Experimental Evidence for Plant Aposematism

Abstract

The direct experimental evidence for the operation of aposematic coloration in plants is meager; however, the direct evidence that it operates is slowly accumulating. Cook et al. (1971) showed that poisonous gray seeds of Eremocarpus setigerus are rejected by the mountain dove. Cahn and Harper (1976) showed that sheep avoid Trifolium repens plants with leaf marks, but did not discuss aposematism. Lev-Yadun and Ne’eman (2004) showed that sheep, goats, camels, donkeys and cattle reject conspicuous green plants in the yellow/gray desert in the summer. Numata et al. (2004) found that leaves with delayed greening suffer lower levels of insect damage when they are still young. Hill (2006) showed that the Florida scrub jay (Aphelocoma coerulescens) rejects poisonous red fruits. Karageorgou and Manetas (2006) showed that red young leaves of the evergreen oak Quercus coccifera are attacked less by insects than green ones, but rejected the aposematic coloration hypothesis and adopted other visual defensive explanations (red masks the green color, it undermines insect camouflage). Similar results were found for other species growing in Greece (Karageorgou et al. 2008). Recently, additional data about the defensive operation of white variegation that mimics insect damage in leaves was published (Campitelli et al. 2008; Soltau et al. 2009). Gerchman et al. (2012) tested the question of whether colorful visual signaling for pollinators can simultaneously serve for aposematism. The conspicuous purple tufts of leaves (“flags”), which often terminate vertical inflorescences in the Mediterranean annual Salvia viridis and attract insect pollinators to the flowering patch, have an aposematic potential towards herbivores. 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. Furthermore, when these authors conducted feeding trials using larvae of the generalist herbivore Ctenopseustis obliquana (brown-headed leafroller moth), which are known to naturally feed on P. colorata leaves, a significant preference for leaves lacking red margins was observed under white light, but not under red light or darkness that cancelled the visual signaling, consistent with a visual, herbivory-deterrent function (Cooney et al. 2012). Field data from Finland for ergot (Claviceps purpurea) mutualism in Festuca rubra plants in grazed areas, showed that mammalian grazers indeed refrain from eating infected plants (Wali et al. 2013), thus supporting the hypothesis posited by Lev-Yadun and Halpern (2007) about ergot aposematism. Rostas et al. (2013) showed that red galls that emit various repeling volatiles are rejected by goats in choice feeding experiments. Maskato et al. (2014) studied in more detail the find by Gerchman et al. (2012) that locusts preferred green cabbage over anthocyanin-rich red cabbage. They found that female Pieris butterflies avoid laying eggs on anthocyanin-rich red foliage, suggesting that red color is at least a visual cue affecting oviposition behavior. They reared P. brassicae larvae on green and red cabbage leaves, to determine whether foliage color reliably indicates host plant quality. They did not find a difference in survival rates or maximal larval body mass in the two food treatments. However, larvae feeding on red cabbage leaves exhibited significantly lower growth rates and longer durations of larval development. Interestingly, this longer development was coupled with a higher consumption rate of dry food matter. The lower ratio of body mass gain to food consumption in larvae feeding on red cabbage leaves was coupled with significantly higher (ca. 10 %) larval metabolic rates. This suggested that insect development on red foliage may incur an increased metabolic load associated with detoxification of various secondary plant metabolites. Energy and oxygen allocation to detoxification could come at the expense of growth and thus compromise larval fitness as a result of extended development. Maskato et al. (2014) proposed that from an evolutionary perspective, red foliage color may serve as an honest defensive cue, and I say probably a signal, as it reliably indicates the plant’s low quality as a substrate for larval development. The possibility of simultaneous olfactory aposematism has not been tested in any of these cases.