Dosage-Dependent Impacts of a Floral Volatile Compound on Pollinators, Larcenists, and the Potential for Floral Evolution in the Alpine SkypilotPolemonium viscosum

Abstract

All volatile organic compounds (VOCs) vary quantitatively, yet how such variation affects their ecological roles is unknown. Because floral VOCs are cues for both pollinators and floral antagonists, variation in emission may have major consequences for costs and benefits in plant-pollinator interactions. In Polemonium viscosum, the emission rate for the floral VOC 2-phenylethanol (2PE) spans more than two orders of magnitude. We investigated the ecological and evolutionary impacts of this immense phenotypic variation. The emission rate of 2PE varies independently of nectar rewards and thus is uninformative of profitability. Emission is elevated in flowers that are morphologically vulnerable to ant larcenists, suggesting that chemical deterrence may compensate for weak physical barriers. In nature, plants emitting more 2PE than their neighbors escape ant damage. Flower-damaging ants die when exposed to 2PE in the laboratory, and they avoid high 2PE emitters in the field. High 2PE also reduces bumblebee visitation and pollination, suggesting an ecological cost of defense in pollinator service. However, at more moderate emission rates, 2PE enhances the amount of nectar left in flowers, at no pollination cost. In conclusion, repellency of 2PE is highly sensitive to dosage, giving it a key role in shaping ecological interactions between skypilot plants and their floral visitors.

Natural selection on floral volatile production inPenstemon digitalis: Highlighting the role of linalool

“…Moreover, as scent sampling methods, chemical analyses and data handling of the large data sets produced by measuring scent bouquets advance, [27][28][29] large-scale field-based ecological experiments are becoming more attainable. 6,[30][31][32] Thus, future floral evolutionary research will likely increasingly incorporate scents to understand how integrated floral phenotypes evolve.…”

Passive partner choice through exploitation barriers

“…Exploitation barriers allow flowers to filter out some undesired visitors: short-tongued nectar feeders do not reach the nectar hidden at the bottom of long corolla tubes (Harder 1985), small bees are not able to open personate and keel flowers (Bohart 1957;Lebuhn and Anderson 1994) and many pollinators are unable to harvest the pollen of poricidal anthers (Buchmann et al 1983;Thorp 2000). But exploitation barriers can also be subtle traits, such as colour (Raven 1972;Rodríguez-Gironés and Santamaría 2004) and fragrance (Galen et al 2011)-because a change in colour or scent can make flowers more difficult to detect. In this paper we present a general framework to study the evolution of exploitation barriers, generalising a previous model investigating the conditions under which barriers that impose costs to effective pollinators can evolve (Rodríguez-Gironés and Santamaría 2005).…”

The raison d'être of chemical ecology

“…However, more generalized plant-pollinator interactions tend to be mediated by generic volatiles that are innately attractive to diverse groups of pollinators, or are easily learned by them in association with nectar-or pollen-based floral resources (Raguso 2008). Furthermore, the diversity of visitors to generalized flowers appears to select for multifunctional compounds (volatile or not) that simultaneously repel enemies and attract pollinators or adaptively modify their behavior (Galen et al 2011, Kessler et al 2012b. Multifunctionality is emerging as one of the most important and common attributes of natural products, which is surprising in the light of their great structural diversification.…”