response that included this technology. In this study, we assessed factors affecting mating success from a bisex release of irradiated moths: effects of radiation dose on male multiple mating, male flight competition, female sex pheromone titre and attractiveness of irradiated females to males, and identification of successful mating in vineyards of either irradiated or wild males (identified by isotope analysis of spermatophores from sentinel females). There was a significant negative relationship between male radiation dose and mating frequency. In head‐to‐head flights of irradiated males against non‐irradiated males to a pheromone lure in a wind tunnel, irradiated males reached the lure first only 31% of the time. With increasing radiation dose, the production of the major sex pheromone component in females, (E)‐11‐tetradecenyl acetate, dropped, from 0.7 ± 0.1 ng per female in non‐irradiated females to 0.2 ± 0.07 ng per female when irradiated at 300 Gy. Male catch was reduced to 11% of control females in traps containing females irradiated at 300 Gy. Isotope analysis of spermatophores found in the bursa copulatrix of females indicated that mating success of irradiated males inside the live (entry‐only) traps containing virgin females was lower (13.1 ± 3.3%) than suggested by male catch (21.2 ± 3.8%) in pheromone traps, the current standard for assessing field competitiveness. Impacts of irradiation on male and female moth fitness should be taken into account to improve estimates of irradiated to wild male E. postvittana overflooding ratios needed for population suppression.     

A flight cylinder bioassay as a simple,effective quality control test for Cydia pomonella

Assessment of quality of the sterile male insects that are being mass‐reared for release in area‐wide integrated pest management programmes that include a sterile insect technique component is crucial for the success of these programmes. Routine monitoring of sterile male quality needs to be carried out both in the mass‐rearing facility and in the field. Simple bioassays that can be conducted in the laboratory and that would be surrogates for laborious field tests would be a very cost‐effective way of monitoring sterile male field performance. Simple flight cylinders were used to assess whether these could detect differences in quality of male codling moth Cydia pomonella. The number of male and female codling moths that flew out of the cylinders was influenced by cylinder diameter, cylinder height and number of hours following the initiation of the test. The flight cylinder bioassay was capable of detecting differences in quality of codling moths induced by irradiation when moths were shipped, but no differences were found in flight ability when the moths were not transported. The tests also confirmed that handling and shipment reduced quality more for irradiated than for non‐treated codling moth, and that insect quality was significantly influenced by larval rearing protocols. The flight cylinder bioassay was therefore successful in detecting differences in codling moth quality induced by various treatments that had been identified previously by more complex laboratory bioassays and field trials. Treatment differences were most likely detected when flight cylinders were 16 cm high.     

The role of abiotic factors in the pupation of Thaumatotibia leucotreta Meyrick (Lepidoptera: Tortricidae) in the soil

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The effects of farming system,habitat type and bait type on the isolation of entomopathogenic fungi from citrus soils in the Eastern Cape Province,South Africa

A survey of occurrence of entomopathogenic fungi was undertaken on soils from citrus orchards and refugia on conventionally and organically managed farms in the Eastern Cape Province in South Africa. An adapted method for baiting soil samples with key citrus pest Thaumatotibia leucotreta (Meyrick; Lepidoptera: Tortricidae) and Ceratitis capitata (Wiedemann; Diptera: Tephritidae) larvae, as well as with the standard bait insect, Galleria mellonella (Linnaeus; Lepidoptera: Pyralidae), was implemented. Sixty-two potentially useful entomopathogenic fungal isolates belonging to four genera were collected from 288 soil samples, an occurrence frequency of 21.53%. The most frequently isolated entomopathogenic fungal species was Beauveria bassiana (Balsamo) Vuillemin (15.63%), followed by Metarhizium anisopliae var. anisopliae (Metschnikoff) Sorokin (3.82%). Galleria mellonella was the most effective bait insect used to isolate fungal species (χ ² = 40.13, df = 2, P ≤ 0.005), with a total of 45 isolates obtained, followed by C. capitata with 11 isolates, and T. leucotreta with six isolates recovered. There was a significantly (χ ² = 11.65, df = 1, P ≤ 0.005) higher occurrence of entomopathogenic fungi in soil samples taken from refugia compared to cultivated orchards of both organically and conventionally managed farms. No significant differences were observed in the recovery of fungal isolates when soil samples from both farming systems were compared.     

Simultaneous use of SIT plus disseminator devices of Beauveria bassiana enhances horizontal transmission in Anastrepha ludens

Beauveria bassiana is an entomopathogenic fungus widely used to control different insect pests including Anastrepha ludens (Diptera: Tephritidae), a key pest of citrus and mangoes. Currently, to control this pest, sterile A. ludens males of the Tap-7 genetic sexing strain are released weekly by aircraft at a density of 1,000 males/ha as part of an integrated pest management programme (IPM) in Southern Mexico. Our objective here was to determine whether the sterile insect technique (SIT) could be enhanced by augmenting it with horizontal transmission of fungus conidia by using Beauveria bassiana disseminator devices (DBb) designed to distribute it with minimal impact on non-target species. Four treatments were established: DBb only, DBb + SIT, SIT only and untreated control, and fruit fly populations were monitored using two Multilure traps baited with 250 ml of CeraTrap per plot. We found that the presence of B. bassiana disseminator devices in areas where A. ludens sterile males were released resulted in higher proportions of infected wild fruit flies in the field, and that high relative humidity (rainy season) played an important role in the efficiency of horizontal conidia transmission to the wild populations. We conclude that the simultaneous use of both strategies (SIT + DBb) increases the conidia transmission to wild populations, and that this approach could be incorporated to an integrated pest management for the better suppression of fruit fly populations.     

Effects of radiation on the fertility of the Ethiopian fruit fly,Dacus ciliatus

The Ethiopian fruit fly, Dacus ciliatus (Loew) (Diptera: Tephritidae), is a significant pest of cucurbit crops in Asia and Africa and is currently controlled with insecticides. The sterilizing effect of gamma radiation on D. ciliatus adults was investigated to assess the suitability of sterile insect technique (SIT) for use as an alternative, non‐chemical strategy for the control of this pest. Late pupae (48 h before emergence) were irradiated with 60, 80, 100, 120, and 140 Gy of gamma rays emitted by a ⁶⁰Co source. Following emergence, the biological characteristics of the experimental cohorts (including all possible male‐female combinations of irradiated and untreated flies) were recorded. No significant negative effects of irradiation on pupal eclosion or the ability of newly emerged flies to fly were observed. Samples of eggs at reproductive fly‐ages (12‐, 15‐, and 17‐day‐old pairs) were collected and their hatch rates were assessed. At 60 Gy, females were completely sterilized, whereas complete sterilization of the males was observed only at 140 Gy (a small amount of fertility persisted even at 120 Gy). In addition to the above experiments, three fruit infestation trials were conducted with zucchini [Cucurbita pepo L. (Cucurbitaceae)] as the plant host and the pupae produced in those trials were collected and recorded. We observed significant (ca. 10%) infestation following treatment with up to 120 Gy and zero progeny only at 140 Gy, mirroring the egg‐hatch results. Our findings support the feasibility of SIT for the control of D. ciliatus.     

Genetics‐based methods for agricultural insect pest management

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A high‐quality chromosome‐level genome assembly of a generalist herbivore,Trichoplusia ni

The cabbage looper, Trichoplusia ni, is a globally distributed highly polyphagous herbivore and an important agricultural pest. T. ni has evolved resistance to various chemical insecticides, and is one of the only two insect species that have evolved resistance to the biopesticide Bacillus thuringiensis (Bt) in agricultural systems and has been selected for resistance to baculovirus infections. We report a 333‐Mb high‐quality T. ni genome assembly, which has N50 lengths of scaffolds and contigs of 4.6 Mb and 140 Kb, respectively, and contains 14,384 protein‐coding genes. High‐density genetic maps were constructed to anchor 305 Mb (91.7%) of the assembly to 31 chromosomes. Comparative genomic analysis of T. ni with Bombyx mori showed enrichment of tandemly duplicated genes in T. ni in families involved in detoxification and digestion, consistent with the broad host range of T. ni. High levels of genome synteny were found between T. ni and other sequenced lepidopterans. However, genome synteny analysis of T. ni and the T. ni derived cell line High Five (Hi5) indicated extensive genome rearrangements in the cell line. These results provided the first genomic evidence revealing the high instability of chromosomes in lepidopteran cell lines known from karyotypic observations. The high‐quality T. ni genome sequence provides a valuable resource for research in a broad range of areas including fundamental insect biology, insect‐plant interactions and co‐evolution, mechanisms and evolution of insect resistance to chemical and biological pesticides, and technology development for insect pest management.     

Artificial selection,pre‐release diet,and gut symbiont inoculation effects on sterile male longevity for area‐wide fruit‐fly management

Longevity is an important life‐history trait for successful and cost‐effective application of the sterile insect technique. Furthermore, it has been shown that females of some species – e.g., Anastrepha ludens (Loew) (Diptera: Tephritidae) – preferentially copulate with ‘old’, sexually experienced males, rather than younger and inexperienced males. Long‐lived sterile males may therefore have greater opportunity to find and mate with wild females than short‐lived males, and be more effective in inducing sterility into wild populations. We explored the feasibility of increasing sterile male lifespan through selection of long‐lived strains and provision of pre‐release diets with added protein, and inoculated with bacterial symbionts recovered from cultures of the gut of wild Anastrepha obliqua (Macquart). Artificial selection for long‐lived A. ludens resulted in a sharp drop of fecundity levels for F1 females. Nevertheless, the cross of long‐lived males with laboratory females produced a female F1 progeny with fecundity levels comparable to those of females in the established colony. However, the male progeny of long‐lived males*laboratory females did not survive in higher proportions than laboratory males. Provision of sugar to A. obliqua adults resulted in increased survival in comparison to adults provided only with water, whereas the addition of protein to sugar‐only diets had no additional effect on longevity. Non‐irradiated males lived longer than irradiated males, and supplying a generic probiotic diet produced no noticeable effect in restoring irradiated male longevity of A. obliqua. We discuss the need to evaluate the time to reach sexual maturity and survival under stress for long‐lived strains, and the inclusion of low amounts of protein and specific beneficial bacteria in pre‐release diets to increase sterile male performance and longevity in the field.     

Toxicity of insecticidal soaps to the Asian citrus psyllid and two of its natural enemies

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is an important pest of citrus because it transmits plant pathogens responsible for a serious disease of citrus known as huanglongbing. Conventional insecticides are frequently used to manage ACP. Insecticidal soaps (hereafter ‘soaps’) are an insect control option labelled for commercial use as well as for use by homeowners and organic growers. Soaps have been shown to be toxic to some insect pests and therefore might be an alternative to conventional pesticides for control of ACP, but the efficacy of soaps against ACP was largely unknown. Our objective was to test whether different concentrations of two insecticidal soaps, M‐Pede and Safer Insecticidal Soap Concentrate, caused mortality of ACP adults, nymphs and eggs. In addition, we tested whether these soaps were toxic to two natural enemies of ACP, adults of the lady beetle Cycloneda sanguinea (L.) (Coleoptera: Coccinellidae) and the parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae). Direct sprays of M‐Pede or Safer Insecticidal Soap were acutely toxic to ACP adults (regardless of gender) and nymphs when applied in solutions of 0.8–2% in water. Insecticidal soaps were non‐toxic to eggs at rates of up to 2%. Residues of soap were less toxic to adult ACP than direct sprays, even when applied at concentrations of up to 4%. M‐Pede or Safer soap at high concentrations (for example, 2% v/v in water) may be an effective alternative to conventional pesticides to manage adult and nymphal ACP, although multiple applications may be needed if a target population includes eggs. A 2% concentration of either soap applied as a direct spray was non‐toxic to adult C. sanguinea but acutely toxic to adult T. radiata. Soaps therefore may be compatible with biological control of ACP by adult coccinellids but not the parasitoid T. radiata.     

Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests

Lepidoptera are among the most severe pests of food and fibre crops in the world and are mainly controlled using broad spectrum insecticides. This does not lead to environmentally sustainable control and farmers are demanding alternative control tools which are both effective and friendly to the environment. The sterile insect technique (SIT), within an area‐wide integrated pest management (AW‐IPM) approach, has proven to be a powerful control tactic for the creation of pest‐free areas or areas of low pest prevalence. Improving the quality of laboratory‐reared moths would increase the efficacy of released sterile moths applied in AW‐IPM programmes that integrate the (SIT). Factors that might affect the quality and field performance of released sterile moths are identified and characterized in this study. Some tools and methods to measure, predict and enhance moth quality are described such as tests for moth quality, female moth trapping systems, ‘smart’ traps, machine vision for recording behaviour, marking techniques, and release technologies. Methods of enhancing rearing systems are discussed with a view to selecting and preserving useful genetic traits that improve field performance.     

Fractionated irradiation improves the mating performance of the West Indian sweet potato weevil Euscepes postfasciatus

• 1 The sterile insect technique (SIT) is widely used to suppress or eradicate target pest insect populations.
• 2 The effectiveness of SIT depends on the ability of released sterile males to mate with and inseminate wild females. The use of gamma radiation to induce sterility, however, negatively affects both somatic cells as well as reproductive cells. Consequently, mating performance of sterilized individuals decreases drastically over time. The mating propensity of sterilized Euscepes postfasciatus (Fairmaire) males irradiated with a single dose of 150 Gy (the current standard of the Okinawa Prefecture SIT programme) is equal to that of non‐irradiated weevils for the first 6 days.
• 3 Fractionated irradiation, in which a sterilizing dose is delivered over time in a series of smaller irradiations, reduces the damage of irradiation in insects. In the present study, we evaluated the effect of fractionated irradiation on male fertilization ability, longevity and mating propensity of E. postfasciatus for a period of 16 days after irradiation.
• 4 Although fractionated irradiation totalling 150 Gy was found to induce full sterility regardless of the number of individual doses, the mating propensity of male weevils sterilized by fractionated irradiation was maintained for the first 12 days. These results demonstrate that fractionated irradiation can be highly advantageous in programmes aimed at eradication of E. postfasciatus.

     

Mutation in the ace‐1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance

The tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae), is a major invasive pest that has spread throughout many countries in the Mediterranean basin and parts of Asia over the last decade. The control of T. absoluta has relied heavily on the use of chemical insecticides, a strategy that has led to the evolution of resistance. In this study, biological and molecular methods were used to determine the susceptibility of five strains of T. absoluta to the organophosphate chlorpyrifos and to investigate the molecular mechanisms underlying resistance to this class of insecticides. High levels of resistance to chlorpyrifos were observed in all five strains tested. Cloning and sequencing of the gene encoding the organophosphate target site, ace‐1, of T. absoluta revealed the presence of an alanine to serine substitution at a position that has been previously linked with organophosphate resistance across a range of different insect and mite species. The presence of this mutation at high frequency in T. absoluta populations originating from various countries further supports the suggestion that the rapid expansion of this species is, in part, mediated by the resistance of this pest to chemical insecticides.