Flower Conspicuousness to Bees Across Pollination Systems: A Generalized Test of the Bee-Avoidance Hypothesis

Abstract

Flower signals of bee-and bird-pollinated plants have converged via pollinator-mediated evolution, driven by the visual system of their respective pollinators. For bird flowers, sensory exclusion of less effective bees is also important and such exclusion is also mediated by floral morphological filters. Likewise, other systems based on pollination by red-sensitive insects are also associated with red flowers displaying lower shortwavelength secondary peaks of reflectance, which decreases detectability to animals that are less sensitive to red, such as bees. These flowers often also present long tubes. Here, we tested a generalization of the bee-avoidance hypothesis in order to assess if it holds only for bird flowers or for other non-bee pollination systems as well. For this, we compared flower contrasts and spectral purity in bee visual systems as proxies for conspicuousness among four kinds of pollination systems: bee-visited flowers, insectvisited flowers (including bees and other insects), non-bee insect flowers (flowers visited by red-sensitive insects such as flies, butterflies and beetles, but not bees), and birdvisited flowers. We also assessed the association between conspicuousness to bees and flower depth, used as a proxy for morphological exclusion of bees. Overall, flower conspicuousness to bees differed only between insect (all three groups) and bird flowers, due to lower visual signals for the latter. This suggests that bee sensory exclusion via color signals is exclusive to bird flowers, while non-bee insect flowers might use other sensory channels to exclude bees, such as olfactory signals. Visual bee avoidance might be a mechanism exclusive to plants pollinated by specific guilds of redsensitive insects not well represented in our sample. We also found a negative association between flower conspicuousness to bees and flower depth, suggesting an interplay of morphological and spectral traits in discouraging bee visits. Our results support the beeavoidance hypothesis exclusively for bird flowers and an overall association between lower visual signals to bees and long tubes.

Major Flower Pigments Originate Different Colour Signals to Pollinators

“…On the one hand, they showed low chromatic contrast values in all visual models, excepting the fly model where contrast values were intermediate and only lower than those of flowers with aurones-chalcones, which matches our predictions of both groups of flowers generating the highest chromatic contrasts for dipterans. On the other hand, these flowers showed the highest achromatic contrast in the bee visual model, as reported in previous studies with white flowers (Chittka et al, 1994;Lunau et al, 2011;Coimbra et al, 2020). This fact might be relevant because honeybees use such achromatic contrast to find small flowers and flowers at long distance (Giurfa et al, 1997;Spaethe et al, 2001).…”

“…A considerable number of studies show that functional groups of pollinators can perceive differently the same flower colour (e.g., Ohashi et al, 2015;Bergamo et al, 2018;Whitney et al, 2020). In fact, it has been demonstrated that flower colours have evolved in different regions of the world to match the visual capabilities and preferences of local pollinator fauna (Burd et al, 2014;Shrestha et al, 2016;Camargo et al, 2019;Coimbra et al, 2020). Recently, it has been found in species of the Gesneriaceae that the production of certain groups of anthocyanins may generate flower reflectance spectra that are adapted to the specific pollinator groups (Ogutcen et al, 2020).…”

Fragmentary Blue: Resolving the Rarity Paradox in Flower Colors

“…This difference results from the frequent evolution of red floral signals among bird-pollinated flowers ( Shrestha et al, 2013 ; Burd et al, 2014 ), which tend to have spectral patterns that only weakly modulate bee photoreceptors ( Lunau et al, 2011 ). It has been argued that the highly saturated red of bird-pollinated flowers has evolved to make flowers less apparent to bees and thus serving as bee avoidance mechanism ( Lunau et al, 2011 ; Camargo et al, 2019 ; Coimbra et al, 2020 ). However, the spectral evidence could also be compatible with direct selection by birds, with the effect on bee perception arising as a by-product.…”

Bird pollination syndrome is the plant's adaptation to ornithophily, but nectarivorous birds are not so selective

“…Considering the bird pollination syndrome, it has been shown for example that the most specialized nectarivorous birds, hummingbirds, have no preference for red colouration (Collias and Collias 1968, Miller and Miller 1971). Instead the red colour may sensorially exclude bees (a group with no photoreceptors for red light) from ornithophilous flowers (Bergamo et al 2016, Coimbra 2020). Therefore, while the most efficient pollinators may truly coincide with the defined pollination syndrome (Rosas‐Guerrero et al 2014), from the pollinators' perspective, floral choice may likely be simplerdetermined only by the quantity and quality of food rewards (Waser 1983, Pleasants and Waser 1985, Stromberg and Johnsen 1990, Essenberg 2012, Schmid et al 2016).…”