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

Abstract

Summary Related 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. Whereas L. nana is known to attack the pupae of a number of primary parasitoids in the genus Cotesia, both C. glomerata and P. brassicae are 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 of B. nigra than in corresponding shoots of B. oleracea. Cocoon weight in C. glomerata was unaffected by the foodplant on which P. brassicae was 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 on B. oleracea than on B. nigra. Moreover, body mass in L. nana was typically larger in young (c. 24 h), than in older (c. 72 h) cocoons of C. glomerata. Egg‐to‐adult development time in L. nana generally increased with host size and age, and wasps on younger hosts completed their development more rapidly on B. 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.

Development of an Insect Herbivore and its Pupal Parasitoid Reflect Differences in Direct Plant Defense

“…The similarity in the effect of plant strain on the body mass of Pieris rapae and Pteromalus puparum reveals that qualitative constraints on the herbivore were passed from the second to the third trophic level. Several other studies have reported variable effects of plant quality, probably mediated by allelochemicals, on the performance of insect parasitoids and predators (Campbell and Duffey 1979;Barbosa et al 1986, Gunasena et al 1990Havill and Raffa 2000;Harvey et al 2003Harvey et al , 2005Harvey et al , 2007. If herbivore and parasitoid performance were positively correlated with total glucosinolate levels, we would have predicted that the rank order of plant quality would be cultivar > Kimmeridge > Old Harry > Winspit.…”

“…A number of studies have reported that allelochemicals in the diet of hosts or prey negatively affect the development of their parasitoids and predators (Barbosa et al 1986, Duffey et al 1986Gunasena et al 1990;Traugott and Stamp 1996;Havill and Raffa 2000;reviewed by Harvey 2005 andOde 2006). Further, the effects of allelochemicals may even be manifested in the fourth trophic level (Orr and Boethel 1986;Harvey et al 2003;Soler et al 2005), showing that they can work their way up through the food chain.…”

Variation In Plant Volatiles and Attraction Of The ParasitoidDiadegma semiclausum(Hellén)

“…Plants used were malting barley (Hordeum vulgare L. cv Video) (Cyperales, Gramineae), white mustard (Sinapis alba L. cv Carnaval) (Capparales, Brassicaceae), Brussels sprout (Brassica oleracea L. gemmifera cv Cyrus) (Capparales, Brassicaceae), and a naturalized population of Brassica oleracea L. This feral population was found in a roadside hollow in 2001, it probably "escaped" from a local farm, and it is unknown how long it has been growing in the wild (Harvey et al, 2003). Plants were reared in a greenhouse compartment under a 16L; 8D photoperiod, 20-28 • C, and 40-80% R.H. Plants were sown in ca.…”

Population genetic structure of two primary parasitoids of Spodoptera frugiperda (Lepidoptera), Chelonus insularis and Campoletis sonorensis (Hymenoptera): to what extent is the host plant important?

“…These effects can strongly vary among plant species (Smith 1957;Altahtawy et al 1976;Bhatt & Singh 1989;Senrayan & Annadurai 1991;Werren et al 1992;Fox et al 1996;Kruse & Raffa 1997;Eben et al 2000;Harvey et al 2003;Zvereva & Rank 2003;Lu et al 2004) and even among cultivars of a same plant species (Kauffman & Flanders 1985;Orr & Boethel 1985;Hare & Luck 1991;Reed et al 1991;Rogers & Sullivan 1991;Riggin et al 1992;Stark et al 1992;Dosdall & Ulmer 2004;KahuthiaGathu et al 2008).…”