Non-glandular trichomes of Solanum carolinense deter feeding by Manduca sexta caterpillars and cause damage to the gut peritrophic matrix

Abstract

Plant trichomes constitute a first line of defence against insect herbivores. The pre- and post-ingestive defensive functions of glandular trichomes are well documented and include direct toxicity, adhesion, antinutrition and defence gene induction. By contrast, the defensive functions of non-glandular trichomes are less well characterized, although these structures are thought to serve as physical barriers that impede herbivore feeding and movement. We experimentally varied the density of stellate non-glandular trichomes in several ways to explore their pre- and post-ingestive effects on herbivores. Larvae of Manduca sexta (Sphingidae) initiated feeding faster and gained more weight on Solanum carolinense (Solanaceae) leaves having lower trichome densities (or experimentally removed trichomes) than on leaves having higher trichome densities. Adding trichomes to artificial diet also deterred feeding and adversely affected caterpillar growth relative to controls. Scanning electron and light microscopy revealed that the ingestion of stellate trichomes by M. sexta caterpillars caused extensive damage to the peritrophic membrane, a gut lining that is essential to digestion and pathogen isolation. These findings suggest that, in addition to acting as a physical barrier to deter feeding, trichomes can inhibit caterpillar growth and development via post-ingestive effects.

Keywords: Manduca sexta; Solanum carolinense; herbivory; peritrophic matrix; plant defence; trichomes.

Figure 1.

Mean ± s.e. of time until feeding onset (a) and per cent weight gain (b) for first-instar M. sexta caterpillars on inbred (low trichome density) and outbred (high trichome density) horsenettle plants after 3 days of feeding. Asterisk indicates significance (p < 0.05) for post hoc Tukey tests from ANOVA. (Online version in colour.)

Figure 2.

Mean ± s.e. of per cent weight gain of first-instar M. sexta caterpillars after 2 days of feeding on leaves with intact trichomes and ‘shaved’ leaves lacking trichomes. Asterisk indicates significance (p < 0.05) after unpaired t-test. (Online version in colour.)

Figure 3.

Mean ± s.e. of per cent weight gain of first-instar M. sexta caterpillars on control artificial diet and artificial diet enriched with trichomes. Data collected after 3 days of feeding. Asterisk indicates significance (p < 0.05) after unpaired t-test. (Online version in colour.)

Figure 4.

First-instar M. sexta choice between regular artificial diet and diet enriched with trichomes. First choice (initial) and choice after 24 h were recorded. Asterisk indicates significance (p < 0.05) for χ² analyses. (Online version in colour.)

Figure 5.

Images of frass (a,b) and PM (c–f) from third-instar M. sexta caterpillars fed diets varying in trichome content. (a) Frass from caterpillar fed trichome-free artificial diet. (b) Frass from a caterpillar fed intact S. carolinense leaves, showing embedded trichomes. (c) PM from a caterpillar fed trichome-free artificial diet. (d) PM from a caterpillar fed intact S. carolinense leaves, showing protruding trichome spines. (e) PM from a caterpillar fed intact Nicotiana tabacum leaves (which lack stellate trichomes), showing no damage. (f) PM from a caterpillar fed intact S. eleagnifolium leaves, showing protruding trichomes. Scanning electron microscopy was used for a–d, light microscopy for e and f.