Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid

Abstract

SummaryRelated plant species with different spatial and/or temporal life‐history characteristics often possess differences in secondary chemistry and thus direct defensive capability. These differences are often attributed to a range of divergent selection pressures from herbivores and pathogens. Most studies of insect–plant interactions have examined the effects of plant defence on herbivore performance, with less attention being paid to higher trophic levels, such as parasitoid wasps. Moreover, to date it is not known whether secondary plant compounds may affect organisms in the fourth trophic level.Here, we study interactions in a four‐trophic‐level system. The development of a solitary secondary hyperparasitoid,Lysibia nana, and its primary endoparasitoid host,Cotesia glomerata, are compared when reared from a primary herbivore host,Pieris brassicae, which was itself reared on two cruciferous plants with contrasting life histories. WhereasL. nanais known to attack the pupae of a number of primary parasitoids in the genusCotesia, bothC. glomerataandP. brassicaeare intimately associated with plants in the family Brassicaceae.Insects were reared from a feral population of the spring perennial,Brassica oleracea, and a naturally occurring population of a summer annual,B. nigra. Like other cruciferous plants, both species are known to produce glycoside toxins (= glucosinolates) after they are attacked by foliar herbivores. However, concentrations of glucosinolates were more than 3·5 times higher in young shoots ofB. nigrathan in corresponding shoots ofB. oleracea.Cocoon weight inC. glomeratawas unaffected by the foodplant on whichP. brassicaewas reared, whereas in 24‐h‐old host cocoons emerging adult hyperparasitoid body mass increased significantly with cocoon size and wasps were significantly larger, and survived better onB. oleraceathan onB. nigra. Moreover, body mass inL. nanawas typically larger in young (c.24 h), than in older (c.72 h) cocoons ofC. glomerata. Egg‐to‐adult development time inL. nanagenerally increased with host size and age, and wasps on younger hosts completed their development more rapidly onB. nigra.Our results clearly demonstrate that qualitative differences in herbivore diet can differently affect the performance of interacting organisms across several trophic levels, and suggest that bottom‐up forces may also play a role in mediating interactions involving plants–herbivores–parasitoids and hyperparasitoids.