The endoparasitoid Psyllaephagus arenarius benefits from ectoparasitic venom via multiparasitism with the ectoparasitoid Tamarixia lyciumi

As solitary nymphal parasitoids of Paratrioza sinica, the ectoparasitoid Tamarixia lyciumi and the endoparasitoid Psyllaephagus arenarius act as effective biocontrol agents. Thus, it is necessary to facilitate mass productions of both species. Despite showing an excellent parasitic ability, Ps. arenarius is often trapped fatally inside 5th-instar nymphs of Pa. sinica due to strong host immunity. To improve the emergence rate of Ps. arenarius, we evaluated whether Ps. arenarius could utilize T. lyciumi venom via multiparasitism, so the parasitism characteristics of both species were examined between separate-existence (monoparasitism only) and co-existence (mono- and multiparasitism) systems. Further, the parasitism characteristics of Ps. arenarius on venom-injected hosts with/without T. lyciumi eggs were tested to further identify the facilitator. The results showed the parasitism rate of T. lyciumi was increased while that of Ps. arenarius did not change from separate-existence to co-existence systems. The intrinsic performances of two species in monoparasitism did not differ between separate- and co-existence systems. From monoparasitism (separate-existence) to multiparasitism (co-existence), no differences were detected in the intrinsic performances of T. lyciumi, but those of Ps. arenarius were greatly improved. After T. lyciumi venom injection, the parasitism characteristics of Ps. arenarius did not differ between venom-injected hosts with T. lyciumi eggs and those without, further indicating Ps. arenarius benefited from the venom of T. lyciumi females rather than T. lyciumi egg/larval secretions. Instead of negative effects, multiparasitism with ectoparasitoids improves endoparasitoids due to ectoparasitic venom. The study increases host resource utilization and provides creative ways for mass production of endoparasitoids.