Flower vs. leaf feeding by Pieris brassicae: glucosinolate-rich flower tissues are preferred and sustain higher growth rate

Abstract

Interactions between butterflies and caterpillars in the genus Pieris and plants in the family Brassicaceae are among the best explored in the field of insect-plant biology. However, we report here for the first time that Pieris brassicae, commonly assumed to be a typical folivore, actually prefers to feed on flowers of three Brassica nigra genotypes rather than on their leaves. First- and second-instar caterpillars were observed to feed primarily on leaves, whereas late second and early third instars migrated via the small leaves of the flower branches to the flower buds and flowers. Once flower feeding began, no further leaf feeding was observed. We investigated growth rates of caterpillars having access exclusively to either leaves of flowering plants or flowers. In addition, we analyzed glucosinolate concentrations in leaves and flowers. Late-second- and early-third-instar P. brassicae caterpillars moved upward into the inflorescences of B. nigra and fed on buds and flowers until the end of the final (fifth) instar, after which they entered into the wandering stage, leaving the plant in search of a pupation site. Flower feeding sustained a significantly higher growth rate than leaf feeding. Flowers contained levels of glucosinolates up to five times higher than those of leaves. Five glucosinolates were identified: the aliphatic sinigrin, the aromatic phenylethylglucosinolate, and three indole glucosinolates: glucobrassicin, 4-methoxyglucobrassicin, and 4-hydroxyglucobrassicin. Tissue type and genotype were the most important factors affecting levels of identified glucosinolates. Sinigrin was by far the most abundant compound in all three genotypes. Sinigrin, 4-hydroxyglucobrassicin, and phenylethylglucosinolate were present at significantly higher levels in flowers than in leaves. In response to caterpillar feeding, sinigrin levels in both leaves and flowers were significantly higher than in undamaged plants, whereas 4-hydroxyglucobrassicin leaf levels were lower. Our results show that feeding on flower tissues, containing higher concentrations of glucosinolates, provides P. brassicae with a nutritional benefit in terms of higher growth rate. This preference appears to be in contrast to published negative effects of volatile glucosinolate breakdown products on the closely related Pieris rapae.

Fig. 1

Schematic drawing (top and lateral views) and dimensions of water barrier applied around the stem of B. nigra plants to prevent movement of caterpillars from leaves to flowers and vice versa. A circular water container was manufactured of plastic. The middle circle consisted of a central platform, preventing drowning of caterpillars feeding on the inflorescence in the rare events of falling down or downward migration. In the center of the platform, a hole allowed the main stem to grow through. The platform was put in place around the main stem just below the branch carrying the first flower buds. The circular opening between the central hole and the stem was blocked with soft foam (not drawn)

Fig. 2

Frequency distribution of caterpillar position on B. nigra plants observed daily over a period of 12–13 d. On day 1, neonates were introduced on a true leaf just below the inflorescence. Four organ positions were distinguished: on a true leaf, on a small leaf in the inflorescence, on a flower, or on a stem in the inflorescence. Percentages are averaged based on three caterpillars per plant for eight, seven, and nine plants of accessions A, B, and C, respectively

Fig. 3

Fresh body mass of P. brassicae on either flowers (circles) or leaves (squares) of B. nigra in mid-fourth, mid-fifth, and late-fifth instar developing on B. nigra, accession A. Mean and SEM are plotted for 30 caterpillars

Fig. 4

Concentrations of five glucosinolates (mean + SEM) in leaves and flowers of 10 plants of accession A. For both leaves and flowers, the initial concentration just before treatment, the concentration in leaves or flowers of plants damaged by feeding caterpillars during 4 d, and the concentration determined in leaves or flowers of intact plants 4 d after caterpillars were introduced on the treated plants