Effects of ozone stress on flowering phenology, plant-pollinator interactions and plant reproductive success

Tropospheric ozone is a highly oxidative pollutant with the potential to alter plant metabolism. The direct effects of ozone on plant phenotype may alter interactions with other organisms, such as pollinators, and, consequently, affect plant reproductive success. In a set of greenhouse experiments, we tested whether exposure of plants to a high level of ozone affected their phenological development, their attractiveness to four different pollinators (mason bees, honeybees, hoverflies and bumblebees) and, ultimately, their reproductive success. Exposure of plants to ozone accelerated flowering, particularly on plants that were growing in autumn, when light and temperature cues, that commonly promote flowering, were weaker. Simultaneously, there was a tendency for ozone-exposed plants to disinvest in vegetative growth. Plant exposure to ozone did not substantially affect pollinator preference, but bumblebees had a tendency to visit more flowers on ozone-exposed plants, an effect that was driven by the fact that these plants tended to have more open flowers, meaning a stronger attraction signal. Honeybees spent more time per flower on ozone-exposed plants than on control plants. Acceleration of flower production and the behavioural responses of pollinators to ozone-exposed plants resulted in retained reproductive fitness of plants pollinated by bumblebees, honeybees and mason bees, despite the negative effects of ozone on plant growth. Plants that were pollinated by hoverflies had a reduction in reproductive fitness in response to ozone. In a natural setting, acceleration of flowering by ozone might foster desynchronization between plant and pollinator activities. This can have a strong impact on plants with short flowering periods and on plants that, unlike wild mustard, lack compensatory mechanisms to cope with the absence of pollinator activity in the beginning of flowering.