Population-related variation in plant defense more strongly affects survival of an herbivore than its solitary parasitoid wasp

Abstract

The performance of natural enemies, such as parasitoid wasps, is affected by differences in the quality of the host's diet, frequently mediated by species or population-related differences in plant allelochemistry. Here, we compared survival, development time, and body mass in a generalist herbivore, the cabbage moth, Mamestra brassicae, and its solitary endoparasitoid, Microplitis mediator, when reared on two cultivated (CYR and STH) and three wild (KIM, OH, and WIN) populations of cabbage, Brassica oleracea. Plants either were undamaged or induced by feeding of larvae of the cabbage butterfly, Pieris rapae. Development and biomass of M. brassicae and Mi. mediator were similar on both cultivated and one wild cabbage population (KIM), intermediate on the OH population, and significantly lower on the WIN population. Moreover, development was prolonged and biomass was reduced on herbivore-induced plants. However, only the survival of parasitized hosts (and not that of healthy larvae) was affected by induction. Analysis of glucosinolates in leaves of the cabbages revealed higher levels in the wild populations than cultivars, with the highest concentrations in WIN plants. Multivariate statistics revealed a negative correlation between insect performance and total levels of glucosinolates (GS) and levels of 3-butenyl GS. However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics. This result suggests that, in addition to aliphatic GS, other non-GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host. Remarkably, when developing on WIN plants, the survival of Mi. mediator to adult eclosion was much higher than in its host, M. brassicae. This may be due to the fact that hosts parasitized by Mi. mediator pass through fewer instars, and host growth is arrested when they are only a fraction of the size of healthy caterpillars. Certain aspects of the biology and life-history of the host and parasitoid may determine their response to chemical challenges imposed by the food plant.

Fig. 1

Fitness correlates (development time and mass) of the herbivore Mamestra brassicae (a, b) and its parasitoid Microplitis mediator (c, d) when they were reared on cultivated (CYR or STH) or wild (KIM, OH, WIN) cabbage (Brassica oleracea). Hosts (healthy or parasitized) were reared in Petri dishes and provided with leaf tissues collected from non-induced plants (open bars) or from plants that had been exposed to Pieris rapae feeding for 7 d (hatched bars). Leaf tissues were replaced every other day. Parasitoids data are given for males (grey or hatched grey bars) and females (white or hatched white bars) separately. Bars are the mean values (+SE) based on pooled data per dish

Fig. 2

Survival curves of healthy unparasitized Mamestra brassicae caterpillars (a) and caterpillars parasitized by Microplitis mediator (b). Survival was measured from hatching to pupation for healthy M. brassicae and for Mi. mediator from oviposition until cocoon formation. A few parasitized caterpillars developed into healthy caterpillars. These caterpillars were either not parasitized or the eggs were encapsulated and these were excluded from the data set

Fig. 3

Glucosinolate (GS) concentrations measured in samples taken from cultivated (CYR or STH) or wild cabbage (Brassica oleracea) plants originating from England (KIM, OH, WIN population). Samples were taken from non-induced plants (Non) and from plants that had been exposed to Pieris rapae feeding for 7 d (Ind). Concentrations of the detected 11 GS compounds were pooled for the three different GS classes: aromatic, indole, and aliphatic GS. Aliphatic GS were further subdivided into sulfinyl, alkenyl and hydroxylated GS. Bars give the mean values (+SE) for total GS concentrations. The number of samples varied between 8 and 10 per plant line and treatment

Fig. 4

Conceptual diagram showing the relationship between herbivore (healthy or parasitized) growth curves and cumulative mortality on food plants that differ in their quality. Solid line a and short dashed line e represent herbivore growth curves on non-induced plants; long dashed line b, dotted line c and alternating dot-dashed line d lines represent herbivore growth curves on induced plants. In this example, the parasitoid is solitary and the host caterpillar must reach a much smaller critical size to support parasitoid development (left dashed black vertical line) than to successfully pupate (right vertical black dashed line). In this study, induction steepens the mortality curve (lines a, b) reducing survival of both the parasitoid and the herbivore; the latter does not survive at all on induced plants because it cannot grow large enough to reach a minimum viable size for pupation. If the plant is even more toxic, then the parasitized host does not even reach a critical size and all parasitoids die before egression form the host (line c). In some instances, perhaps due to stress caused by parasitism, parasitoids may experience higher mortality on induced plants than their hosts (line d), or else herbivore and parasitoid mortality on non-induced plants does not differ (line e). Many different combinations are possible, depending on the effects of the plant on the herbivore and parasitoid, the parasitoid on the herbivore, and quantitative differences in the required growth of healthy and parasitized hosts