The evolution of floral scent as a plant reproductive signal is assumed to be driven by pollinator behavior, with little attention paid to other potential selective forces such as herbivores. I tested 10 out of the 13 compounds emitted by dioecious Cirsium arvense, Canada thistle, including 2-phenylethanol, methyl salicylate, p-anisaldehyde, benzaldehyde, benzyl alcohol, phenylacetaldehyde, linalool, furanoid linalool oxides (E and Z), and dimethyl salicylate. Single compounds (and one isomer) set out in scent-baited water-bowl traps trapped over 10 species of pollinators and 16 species of floral herbivores. The two dominant components of the fragrance blend of C. arvense, benzaldehyde and phenylacetaldehyde, trapped both pollinators and florivores. Other compounds attracted either pollinators or florivores. Florivores of C. arvense appear to use floral scent compounds as kairomones; by advertising to pollinators, C. arvense also attracts its own enemies.
Abstract. Herbivores affect plants through direct effects, such as tissue damage, and through indirect effects that alter species interactions. Interactions may be positive or negative, so indirect effects have the potential to enhance or lessen the net impacts of herbivores. Despite the ubiquity of these interactions, the indirect pathways are considerably less understood than the direct effects of herbivores, and multiple indirect pathways are rarely studied simultaneously. We placed herbivore effects in a comprehensive community context by studying how herbivory influences plant interactions with antagonists and mutualists both aboveground and belowground. We manipulated early-season aboveground herbivore damage to Cucumis sativus (cucumber, Cucurbitaceae) and measured interactions with subsequent aboveground herbivores, root-feeding herbivores, pollinators, and arbuscular mycorrhizal fungi (AMF). We quantified plant growth and reproduction and used an enhanced pollination treatment to determine if plants were pollen limited. Increased herbivory reduced interactions with both antagonists and mutualists. Plants with high levels of early herbivory were significantly less likely to suffer leaf damage later in the summer and tended to be less attacked by root herbivores. Herbivory also reduced pollinator visitation, likely due to fewer and smaller flowers, and reduced AMF colonization. The net effect of herbivory on plant growth and reproduction was strongly negative, but lower fruit and seed production were not due to reduced pollinator visits, because reproduction was not pollen limited. Although herbivores influenced interactions between plants and other organisms, these effects appear to be weaker than the direct negative effects of early-season tissue loss.
Mutualists and antagonists may place conflicting selection pressures on plant traits. For example, the evolution of floral traits is typically studied in the context of attracting pollinators, but traits may incur fitness costs if they are also attractive to antagonists. Striped cucumber beetles (Acalymma vittatum) feed on cucurbits and are attracted to several volatiles emitted by Cucurbita blossoms. However, the effect of these volatiles on pollinator attraction is unknown. Our goal was to determine whether pollinators were attracted to the same or different floral volatiles as herbivorous cucumber beetles. We tested three volatiles previously found to attract cucumber beetles in a factorial design to determine attraction of squash bees (Peponapis pruinosa), the specialist pollinators of cucurbita species, as well as the specialist herbivore A. vittatum. We found that 1,2,4-trimethoxybenzene was attractive to both the pollinator and the herbivore, indole was attractive only to the herbivore, and (E)-cinnamaldehyde was attractive only to the pollinator. There were no interactions among volatiles on attraction of squash bees or cucumber beetles. Our results suggest that reduced indole emission could benefit plants by reducing herbivore attraction without loss of pollination, and that 1,2,4-trimethoxybenzene might be under conflicting selection pressure from mutualists and antagonists. By examining the attraction of both mutualists and antagonists to Cucurbita floral volatiles, we have demonstrated the potential for some compounds to influence only one type of interaction, while others may affect both interactions and possibly result in tradeoffs. These results shed light on the potential evolution of fragrance in native Cucurbita, and may have consequences for yield in agricultural settings.
Many organisms face challenges in avoiding predation while searching for mates. For plants, emitting floral fragrances to advertise reproductive structures could increase the attraction of detrimental insects along with pollinators. Very few studies have experimentally evaluated the costs and benefits of fragrance emission with explicit consideration of how plant fitness is affected by both pollinators and florivores. To determine the reproductive consequences of increasing the apparency of reproductive parts, we manipulated fragrance, pollination, and florivores in the wild Texas gourd, Cucurbita pepo var. texana. With enhanced fragrance we found an increase in the attraction of florivores, rather than pollinators, and a decrease in seed production. This study is the first to demonstrate that enhanced floral fragrance can increase the attraction of detrimental florivores and decrease plant reproduction, suggesting that florivory as well as pollination has shaped the evolution of floral scent.
By increasing floral apparency to promote fertilization, plants risk attracting herbivores with the same signals that they use to lure pollinators. We hypothesized that fragrance is emitted in patterns that correspond to pollinators, with high emissions during periods of pollinator activity and low emissions otherwise, especially during periods of peak floral herbivore activity. Using a combination of analytical chemistry and field observations, we examined both the diel and ontogenetic patterns of fragrance in two Cirsium species, in relation to visitation patterns of pollinators and florivores. Emission rates were highest at reproductive maturity, when insect visitation by both pollinators and florivores was also highest. In Cirsium arvense, the diel pattern of fragrance emission matched patterns of pollinator activity and was lowest when florivores were active. In contrast, scent in Cirsium repandum peaked at midday rather than with insect activity; neither species had a diel pattern that followed ambient temperature. Fragrance emission from C. repandum was 25 times lower than from staminate C. arvense and may not be essential for pollinator attraction, at least from a distance. The scent dynamics we observed in C. arvense are consistent with the hypothesis that fragrance emissions correspond with pollinator activity and are low when florivores are active.
We investigated postpollination changes in fragrance composition and emission rates, as well as pollinator discrimination in hand-pollinated flower heads of two thistle species: Canada thistle (Cirsium arvense) and sandhill thistle (C. repandum). Following pollination, neither species emitted any novel compounds that could function as repellents. Scent emission rates declined in pollinated plants of both species by approximately 89% within 48 hr. This decline was evident in all 13 scent components of C. arvense. Apis mellifera, the dominant pollinator in the study population of C. arvense, was nearly three times more likely to visit an unpollinated rather than a pollinated flower head. A more complex pattern was observed for C. repandum, whose scent comprised 42 compounds. Quantities of aromatic and sesquiterpenoid volatiles declined after pollination, whereas two classes of scent compounds, fatty acid derivatives and monoterperpenoids, continued to be emitted. In C. repandum, discrimination against pollinated flower heads by Papilio palamedes (its primary pollinator) was not as marked. Unpollinated control plants of both species maintained moderate levels of scent production throughout this experiment, demonstrating that senescence and floral advertisement may be delayed until pollination has occurred. We expect postpollination changes in floral scent contribute to communication between plants with generalized pollinator spectra and their floral visitors. This study provides the first field study of such a phenomenon outside of orchids.
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