Benefits of remating of a hyperparasitoid acting as a biocontrol agent

Abstract

Encarsia sophia is the dominant parasitoid of invasive whitefly pest such as Bemisia tabaci. This heteronomous hyperparasitoid species lays fertilised diploid eggs in whitefly nymphs, which serve as primary hosts. Larvae develop as female progeny by consuming whitefly hosts, providing direct biocontrol benefits. However, male progeny originate from unfertilised eggs laid on secondary hosts (primary parasitoids within whitefly nymphs) and develop by consuming primary parasitoid larvae rather than whitefly hosts. Therefore, it is crucial for indoor rearing and field release of the hyperparasitoid to determine whether a female with single-mating experience can parasitise primary hosts and produce female progeny for a whole lifetime and, if not, whether it is remating events and prolong the period of female production, thereby increasing the amount of parasitism on whiteflies. Our fecundity experiments of females with single-mating experience, equally provided with primary and secondary hosts, showed that single mating was insufficient for E. sophia females to lay fertilised eggs in whitefly nymphs for their whole lifetime. In multiple mating experiments, 76.7 % of male adults completed their second mating 2 h after the first, whereas female adults accepted the second mating only if primary hosts were available thereafter. Remating was beneficial for female adults as it prolonged the ovipositional period of fertilised eggs (from 13.3 ± 0.6 days for single to 17.1 ± 0.7 days for twice mating) and increased parasitism on B. tabaci primary host (from 53.1 ± 3.8 for single to 76.4 ± 5.9 for twice mating respectively). The mating experience of males increased their copulation success, whereas that of females decreased it. In conclusion, recommendations are provided for large-scale indoor rearing and field release of E. sophia. Firstly, sufficient time for providing males can be shortened to within 2 h, and a single male can engage in 2–3 mating sessions. Following the 15-day peak oviposition period, the addition of newly emerged males is advised. Secondly, for field release of adult parasitoids, it is recommended to concentrate on releasing females after completing mating indoors. For the release of pupae cards, ensure a balanced ratio of males and females on each card to facilitate mating upon emergence. Additionally, release extra males and females 2 weeks after the initial batch of releases.