Floral plasticity: Herbivore-species-specific-induced changes in flower traits with contrasting effects on pollinator visitation

Abstract

Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant-pollinator interactions. Current knowledge on the full extent of herbivore-induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore-induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species-specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant-mediated interactions with mutualists.

Keywords: Brassica nigra (black mustard); flower colour; flower morphology; flower rewards; flower volatiles; herbivore-induced plant responses; phenotypic plasticity; plant defence; plant-mediated interactions; specificity.

Figure 1

Relative diffuse reflection (RDR) of yellow (570–650 nm) and UV (310–370 nm) wavelengths by petals of uninfested Brassica nigra plants or plants infested with different herbivores. (a) Relative diffuse reflection of yellow of top parts of petals. (b) Relative diffuse reflection of yellow of base parts of petals. (c) Relative diffuse reflection of UV of top parts of petals. (d) Ratio RDR yellow/RDR UV of top parts of petals. Boxplots show median (line), mean (x), first and third quartiles, and minimum and maximum. Outliers (1.5 times the interquartile range below the first quartile or above the third quartile) are represented by circles. The red dot on the flower images indicates where measurements were taken (top or base), which was done after 7 days of herbivory. Number of replicates per herbivore treatment varied between six and eight plants. From each plant, six flowers were used, of which each petal was measured, both top and base parts. Letters above bars indicate significant differences at α = 0.05 based on Tukey's post hoc tests [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Dendrogram and heat map of the emission of volatile compounds of Brassica nigra plants infested with different herbivores or uninfested plants. Dendrogram clustering was performed using Ward's clustering algorithm with Euclidean distances. Values in the dendrogram are approximately unbiased probability values, where values ≥ 95 indicate significant differences. For the heat map, we used range‐scaled log‐transformed values of volatile emission (peak area/g FW) for each compound. Volatiles were collected after 7 days of herbivory. Number of replicates per herbivore treatment varied between seven and nine plants [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Nectar volume and number of pollen grains of uninfested Brassica nigra plants or plants infested with different herbivores. (a) Nectar volume of eight flowers of uninfested B. nigra plants or plants infested with different herbivores. Number of replicates per herbivore treatment varied between 14 and 15 plants. (b) Number of pollen grains of one flower of uninfested B. nigra plants or plants infested with different herbivores. Boxplots show median (line), mean (x), first and third quartiles, and minimum and maximum. Outliers (1.5 times the interquartile range below the first quartile or above the third quartile) are represented by circles. Nectar volume and number of pollen grains were measured after 7 days of herbivory. Number of replicates per herbivore treatment was 10 plants; per plant, we measured pollen for five flowers. Letters above bars indicate significant differences at α = 0.05 based on Tukey's post hoc tests [Colour figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Preferences of the butterfly Pieris brassicae for uninfested Brassica nigra plants or plants infested with different herbivores. (a) Proportion of P. brassicae butterflies (mean ± SE) that first landed on flowers or leaves of B. nigra plants infested with different herbivores or uninfested plants. (b) Visitation duration (mean ± SE); (c) number of flowers visited (mean ± SE); and (d) time spent per flower (mean ± SE) by individual pollinators on infested or uninfested B. nigra plants. Butterfly behaviour was assessed after 7 days of herbivory. Number of replicates per herbivore treatment varied between 75 and 89 butterflies, and eight and 10 plant pairs. Asterisks above bars indicate significant differences with ***P < 0.001, **0.001 ≥ P < 0.01, *0.01 ≥ P ≤ 0.05, and ●0.05 > P < 0.1, based on Tukey's post hoc tests. Photograph shows a P. brassicae butterfly visiting flowers of B. nigra. Photograph credit: Quint Rusman [Colour figure can be viewed at http://wileyonlinelibrary.com]