Degradation of Odour signals by air pollution: chemical Mechanisms, plume dynamics and INsect-Orientation behaviour (DOMINO)

Lead Research Organisation: University of Reading
Department Name: Sch of Agriculture Policy and Dev

Abstract

This project will investigate the mechanisms by which air pollution can disrupt vital airborne chemical signals that insects use for critical processes, such as mating or finding a flower, and will evaluate the ecological consequences of this phenomenon.

Air pollution is a global issue that regularly hits the front pages of newspapers. Despite tough legislation, pollution levels in many areas remain above the legal limits. For example, multiple locations in London breached annual limits for the traffic-produced gas nitrogen dioxide within the first week of January 2016. Exceeding these limits not only poses major risks for human health, but also leads to substantial EU imposed fines for the UK. In developing nations the problem can be even greater. For example, in December 2015 China issued its second ever "red alert" for air pollution in Beijing, resulting in restrictions on vehicle use and the closure of schools. Air pollution, however, is not limited to large industrialised cities. Rural areas are also regularly exposed to pollution transported from cities and major roadways and are increasingly impacted by ozone pollution due to both a rise in the global background and regular weather-induced episodic ozone peaks often referred to as ozone bubbles. One such episode was triggered during the August 2003 heat wave and is thought to have resulted in 2139 deaths in England and Wales.

Concerns over public health have driven current efforts to reduce air pollution, but there is strong evidence to suggest that the health of plants and insects are also at risk. The honey bee for example, finds food by following the unique blend of volatile organic compounds (VOC) emitted by flowers. However, we and others have recently demonstrated in laboratory experiments that common air pollutants, such as diesel exhaust and ozone, can disrupt these floral odours, but we do not yet understand what consequences this might have in the real-world. Nonetheless, it is clear that any disruption to these signals may have wide ranging and as yet unquantified impacts on the important ecosystem services they provide, such as pollination (estimated to be $361bn globally and £691m in the UK) and pest-regulation ($417bn globally).

This project will result in a step-change in our knowledge of this subject by radically advancing our conceptual understanding of how air pollution interacts with the VOCs that many insects rely on to communicate and interact with their environment.

Initially we will conduct studies to provide comprehensive evidence of how a range of key air pollutants (nitrogen dioxide, nitrate radicals and ozone) in isolation and in combination, react and interact with a series of selected VOCs, which function as either floral attractants or pheromones. We will then establish which products of these reactions a pair of model insects, the silver y moth and the buff-tailed bumblebee, are capable of detecting. Next, we will for the first time measure how degradation occurs spatially within odour plumes at time scales relevant to atmospheric mixing processes and insect navigation. Finally, we will use these data to: (i) quantify the effects of diesel exhaust (a major contributor to nitrogen dioxide pollution) and ozone pollution on the ability of male moths to locate females and pollinators to locate and pollinate flowers in field studies; and (ii) establish the effects of odour degradation in the plume on in-flight orientation behaviour of moths flying to the selected VOCs in a wind tunnel. This will provide us with a significantly advanced erudition of the mechanisms by which pollutants can degrade volatile odours used by insects and the effects that this has on insect behavioural ecology and the vital ecosystem service of pollination.

Planned Impact

This multidisciplinary research project will be of interest to a wide range of researchers, practitioners, organisations and the general public. This is a very novel area of research, therefore precise quantification of possible impacts poses a challenge. However, we have identified four key stakeholder groups with the potential to directly benefit from the planned research:

1. NGOs: A number of non-governmental organisations may benefit from the outcomes of the project, particularly wildlife and conservation organisations. Insects are a critical part of all terrestrial and freshwater ecosystems and are required for healthy ecosystem functioning and the maintenance of biodiversity. This project will provide information on how air pollution may interfere with insect ecology. This will be used to provide actionable insights for wildlife and conservation organisations in planning and developing conservation strategies, which will impact upon the management of wildlife reserves.

2. Practitioners: The two main sub-divisions of practitioners who will benefit from the research are: (i) beekeeper groups, and (ii) producers and advisors. The value of insect pollination to UK agriculture is estimated at £691M p.a. (2011). Under current agricultural practices, honey bees play a vital role in global production of pollinated crops, e.g. in the United States pollination by honey bees is estimated to be worth $11.68bn, 3 times the value of wild pollination. Using, field studies, this project will provide the first ever estimate of the effects of odour signal degradation on the ability of insects to provide pollination services and therefore the potential scale of this problem for practitioners. The outcomes of the research will be used to design and provide advisories for beekeepers on how best to manage pollinators to reduce impacts of air pollution, with respect to siting of hives. It will benefit producers/advisors, by providing information on how to enhance pollination services by taking into account the potential impacts of air pollution.

3. Policy makers: The project will play a significant contribution in shaping policy, both nationally and internationally. There is currently great political interest and debate relating both to the wider environmental and health impacts of air pollution, and to declines in pollinator populations and wider biodiversity. The outcomes of this project will be used to inform both debates and influence future policy. At national level Defra's recent National Pollinator Strategy and associated Implementation Plan are critical policy implements, but currently the effects of air pollution interrupting odour communication are not featured because there is insufficient evidence and very limited understanding of field scale effects. This project will provide that lacking evidence and thus have a major influence on future policy, for example by contributing actionable outcomes from the project to influence package design for the Countryside Stewardship Scheme to greater benefit pollinator communities.

4. General public: The recent VW emissions scandal garnered much attention in the mainstream media and has brought air quality issues to the forefront of public awareness, meaning the subject of this research project will resonate strongly. Furthermore, there is already significant public interest in pollinator and biodiversity declines. In 2010 it was estimated that nearly 6k people died prematurely in London alone as a result of NOx pollution. The public will benefit from this research because it is very likely to provide increased political pressure to ensure that current air pollution legislation is rigorously enforced and tightened. Additionally, because those ecosystem services that pollinators and other insect groups provide sustain the production of high value nutritious foods the positive impacts of this project for practitioners in food production will also have direct benefits on UK consumers.
 
Description This aim of this project was to investigate the mechanisms by which air pollution can disrupt vital airborne chemical signals that insects use for critical processes, such as mating or finding a flower, and to evaluate the ecological consequences of this phenomenon. For this ambitious project we conducted research on: i) the impacts of two ubiquitous air pollutants, nitrogen oxide (NOx) and ozone, on the chemistry and structure of airborne chemical signals/cues that insects use to locate resources when foraging, and ii) the impacts of diesel exhaust (principally NOx) and ozone on the ecology and behaviour of foraging insects.

In order to investigate the impacts of pollutants on the airborne structure of volatile chemical signals, our primary objective was to determine the temporal and spatial evolution of plumes of key volatile organic compounds (VOCs) and their reaction products during exposure to ozone. A series of controlled studies were undertaken within the NERC EnFlo wind tunnel facility to determine: i) whether the degradation of a reactive monoterpene (alpha terpinene) plume follows that predicted by laboratory derived rate constants; ii) how the structure of the plume varies spatially, and; iii) how the ratios of a blend of VOCs change spatially upon exposure to ozone. These successful studies have revealed that alpha terpinene concentrations decayed at a rate faster than that predicted by the literature rate constants. This was contrary to expectation, because it is assumed that reaction rates would be slower within a real-world plume due to incomplete mixing. A further key finding was that the rate of degradation was not consistent throughout the plume, with reaction rates 30% faster at the edge of the plume compared to the plume centre. This result indicates that oxidants not only reduce the overall lifetime of floral VOCs but also limit the spatial extent of the plume.

For our studies on the impacts of diesel exhaust and ozone pollutants on the ecology, behaviour and physiology of foraging insects, we pioneered the design and construction of the first ever Free-Air Diesel and Ozone Enrichment (FADOE) fumigation facility. The facility allowed experiments to be conducted on the ecological impacts of air pollution in the field, which had not previously been attempted. The experiments we conducted using this facility exceeded our initial expectations and offered new insight into the broader impacts of air pollution on insect ecology. We quantified the effects of diesel exhaust and ozone pollution on free-living pollinating insects, with controlled field-based studies, using pan trapping and observational flower visitation experiments within the FADOE fumigation rings. These experiments provided the first ever evidence of the substantial negative field-scale effects of diesel exhaust and ozone pollution (at concentrations commonly recorded in the lower troposphere) on insect-mediated pollination services. These pollutants, individually and in combination, significantly reduced pollinator counts and flower visits, of our study plant (Brassica nigra), by at least 62% and 83%, respectively. These reductions, which were consistent over two years, were driven by responses of major pollinator groups (honeybees, bumble bees, solitary bees and hoverflies) and coincided with significant decreases in pollination and yield metrics.

To investigate the behavioural mechanisms behind the changes we observed in pollinator behaviour during the FADOE experiments, we conducted odour plume recognition studies using honeybees. The aim of these experiments was to assess whether honeybees could recognise and respond to the degree of changes in the ratio of VOCs that is predicted to occur in an odour plume moving through an ozone polluted environment. The ratios used in these studies were identified based upon the changes in VOC ratios observed at three distances from the source of VOC release (2, 6 and 12 m) in the EnFlo wind-tunnel studies. Honeybees were trained to recognise the ratio that they would encounter at the plume source and subsequently tested to see whether they recognised modified VOC ratios that mimicked those ratios that they would encounter at the different distances from the source under ozone pollution. Results showed that the percentage of honeybees that recognised the altered ratios of VOCs decreased dramatically with only 10% recognising the blend that represented 12 metres from the source at 140ppb of ozone. This suggests that ozone may dramatically reduce recognition of odour plumes even over relatively short distances and may provide an explanation for the changes in pollination services we observed during the FADOE studies.

In summary, the results of this project are particularly concerning in that, when considered at a field scale and when investigating odour degradation in plumes that are more representative of those insects would encounter, the impacts of air pollution on insect floral foraging behaviour appears to be more dramatic and potentially more damaging than had initial been predicted from small-scale laboratory assays and atmospheric modelling. This research adds to a growing body of evidence about the effects of air pollution on insect foraging and has raised new questions and concerns about the ubiquity of such impacts on other critical chemically-mediated foraging behaviours and the ecosystem services provided by other insect groups.
Exploitation Route It is clear from the outputs of this project that further research is required to provide a robust understanding of the broader impacts that air pollution may have on insect biodiversity and other ecosystem services which rely upon insects successfully completing chemically-mediated interactions. On the basis of the results of our FADOE studies, funding was secured for a permanent FADOE facility based at the University of Reading. The use of this facility is open to the wider scientific community and will facilitate research on the subject area. This is an emerging research field and therefore, requires a growing body of scientific evidence to provide a significant influence on key stakeholders, for example NGOs (such as wildlife and conservation organisations) practitioners (such as beekeeper groups and agricultural producers) and policy makers. Research from this project has contributed to an increased awareness of the potentially deleterious effects of air pollution on insect ecology. On the back of this growing wave of research there have recently been major investments internationally in this field. It is by providing evidence as an international research community that we will be able to make real impact and encourage policy change on a national and international level.
Sectors Agriculture, Food and Drink,Environment,Government, Democracy and Justice

 
Description 2020 Research Fellowship
Amount £806 (GBP)
Organisation University of Reading 
Sector Academic/University
Country United Kingdom
Start 03/2018 
End 09/2018
 
Description A novel Free-Air Diesel and Ozone Enrichment (FADOE) research platform
Amount £193,121 (GBP)
Funding ID NE/T009012/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2019 
End 03/2020
 
Description Deciphering how common air pollutants impact on pest regulation services
Amount £32,612 (GBP)
Organisation University of Reading 
Sector Academic/University
Country United Kingdom
Start 03/2020 
End 07/2021
 
Description Does air pollution inhibit the recruitment of plant bodyguards?
Amount £19,713 (GBP)
Funding ID LRB18/1009 
Organisation British Ecological Society 
Sector Charity/Non Profit
Country United Kingdom
Start 05/2018 
End 11/2019
 
Description Investigating the Impact of Volatile Organic Compounds Released by Plants in Response to Biotic and Abiotic Stressors under ambient and elevated CO2 conditions (VOC-Plant-Stress-CO2)
Amount £67,500 (GBP)
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 09/2019 
End 09/2022
 
Description NERC SCENARIO Studentship: Love isn't in the air: Assessing how air pollution interrupts insect sex pheromone signalling - Georgia England
Amount £0 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 10/2020 
End 09/2024
 
Description The effects of two common air pollutants (diesel exhaust and ozone) on plant VOC mediated Interactions
Amount € 95,000 (EUR)
Organisation Finnish Cultural Foundation 
Sector Charity/Non Profit
Country Finland
Start 09/2020 
End 08/2022
 
Description The little things that run a polluted world
Amount £104,000 (GBP)
Funding ID ECF-2020-017 
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 02/2021 
End 12/2023
 
Title EnFlo Wind-Tunnel PTR Data 
Description PTR-MS, FFID and Anemometer data of the degradation of common floral VOCs under different ozone conditions. This data when complete will be uploaded to a relevant data archive. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? No  
Impact N/A 
 
Description Academy of Finland project with James Blande 
Organisation University of Eastern Finland
Department Department of Environmental Science
Country Finland 
Sector Academic/University 
PI Contribution I am an advisor to an Academy of Finland funded research project investigating stress induced changes to floral volatile bouquets and the effects of atmospheric pollutants on pollinator foraging. This will integrate with work we are conducting as part of our NERC-funded DOMINO project. For this collaboration I will be providing advice and guidance on the use of methods that we are developing in the DOMINO project and methods that we have developed in this area on previous research projects. I will host a post-doc funded on this project at the University of Reading to provide them with training and will also spend time during the summer of 2018 at the University of Eastern Finland to provide additional training.
Collaborator Contribution The research project was initiated and devised by Dr James Blande of the University of Eastern Finland. I was asked to be a named collaborator on this project to allow cross-learning between the project and our DOMINO project. The majority of the research for this project with be conducted by the researchers in Finland.
Impact None as of yet
Start Year 2018
 
Description Air Pollution and Atmospheric Chemistry Seminar by Dr Christian Pfrang at the University of Birmingham on 11th September 2020 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Air Pollution and Atmospheric Chemistry Seminar by Dr Christian Pfrang at the University of Birmingham on 11th September 2020 on a range of his research activities including the work on air pollution impact on insect communication as well as the work on levitated aerosols and monolayer ageing.
Year(s) Of Engagement Activity 2020
 
Description NERC Council invited speaker 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Policymakers/politicians
Results and Impact I was invited to present the research from my NERC DOMINO project to the NERC Council as a pre-dinner speaker at their quarterly meeting. This sparked a lot of discussion and questions on how this work might be used to influence current air pollution policy.
Year(s) Of Engagement Activity 2020
 
Description New Scientist Article 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact I was interviewed by New Scientist about my research, along with my collaborator on the DOMINO project Dr Ben Langford (CEH Edinburgh), to discuss our research in the field and what we had planned for the DOMINO studies. A 3-page article was published in New Scientist, which highlighted our research alongside that of other leading researchers in the field.
Year(s) Of Engagement Activity 2018
URL https://www.newscientist.com/article/mg23731650-200-dirty-talk-how-pollution-is-snuffing-out-plants-...
 
Description Open Farm Sunday at Sonning Farm 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact In 2018, the University of Reading participated in Open Farm Sunday on 10 June at their Sonning Farm site. This national event is an opportunity for UK farms of all kinds top open their doors to local residents and show them what farming is all about. This is where our Free Air Diesel and Ozone Enrichment (FADOE) experiment is situated and during the open day it was demonstrated to all attendees.
Year(s) Of Engagement Activity 2018
URL http://www.reading.ac.uk/about-eventreg-openfarmsunday.aspx
 
Description Poster at the BES 2019 annual conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact A poster was presented to attendees of the conference titled :"Does air pollution inhibit the recruitment of plant bodyguards?" by the following authors:

Lisa Bromfield - Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK
Robbie Girling - Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK
James Blande - Department of Environmental and Biological Sciences, University of Eastern Finland, Kuopio, Finland
James Ryalls - Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK
Year(s) Of Engagement Activity 2019
URL https://www.britishecologicalsociety.org/events/annual-meeting-2019/
 
Description Presentation at BES 2019 annual meeting in Belfast by James Ryalls 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact A presentation was made at the BES Annual conference in Belfast titles "Field-scale effects of elevated ozone and diesel exhaust emissions on insect pollination and natural enemy recruitment"

James Ryalls - Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK
Neil Mullinger - Centre for Ecology and Hydrology, Edinburgh, Bush Estate, Penicuik, Midlothian, UK
Ben Langford - Centre for Ecology and Hydrology, Edinburgh, Bush Estate, Penicuik, Midlothian, UK
Eiko Nemitz - Centre for Ecology and Hydrology, Edinburgh, Bush Estate, Penicuik, Midlothian, UK
Christian Pfrang - School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, UK
Robbie Girling - Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK

This led to requests from other academics at the conference to conduct future collaborations with our research facilities and building on the DOMIN and FADOE projects.
Year(s) Of Engagement Activity 2019
URL https://www.britishecologicalsociety.org/events/annual-meeting-2019/
 
Description Presentation at the Association for Science Educators Annual Conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I was an invited speaker at the 2020 Association for Science Education (ASE) annual conference to perform a Frontier Science lecture to inform science educators from across Europe of cutting edge research. My talk was entitled "Mixed messages: how air pollution scrambles floral smells, confusing pollinators." and was based upon the outcomes of my NERC DOMINO project. After my talk a number of educators from across Europe asked for copies of my slides to present to their School aged students.
Year(s) Of Engagement Activity 2019
URL https://aseannualconference2020.sched.com/
 
Description Radio 4 Farming Today Interview on 25/8/2018 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Dr James Ryalls and Dr Robbie Girling were interviewed by BBC Radio 4 farming today on the 25/8/2018 discussing our field trials on the NERC-funded DOMINO research project at Sonning Farm. This radio show has a listenership of approximately 1 million listeners.
Year(s) Of Engagement Activity 2018
 
Description Talk and organisation of special session at International Society of Chemical Ecology Meeting 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact I organised a themed session at the ISCE 2019 Annual Meeting (Atlanta, GA USA, June 2- 6, 2019), entitled: "Anthropogenic Impacts on Chemical Cues, Signals and Chemoreception"

During this session I presented a talk to approximately 100 attendees at the conference based on work conducted during DOMINO called "Field assessments of the effects of elevated ozone and diesel exhaust emissions on insect pollination services"
Year(s) Of Engagement Activity 2019
URL https://isce2019.biosci.gatech.edu/