By Hanna Francis, Biological Sciences ’22
Author’s Note: I grew interested in plants through botany and plant biochemistry courses at UC Davis and learned about insects while volunteering at the Bohart Museum of Entomology on campus. After taking a course about the toxicology of air pollutants, which focused primarily on human health outcomes, I began to wonder how air pollution affects organisms other than ourselves. In investigating current research at the intersection of these three things– plants, insects, and air pollution– I found that plant-pollinator interactions are affected by ozone pollution in a variety of ways, some of which may be harmful to agriculture and biodiversity. I hope that readers will become aware of just how complex the effects of pollution are on the natural world. The paper may at first seem bleak, however, there must always be hope. I truly believe that research like this will help inform regulatory standards for air pollution that will protect both humans and our environment from damage in the future.
The concentration of ozone (O3) in the earth’s atmosphere has increased dramatically due to industrialization and is predicted to increase by two- to four-fold over the next twenty years [1,2]. Human activity, especially in the form of transportation and manufacturing, emits pollutants such as nitrogen oxides (NOx), which react with oxygen and UV light in the atmosphere to form ozone [3,4]. Ozone is a highly reactive gas known to lead to human lung diseases such as asthma , but its effects on other organisms are not as well understood.
Pollination– a process vital to agriculture– is reliant upon insects and plants, so it is crucial to understand the effects of ozone pollution on this process . Insect pollination is necessary for over 80% of global crops . In addition to agricultural plants, wild plant species have also been shown to be sensitive to ozone and studies have found ozone to be associated with a loss in wild species diversity . Recent research has focused on the ways in which ozone pollution may interrupt plant-insect interactions during pollination. This review aims to explain and categorize current knowledge about the various ways in which increased levels of ozone in the atmosphere may impact the process of pollination. I focused on studies which investigated the effects of ozone exposure on flowering plants or insects during pollination. It is clear that exposure to ozone in insect pollinators can lead to changes in mobility , behavior [1,2], and perception of volatile organic compounds, which plants release for signaling and communication . There is also evidence that when plants are exposed to ozone, their reproductive performance , visual features , and signaling compounds are affected [9,10]. However, it is unclear if ozone pollution will have a significant enough impact on pollination to negatively impact agricultural yields and the survival of wild plants.
Ozone Exposure to Plants:
Effects on Plant Visual Traits
There are a variety of effects of ozone on the visual features of plants that may impact pollination, including anatomical and chemical changes . One recent study exposed
an endangered species of alpine geranium called Erodium paularense to ozone. The scientists measured the petal area and the spectral reflectance, which is the ratio of the amount of light reflected off of a surface to the amount of light that hit the surface . Using the spectral reflectance, an anthocyanin reflectance index was calculated, which estimates the content of anthocyanins (blue, purple and red pigments) in each petal. Changes in anthocyanin content would change the perceived color of the flower to pollinators . The study found no significant difference in petal area after ozone fumigation, but ozone exposure did increase petal reflectance. Plants that were exposed to ambient levels of O3 had a significantly higher anthocyanin reflectance index than other treatments. The differing reflectances mean that some insects, such as flies, would see the O3-treated plants as more blue than before, though the effect was not large enough for there to be any difference in the perceived color for butterflies and bees, based on models . This study demonstrates that ozone has a measurable effect on the visual attraction of flowers, which has implications for pollination efficiency in agriculture as well as for endangered wild plants like Erodium paularense.
Effects on Volatile Organic Compounds
Ozone has a strong potential to react with and disrupt VOCs, which plants release for signaling and communication . Plants use various VOCs in order to attract insect pollinators, so any reactions these compounds may undergo in the atmosphere could affect the ability of insects to locate and pollinate plants . A study tested how different concentrations of ozone affect the floral scent of black mustard plants, Brassica nigra, and how the scent changes affect bumblebee behavior . Flowers were placed into a system of tubes in which the floral compounds were exposed to three different concentrations of O3. The floral emissions were then collected at four different distances from the flower. Bees were given the choice between two tubes that visually mimicked mustard inflorescences, each containing either clean air or the VOCs of varying O3 exposure and collection distance . The study found that the ozone concentration negatively affected the concentration of VOCs in the glass tube. In the behavioral experiments, bees showed a preference for ozone-exposed floral scents at shorter distances rather than longer distances. The results indicate that ozone concentration, ozone exposure, and distance from the scent source all affected bumblebee behavior . Another study conducted research on the degradation of VOCs in which rapeseed (Brassica napus) flowers were exposed to ozone. Measurements of VOCs were taken at several timepoints after O3 fumigation . The study found that ozone exposure led to a decrease in monoterpenes and sesquiterpenes (VOCs that contain alkenes) and an increase in many oxygenated species, which are formed when VOCs react with ozone. It was concluded that because monoterpenes and sesquiterpenes are very important in plant-insect signaling, there could be a significant negative impact on this signaling during pollution episodes . Together, these studies demonstrate how ozone negatively affects chemical compounds released from plants and that these changes affect the behavior of pollinators.
Figure 1. Floral compounds were exposed to varying concentrations of ozone and then collected at one of four different distances from the ozone source (ozone generator): Distance 0, 1, 2, and 3.
Figure 2. Bees were given the choice between two tubes that visually mimicked mustard inflorescences (shown in green and yellow). The tubes contained either clean air or VOCs of varying ozone exposure and collection distance.
Effects on Plant Reproduction
The impacts of O3 exposure on the visual and chemical traits of plants may lead to differences in plant reproductive performance. One study investigates whether plant age at the time of exposure impacts reproduction . After wild mustard plants (Sinapis arvensis) were exposed to heightened ozone concentrations at various stages of life, plant reproduction was quantified by measuring the number of seeds produced, seed weight, number of total fruits, and number of visitations by pollinator insects. The study found that the plants were affected differently by O3 depending on the age at which they were exposed. Younger plants (3 and 4 weeks old) tended to have increased reproductive performance (more fruits, more seeds, and higher seed weight than control). In contrast, plants that were exposed later in life had reduced reproductive performance, though this effect was only significant in the total seed weight in plants exposed at 5 weeks old. Overall, the study concluded that younger plants respond to ozone treatment by initiating higher investment in flower production and reproduction, whereas older plants are not as flexible and have decreased reproductive capabilities due to stress response . Understanding how pollution episodes at different life stages could change crop yield is of great interest to agriculture, and may impact crop management strategies in the future.
Ozone Exposure to Insects:
Effects on Insect Motility and Behavior
Research has demonstrated that insects that have been exposed to ozone show negative health effects and changes in behavior, which may impact their ability to successfully pollinate host plants [1,2]. In one recent study, fig wasps were exposed to various O3 concentrations in fumigation chambers and their behavior was recorded at different time intervals afterward . There was a significant deviation in motility behavior after exposure to O3. Specifically, there was a significant decrease in activity from control in wasps exposed to high levels of ozone (120 and 200 ppb) . In a similar study, fig wasps were exposed to differing concentrations of O3 and given a choice between two stems of a Y-tube: one with a fresh air control and one with a mixture of VOCs that mimicked those of the wasps’ host plant . Fig wasps that had been exposed to lower concentrations (80 ppb) of ozone significantly preferred the VOCs, those that had been exposed to an intermediate concentration (120 ppb) showed no preference, and the wasps that had been exposed to the highest concentration (200 ppb) of ozone had a significant preference for the clean air over the VOCs . These results suggest that the higher levels of ozone impaired the wasps’ ability to distinguish VOCs from clean air, or made the VOCs no longer attractive to the insects. Decreased mobility and ability to locate host plants could dramatically reduce the effectiveness of pollinators.
Effects on Insect Perception of VOCs
There is potential for biochemical changes to occur within insects that could alter their sensing abilities. One study exposed fig wasps and bumblebees to varying O3 concentrations and lengths of time in fumigation chambers . After exposure, electroantennograms (EAGs), a method of measuring the electrical response of an antenna to a scent , were measured in order to evaluate the insects’ sensitivity to different VOCs. There was a clear negative relationship between O3 exposure and the ability of pollinators to respond to and detect volatile organic compounds. However, many results were not significant and the responses depended on factors including species, the specific VOC, ozone concentration, and exposure time . Further effects of ozone on insect perception of plant compounds were examined in a study which used western honeybees, a species that is important to agriculture worldwide . The honeybee antennae were mounted into an airflow system in which they were stimulated with different sequences of control paraffin, O3, and three VOCs . Responses were measured using EAG recording devices. One of the three compounds, (Z)-3-hexenyl acetate, showed a significant decrease in antennal responses in the O3 treatment group compared to the control group . These results show that ozone can cause significant effects on antennal response to some VOCs. Therefore it may be worthwhile to test the effects of various ozone concentrations on other VOCs beyond those that were tested in this study. Impaired responses to plant compounds could potentially be detrimental to pollination, which could have far-reaching impacts for wild plant populations as well as for agriculture.
Understanding how and to what extent ozone impacts plant-insect pollination interactions are active areas of research. Further experimentation will help to solidify understanding of the severity of the threat of ozone to agricultural systems and wild plants. Future directions of research include the difference between short-term high-concentration ozone pollution episodes versus long-term exposure to ambient ozone levels. The mechanisms of action of ozone interference with plant and insect biochemistry are also largely unknown . Despite remaining questions, it is clear that there are many ways in which pollination is negatively affected by ozone exposure. Some of these effects are nearly imperceptible even at unrealistically high experimental concentrations of ozone [4,8], meaning that they may not be relevant to real-world scenarios. For example, one study used concentrations of 1000ppb, despite current ozone concentrations not usually exceeding 100ppb . Nevertheless, ozone is a threat to both agriculture and to the biodiversity of wild plants .
In addition to further research, there are ways in which current knowledge can already be applied. Data from studies such as the ones included in this review can inform air pollution standards . Reducing NOx emissions, which are primarily anthropogenic in source (about half come from fossil fuel combustion, and a further 20% from other combustion done by humans) would be beneficial in reducing or at least maintaining ozone levels .
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