Assessing the synergy between the Sterile Insect Technique and Classical Biological Control for sustainable management of the invasive pest Bagrada hilaris (Hemiptera: Pentatomidae)

The phenomenon of biological invasions is largely represented by phytophagous insect pests, which are responsible for global economic losses of at least $70 billion annually. The protagonist of this study, Bagrada hilaris (Burmeister) (Hemiptera: Pentatomidae), in addition to being a pest of cruciferous plants in areas where it is autochthonous, has been recorded as a polyphagous alien species harmful to 74 agricultural relevant crops worldwide. It has not yet been detected in continental Europe but is known to be present on the islands of Malta and Pantelleria (Italy). Common practices for its control involve the use of synthetic pesticides, but they are economically and environmentally unsustainable. Moreover, the prolonged use of chemical insecticides causes the emergence of pest resistance to such active substances, raising the urgent need to shift to targeted and more effective control techniques. The aim of this research was to investigate the potential application of the sterile insect technique (SIT) and to evaluate the synergistic relationships that may emerge from its combination with classical biological control. Sterilization of the male individuals was achieved by exposure to γ-rays emitted from a cobalt-60 source at the Calliope Irradiation Facility of ENEA (Rome, Italy). To identify the irradiation dose that ensures a good balance between sterility, longevity, and the ability to mate and compete with their wild counterparts, the parameters inherent in the intraspecific communication and sexual behavior of treated individuals were investigated. From analyses of substrate-borne vibrational signals of irradiated males, it was found that the 100 Gy dose debilitates the insects' ability to emit vibrations of frequency comparable to that of the control and to exhibit courtship effective for successful mating. In contrast, vibrational communication and mating were unaffected in the males irradiated with 60 Gy. These results were confirmed by observational bioassays on the duration and frequency of mating under the conditions of choice, which suggest that the 80 Gy dose ensures a good level of sterility (7.4 % fecundity of females mated with treated males) and a sexual performance comparable to that exhibited by untreated individuals. In the same study, it was also highlighted that foraging damage is mainly caused by B. hilaris females, mitigating the risk of side effects through the release of sterile males into the environment. The SIT technique is associated with the use of natural enemies in integrated pest management programs to maximize the chances of suppression or eradication of the target species. The candidate biocontrol agent, represented by the oophagous parasitoid Gryon aetherium (Talamas) (Hymenoptera: Scelionidae), was exposed to eggs produced by females mated with males irradiated with 80 Gy (SIT eggs) to test the suitability of this oviposition substrate. The outcomes suggest that G. aetherium can exploit SIT eggs to generate fertile offspring with longevity comparable to that of the controls. Moreover, favorable conditions for reproduction offered by such substrates are maintained for up to 15 days, promoting the use of SIT eggs as long-lasting sentinel eggs for monitoring and eventual detection of oophagous parasitoids already present in invaded areas. The identification of the optimal irradiation dose and confirmation of the favorable association with the use of biocontrol agents provides encouraging information for the feasibility of experiments under semi-field conditions. This proposal is supported by the context of the Italian island of Pantelleria, where the pest is confined to a limited area in the southeast of the island, providing ideal prerequisites for the development of an Area-Wide IPM.