A bee’s eye view of flowers

The large, tunnel-like, dark-red flowers of Iris atropurpurea are likely to have evolved to mimic protective shelters preferred by male solitary bees.
‘Bee-black’ flowers mimic protective shelters for pollination
‘Bee-black’ flowers mimic protective shelters for pollination

Flowering plants around the world deploy a spectacular diversity of floral forms, colours and scents, all interacting in varying degrees, to entice foraging insects that inadvertently move pollen between or within flowers and bring about pollination in the process. Bees in particular, with approximately 20 000 species worldwide and their tight interdependence with flowering plants, are key to the sexual reproduction of both wild plants and cultivated crops. Bees use combinations of visual, olfactory and tactile floral traits to locate floral resources, and although we still know very little about their innate preferences for colours and scents, a series of experimental studies has reported that bees show distinct sensory biases for violet- and blue-coloured flowers.

By contrast, red flowers as we perceive them (‘human-red’) have classically been associated with the pollination by hummingbirds or by butterflies and have been suggested repeatedly to go unnoticed by bees. Recent results suggest that red, as a colour, has a filtering effect on pollinators, discouraging bees whose visual receptors are more sensitive to other wavelengths, namely to the UV-blue-green range of the spectrum. Bees have long been considered to be red-blind because pure red colours usually absorb light across the 30- to 630-nm range and reflect light in wavelengths where the bees’ discrimination capabilities are comparatively very low. However, the analysis of floral colours from a human perspective has limitations, and several studies have challenged this theory of the bees’ red-blindness.

Among the few ‘human-red’ flowers that have evolved specialized interactions with bees are species belonging to the section Oncocyclus of the genus Iris (Iridaceae). These plants are endemic to dry, Mediterranean-type climates, particularly to the semi-desert areas of the Middle-East, Turkey and the Caucasus. The tunnel-like flowers of the Oncocyclus irises are large and some species display dark-red petals with a characteristic black disc marking the entrance of the floral tunnels. The flowers do not produce nectar but provide protective shelters (i.e. a non-nutritive form of reward) primarily to male solitary bees, particularly by eucerine bees (Apidae, Eucerini), that pollinate the flowers during periods of overcast weather or late in the afternoon while looking for an overnight shelter. The same bees that pollinate the Oncocyclus irises can also be found in ‘natural’ shelters, i.e. in rock crevices, under flat stones or in hollow wood stems, at exactly the same time of day and/or under the same climatic conditions. These male eucerine bees generally ignore the flowers altogether during daytime when they visit flowers of other plants for the collection of pollen and nectar. These circumstances led to the hypothesis that the Oncocyclus irises mimic protective shelters used by male solitary bees.

A recent paper in Annals of Botany investigates the adaptive significance of floral traits in Iris atropurpurea. Combining field surveys of pollinators with investigations of floral colours (by spectrophotometry), and scents [by gas chromatography–mass spectrometry] it assesses the adaptive significance of phenotypic characteristics: (a) How do pollinators perceive the floral colours of I. atropurpurea? (b) Do pollinators preferentially visit floral tunnels facing the rising sun? (c) Do pollinators exhibit preferences for floral tunnels emitting specific blends of compounds in their floral scent?

The authors suggest that the large, tunnel-like, dark-red flowers of I. atropurpurea (perceived as ‘bee-black’) is likely to have evolved by pollinator-mediated selection primarily to mimic hollow, dark protective shelters used preferentially by male solitary bees.

 

A pollinators’ eye view of a shelter mimicry system. (2013) Annals of Botany 111 (6): 1155-1165. doi: 10.1093/aob/mct081
‘Human-red’ flowers are traditionally considered to be rather unpopular with bees, yet some allogamous species in the section Oncocyclus (genus Iris, Iridaceae) have evolved specialized interactions with their pollinators, a narrow taxonomic range of male solitary bees. The dark-red, tubular flowers of these irises are nectarless but provide protective shelters (i.e. a non-nutritive form of reward) primarily to male solitary bees (Apidae, Eucerini) that pollinate the flowers while looking for a shelter. An earlier study on orchids suggested that species pollinated predominantly by male solitary bees produce significantly larger amounts and larger numbers of different n-alkenes (unsaturated cuticular hydrocarbons). Whether or not this also applies to the Oncocyclus irises and whether pollinators are attracted by specific colours or scents of these flowers is unknown. Using Iris atropurpurea, recording of pollinator preferences for shelters with different spatial parameters was combined with analyses of floral colours (by spectrophotometry) and scents (by gas chromatography–mass spectrometry) to test the hypotheses that (a) pollinators significantly prefer floral tunnels facing the rising sun (floral heat-reward hypothesis), and that (b) flowers pollinated predominantly by male solitary bees produce significantly larger amounts and larger numbers of unsaturated cuticular hydrocarbons (n-alkenes) in their floral scent (preadaptation to sexual-deception hypothesis). Male bees do not significantly prefer shelters facing the rising sun or with the presence of high absolute/relative amounts and numbers of n-alkenes in the floral scent. The results suggest that the flowers of I. atropurpurea probably evolved by pollinator-mediated selection acting primarily on floral colours to mimic large achromatic (‘bee-black’) protective shelters used preferentially by male solitary bees, and that pollinator visits are presumably not the result of an odour-based sexual stimulation or motivated by an increased morning floral heat reward in tunnels facing the rising sun.