Abstract
Specialised metabolites in lichens are generally considered repellent compounds by consumers. Nevertheless, if the only food available is lichens rich in specialised metabolites, lichenophages must implement strategies to overcome the toxicity of these metabolites. Thus, the balance between phagostimulant nutrients and deterrent metabolites could play a key role in feeding preferences. To further understand lichen-gastropod interactions, we studied the feeding behaviour and consumption in Notodiscus hookeri, the land snail native to sub-Antarctic islands. The lichen Usnea taylorii was used because of its simple chemistry, its richness in usnic acid (specialised metabolite) and arabitol (primary metabolite) and its presence in snail habitats. Choice tests in arenas with intact lichens versus acetone-rinsed lichens were carried out to study the influence of specialised metabolites on snail behaviour and feeding preference. Simultaneously, usnic acid and arabitol were quantified and located within the lichen thallus using HPLC-DAD-MS and in situ imaging by mass spectrometry to assess whether their spatial distribution explained preferential snail grazing. No-choice feeding experiments, with the pure metabolites embedded in an artificial diet, defined a gradual gustatory response, from strong repellence (usnic acid) to high appetence (D-arabitol). This case study demonstrates that the nutritional activity of N. hookeri is governed by the chemical quality of the food and primarily by nutrient availability (arabitol), despite the presence of deterrent metabolite (usnic acid).
Highlights
Optimal foraging in generalist species consists in finding the right balance between need to overcome potential toxic compounds and access to useful nutrients
Unlike other Usnea species (Seymour et al, 2007), the central axis of U. taylorii is divided into several smaller axial strands by the protruding medulla, which are surrounded by some algae
Arabitol and usnic acid were found partly co-localized in the cortex and in the apothecia, and these two parts being eaten by N. hookeri, the question arises whether both metabolites are attractive to the snail
Summary
Optimal foraging in generalist species consists in finding the right balance between need to overcome potential toxic compounds and access to useful nutrients. We intended to explore the spatial localization of the main primary (D-arabitol) and secondary (usnic acid) metabolites of U. taylorii using in situ mass spectrometry imaging. As an example of this statement, Asplund (2011b) described a perpendicular grazing of the lichens thalli after acetone rinsing in two Lobaria species, while snails avoided medulla before removal of acetone soluble metabolites, suggesting the presence of deterrent compounds in the medulla.
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