Overcoming deterrent metabolites by gaining essential nutrients: A lichen/snail case study

Area of Science:

• * Ecology and animal behaviour
• * Biochemistry and chemical ecology

Background:

• * Specialized metabolites in lichens are typically deterrent to consumers.
• * Lichen-feeding animals (lichenophages) must develop strategies to cope with toxic compounds when lichens are the sole food source.
• * The balance between phagostimulant nutrients and deterrent metabolites is crucial in determining feeding preferences.

Purpose of the Study:

• * To investigate the feeding behavior and consumption patterns of the sub-Antarctic land snail Notodiscus hookeri.
• * To understand the role of specialized metabolites, specifically usnic acid and arabitol, in lichen-gastropod interactions.
• * To determine how the chemical composition and spatial distribution of metabolites in Usnea taylorii influence snail feeding preferences.

Main Methods:

• * Conducted choice tests using intact and acetone-rinsed Usnea taylorii lichens to assess snail behavioral responses.
• * Quantified and localized usnic acid and arabitol within the lichen thallus using High-Performance Liquid Chromatography-Diode Array Detection-Mass Spectrometry (HPLC-DAD-MS) and in situ imaging mass spectrometry.
• * Performed no-choice feeding experiments with pure usnic acid and D-arabitol embedded in an artificial diet to evaluate gustatory responses.

Main Results:

• * Acetone-rinsed lichens (with reduced usnic acid) were preferred over intact lichens, indicating the deterrent effect of usnic acid.
• * HPLC-DAD-MS and imaging mass spectrometry revealed the distribution of usnic acid and arabitol within the lichen thallus.
• * No-choice experiments showed a clear gustatory response: strong repellence to usnic acid and high appetence for D-arabitol.

Conclusions:

• * The feeding activity of Notodiscus hookeri is significantly influenced by the chemical quality of its lichen diet.
• * Nutrient availability, particularly the presence of D-arabitol, is the primary driver of feeding preference, overriding the deterrent effect of usnic acid.
• * This study highlights the complex interplay between nutritional needs and chemical defenses in lichen-herbivore interactions.