Variability in floral volatile emissions can occur temporally through floral development, during diel cycles, as well as spatially within a flower. These spatiotemporal patterns are hypothesized to ...provide additional information to floral visitors, but they are rarely measured, and their attendant hypotheses are even more rarely tested. In Penstemon digitalis, a plant whose floral scent has been shown to be under strong phenotypic selection for seed fitness, we investigated spatiotemporal variation in floral scent by using dynamic headspace collection, respectively solid-phase microextraction, and analyzed the volatile samples by combined gas chromatography–mass spectrometry. Total volatile emission was greatest during flowering and peak pollinator activity hours, suggesting its importance in mediating ecological interactions. We also detected tissue and reward-specific compounds, consistent with the hypothesis that complexity in floral scent composition reflects several ecological functions. In particular, we found tissue-specific scents for the stigma, stamens, and staminode (a modified sterile stamen common to all Penstemons). Our findings emphasize the dynamic nature of floral scents and highlight a need for greater understanding of ecological and physiological mechanisms driving spatiotemporal patterns in scent production.
Nectar scents are thought to function as honest signals of reward used by pollinators, but this hypothesis has rarely been tested.
Using Penstemon digitalis, we examined honest signalling of the ...nectar volatile (S)‐(+)‐linalool and pollinator responses to linalool in both field and laboratory settings. Because our previous work showed that linalool emission was associated with higher female fitness and that nectar is scented with linalool, we hypothesized that linalool was an honest signal of nectar reward. To assess honesty, we measured linalool–nectar associations including nectar volume, sugar amount, concentration and production rate for inflorescences and flowers in several populations. We also assessed whether Bombus impatiens, the main pollinator of P. digitalis at our sites, can use linalool as a foraging signal. We supplemented real or artificial flowers in the field and laboratory with varying linalool–nectar combinations to measure pollinator behavioural responses.
We found that an inflorescence's linalool emissions could be used to predict nectar rewards in P. digitalis, but this was driven by indirect associations with display size rather than directly advertising more profitable flowers. For flowers within inflorescences there was also no evidence for an association between signal and reward. Field tests of bumblebee behaviour were inconclusive. However, in laboratory assays, bumblebees generally used variation in linalool emissions to choose more profitable flowers, demonstrating they can detect differences in linalool emitted by P. digitalis and associate them with reward profitability. These results suggest experiments that decouple display size, scent and reward are necessary to assess whether (and when) bees prefer higher linalool emissions. Bees preferred nectars with lower linalool concentrations when linalool flavoured the nectar solution, suggesting the potential for conflicting pressures on scent emission in the field.
Synthesis. Our results highlight the challenges of assessing function for traits important to fitness and suggest that the perception of floral signalling honesty may depend on whether pollinators use inflorescences or flowers within inflorescences when making foraging decisions. We conclude that future research on honest signalling in flowering plants, as well as its connection to phenotypic selection, should explicitly define honesty, in theoretical and experimental contexts.
Signal honesty in flowers is complex: we found that scented‐nectar is not always an honest signal in flowers of Penstemon digitalis. While inflorescences that had stronger linalool emission also produced more nectar with more sugar, we found that linalool is unlikely to predict which flowers within those inflorescences have the most nectar. The main pollinators, Bombus impatiens bumble bees, can use an association between linalool and nectar rewards to make foraging decisions, provided that the rewards are sufficiently motivating to support discriminating differences. Our results suggest that simple correlations between floral signals and rewards are unlikely to be common in nectar‐rewarding plants.
Bacteria on floral tissue can have negative effects by consuming resources and affecting nectar quality, which subsequently could reduce pollinator visitation and plant fitness. Plants however can ...employ chemical defences to reduce bacteria density. In North American, bee-pollinated
Penstemon digitalis
, the nectar volatile
S
-(+)-linalool can influence plant fitness, and terpenes such as linalool are known for their antimicrobial properties suggesting that it may also play a role in plant–microbe interactions. Therefore, we hypothesized linalool could affect bacterial growth on
P. digitalis
plants/flowers. Because
P. digitalis
emits linalool from nectar and nectary tissue but not petals, we hypothesised that the effects of linalool could depend on tissue of origin due to varying exposure. We isolated bacteria from nectary tissue, petals and leaves, and compared their growth relative to control using two volatile concentrations representing the natural emission range of linalool. To assess whether effects were specific to linalool, we compared results with the co-occurring nectar volatile, methyl nicotinate. We show that response to floral volatiles can be substance and tissue-origin specific. Because linalool could slow growth rate of bacteria across the
P. digitalis
phyllosphere, floral emission of linalool could play a role in mediating plant–bacteria interactions in this system.
Natural selection is thought to have shaped the evolution of floral scent; however, unlike other floral characters, we have a rudimentary knowledge of how phenotypic selection acts on scent. We found ...that floral scent was under stronger selection than corolla traits such as flower size and flower color in weakly scented Penstemon digitalis. Our results suggest that to understand evolution in floral phenotypes, including scent in floral selection, studies are crucial. For P. digitalis, linalool was the direct target of selection in the scent bouquet. Therefore, we determined the enantiomeric configuration of linalool because interacting insects may perceive the enantiomers differentially. We found that P. digitalis produces only (S)-(+)-linalool and, more interestingly, it is also taken up into the nectar. Because the nectar is scented and flavored with (S)-(+)-linalool, it may be an important cue for pollinators visiting P. digitalis flowers.
Natural selection is thought to have shaped the evolution of floral scent; however, unlike other floral characters, we have a rudimentary knowledge of how phenotypic selection acts on scent. We found ...that floral scent was under stronger selection than corolla traits such as flower size and flower color in weakly scented Penstemon digitalis. Our results suggest that to understand evolution in floral phenotypes, including scent in floral selection, studies are crucial. For P. digitalis, linalool was the direct target of selection in the scent bouquet. Therefore, we determined the enantiomeric configuration of linalool because interacting insects may perceive the enantiomers differentially. We found that P. digitalis produces only (S)-(+)-linalool and, more interestingly, it is also taken up into the nectar. Because the nectar is scented and flavored with (S)-(+)-linalool, it may be an important cue for pollinators visiting P. digitalis flowers.
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