Red leaf margins indicate increased polygodial content and function as visual signals to reduce herbivory in Pseudowintera colorata

Abstract

Summary• Red-pigmented leaf margins are common, but their functional significance is unknown. We hypothesized that red leaf margins reduce leaf herbivory by signalling to herbivorous insects the presence of increased chemical defences.• Leaves were collected from a natural population of Pseudowintera colorata. Margin size, herbivory damage, anthocyanin content and concentrations of polygodial, a sesquiterpene dialdehyde with antifeedant properties, were quantified. Feeding trials involving larvae of Ctenopseustis obliquana, a generalist herbivore, were conducted on red-and green-margined P. colorata leaves in darkness, or under white, green or red light.• Leaves with wider red margins contained higher concentrations of polygodial and anthocyanins, and incurred less natural herbivory. In trials under white light, C. obliquana consumed disproportionately more green-than red-margined leaf laminae. Larvae exhibited no feeding preference when light was manipulated such that leaf colour discrimination was impaired.• Red leaf margins provide a reliable and effective visual signal of chemical defence in P. colorata. Ctenopseustis obliquana larvae perceive and respond to the colour of the leaf margins, rather than to olfactory signals. Our study provides direct experimental evidence for aposematic coloration in red leaves.

Elucidating the Role of Transport Processes in Leaf Glucosinolate Distribution

“…Whether insects adapted first to plants or the other way around is an ongoing debate in this research field (Schoonhoven et al, 2005;Ali and Agrawal, 2012). Leaf margin accumulation of defense compounds has been demonstrated in various plant species (Gutterman and Chauser-Volfson, 2000;Chauser-Volfson et al, 2002;Kester et al, 2002;Cooney et al, 2012). In the model plant Arabidopsis (Arabidopsis thaliana), higher concentration of glucosinolates, which constitute a major part of the chemical defense system in this plant (Kliebenstein et al, 2001a;Halkier and Gershenzon, 2006), was found at the leaf midrib and margins compared with the leaf lamina (Shroff et al, 2008;Sønderby et al, 2010).…”

Red/purple leaf margin coloration: Potential ecological and physiological functions

“…The authors concluded with a recommendation that future studies examine relative concentrations of specific defense compounds with anthocyanins, rather than entire metabolic pools. Accordingly, Cooney et al (2012) demonstrated that the width of red margins in leaves of Pseudowintera colorata correlated positively with concentrations of the defense compound polygodial, and negatively with the extent of leaf herbivory observed in the field (Fig. 3).…”

“…However, results are not always consistent across insect taxa (Irwin et al, 2003). Support for red leaf coloration as an honest signal of diminished leaf quality and/or elevated chemical defenses include correlations between increased reddening and low foliar nitrogen (Schaberg et al, 2003;Kytridis et al, 2008;Nikiforou et al, 2011;Carpenter et al, 2014), low phosphorus (Dell et al, 1987;Bernier and Brazeau, 1988;Raese, 2002;Tng et al, 2014), increased phenolics (Karageorgou and Manetas, 2006;Karageorgou et al, 2008) and other defense compounds (e.g., polygodial in Cooney et al, 2012). Some studies have further suggested that anthocyanins themselves may impair herbivore growth and vigor.…”

“…Statistically significant differences between groups: *, P < 0.05, **, P < 0.01. Figures adapted with permission from Cooney et al (2012) by permission of Oxford University Press. The role of anti-predatory coloration, a very broad issue in zoology, has received very little attention in plants (see review by Reeves, 2011).…”

Seeing Green: The Re-discovery of Plants and Nature’s Wisdom

“…As the new day approaches, their color turns to pink and later to red and simultaneously the flower orientation changes to become pendulous, to attract day pollinators such as honeybees, flies, and sunbirds [22]. Other plants like Pseudowintera colorata turn their leaf margins red to reduce predatory attacks by signaling to herbivorous insects the presence of increased chemical defenses [23]; this is one of numerous examples of aposematic or warning coloration in plants. Yet despite the recognized evolutionary importance of warning signals in shaping relationship between species [24], it took a long time for scientists to consider plant coloration in this context and sadly, a database search of "aposematism in plants" does not yield anything earlier than the year 2001 (see [25] for a review of the topic).…”