Non-glandular trichomes ofSolanum carolinensedeter feeding byManduca sextacaterpillars 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 (Sphingidae) initiated feeding faster and gained more weight on (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 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.

Leaf trichomes affect caterpillar feeding in an instar-specific manner

“…However, we found that non-glandular trichomes had little effect on the initiation of feeding in third-instar caterpillars. This result provides context for our previous report that third-instar caterpillars, while not deterred from initiating feeding, are detrimentally affected by non-glandular trichomes, which damage the peritrophic matrix [3]. Szyndler et al .…”

“…For example, we previously documented that M. sexta feeding on older leaves of Solanum carolinense induced a higher density of stellate trichomes (branched non-glandular trichomes with spikes) on both surfaces of new leaves after 21 days [5]. In the same system, we also demonstrated that non-glandular stellate trichomes cause physical injury to caterpillars and impede the ability of early instar caterpillars to locate the epidermis and commence feeding [3]. For neonate caterpillars of species like M. sexta , any delay in initiating feeding could potentially prove fatal due to increased risk of desiccation, starvation, and/or predation [11].…”

“…However, various structural defenses, including the waxy plant cuticle, leaf and internode spines, and trichomes, can act to deter herbivory even prior to the onset of feeding [2,3]. Trichomes are commonly considered a first line of defense [4–6] and come in two distinct forms: glandular and non-glandular.…”

“…In the Nicotiana tabacum-Manduca sexta system, glandular trichomes have also been shown to release volatiles following caterpillar damage that are attractive to predators [9]. In contrast, non-glandular trichomes are thought to act primarily as mechanical barriers that restrict herbivore movement and thereby prevent feeding damage [3,10]. Although various defensive functions of both glandular and non-glandular trichomes have been characterized, their relative efficacy in deterring feeding by different herbivores or herbivores at different stages of development are not well understood.…”

“…For example, two commonly cultivated species, Solanum lycopersicon (tomato) and Nicotiana tabacum (tobacco), have multiple types of glandular trichomes [7,9,13], whereas the common non-domesticated weeds Solanum elaeagnifolium and Solanum carolinense are devoid of any glandular trichomes, but have a dense mat of non-glandular stellate trichomes [3,5,14], (Figure 1). Here using multiple species from Solanaceae, we examined the effects of trichome type X M. sexta larval instar on feeding initiation.

10.1080/19420889.2018.1486653-F0001Figure 1.(a) Trichome morphology of S. eleaegnifolium.

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