Anthropogenic air pollutants reduce insect-mediated pollination services

Article

Ryalls, James M.W., Langford, Ben, Mullinger, Neil J., Bromfield, Lisa M., Nemitz, Eiko, Pfrang, Christian and Girling, Robbie D.. 2022. "Anthropogenic air pollutants reduce insect-mediated pollination services." Environmental Pollution. 297, p. 118847. https://doi.org/10.1016/j.envpol.2022.118847
Article Title

Anthropogenic air pollutants reduce insect-mediated pollination services

ERA Journal ID5823
Article CategoryArticle
AuthorsRyalls, James M.W., Langford, Ben, Mullinger, Neil J., Bromfield, Lisa M., Nemitz, Eiko, Pfrang, Christian and Girling, Robbie D.
Journal TitleEnvironmental Pollution
Journal Citation297, p. 118847
Number of Pages7
Year2022
PublisherElsevier
ISSN0269-7491
1873-6424
Digital Object Identifier (DOI)https://doi.org/10.1016/j.envpol.2022.118847
Web Address (URL)https://www.sciencedirect.com/science/article/pii/S0269749122000616
AbstractCommon air pollutants, such as nitrogen oxides (NOx), emitted in diesel exhaust, and ozone (O3), have been implicated in the decline of pollinating insects. Reductionist laboratory assays, focused upon interactions between a narrow range of flowering plant and pollinator species, in combination with atmospheric chemistry models, indicate that such pollutants can chemically alter floral odors, disrupting the cues that foraging insects use to find and pollinate flowers. However, odor environments in nature are highly complex and pollination services are commonly provided by suites of insect species, each exhibiting different sensitivities to different floral odors. Therefore, the potential impacts of pollution-induced foraging disruption on both insect ecology, and the pollination services that insects provide, are currently unknown. We conducted in-situ field studies to investigate whether such pollutants could reduce pollinator foraging and as a result the pollination ecosystem service that those insects provide. Using free-air fumigation, we show that elevating diesel exhaust and O3, individually and in combination, to levels lower than is considered safe under current air quality standards, significantly reduced counts of locally-occurring wild and managed insect pollinators by 62–70% and their flower visits by 83–90%. These reductions were driven by changes in specific pollinator groups, including bees, flies, moths and butterflies, and coincided with significant reductions (14–31%) in three different metrics of pollination and yield of a self-fertile test plant. Quantifying such effects provides new insights into the impacts of human-induced air pollution on the natural ecosystem services upon which we depend.
KeywordsAir pollution; Diesel exhaust ; Tropospheric ozone ; Floral odor cues ; Insect pollinators ; Ecosystem services
ANZSRC Field of Research 2020370102. Air pollution processes and air quality measurement
410204. Ecosystem services (incl. pollination)
310301. Behavioural ecology
310307. Population ecology
Byline AffiliationsUniversity of Reading, United Kingdom
UK Centre for Ecology & Hydrology, United Kingdom
University of Birmingham, United Kingdom
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Girling, Robbie D., Stewart-Jones, Alex, Dherbecourt, Julie, Staley, Joanna T., Wright, Wright and Poppy, Guy M.. 2011. "Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles." Proceedings of the Royal Society B: Biological Sciences. 278 (1718), pp. 2646-2653. https://doi.org/10.1098/rspb.2010.2725
Utilizing insect behavior in chemical detection by a behavioral biosensor
Fernández-Grandon, G., Girling, Robbie D. and Poppy, Guy M.. 2011. "Utilizing insect behavior in chemical detection by a behavioral biosensor." Journal of Plant Interactions. 6 (2-3), pp. 109-112. https://doi.org/10.1080/17429145.2010.544778
The lethal and sub-lethal consequences of entomopathogenic nematode infestation and exposure for adult pine weevils, Hylobius abietis (Coleoptera: Curculionidae)
Girling, R.D., Ennis, D., Dillon, A.B. and Griffin, C.T.. 2010. "The lethal and sub-lethal consequences of entomopathogenic nematode infestation and exposure for adult pine weevils, Hylobius abietis (Coleoptera: Curculionidae)." Journal of Invertebrate Pathology. 104 (3), pp. 195-202. https://doi.org/10.1016/j.jip.2010.04.003
Biology and Reproductive Behavior of Murgantia histrionica (Heteroptera: Pentatomidae)
Zahn, Deane K, Girling, Robbie D., McElfresh, J Steven, Cardé, Ring T. and Millar, Jocelyn G. 2008. "Biology and Reproductive Behavior of Murgantia histrionica (Heteroptera: Pentatomidae)." Annals of the Entomological Society of America: devoted to the interest of classical entomology. 101 (1), pp. 215-228. https://doi.org/10.1603/0013-8746(2008)101[215:BARBOM]2.0.CO;2
Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles
Girling, Robbie D., Madison, Rachael, Hassall, Mark, Poppy, Guy M. and Turner, John G.. 2008. "Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles." Journal of Experimental Botany. 59 (11), pp. 3077-3085. https://doi.org/10.1093/jxb/ern163
Behavioural responses of the seven-spot ladybird Coccinella septempunctata to plant headspace chemicals collected from four crop Brassicas and Arabidopsis thaliana, infested with Myzus persicae
Girling, R.D. and Hassall, M.. 2008. "Behavioural responses of the seven-spot ladybird Coccinella septempunctata to plant headspace chemicals collected from four crop Brassicas and Arabidopsis thaliana, infested with Myzus persicae." Agricultural and Forest Entomology. 10 (4), pp. 297-306. https://doi.org/10.1111/j.1461-9563.2008.00379.x
Analysis and Manipulation of the Structure of Odor Plumes from a Piezo-Electric Release System and Measurements of Upwind Flight of Male Almond Moths, Cadra cautella, to Pheromone Plumes
Girling, Robbie D. and Cardé, Ring T.. 2007. "Analysis and Manipulation of the Structure of Odor Plumes from a Piezo-Electric Release System and Measurements of Upwind Flight of Male Almond Moths, Cadra cautella, to Pheromone Plumes." Journal of Chemical Ecology. 33 (10), pp. 1927-1945. https://doi.org/10.1007/s10886-007-9349-3
Do turning biases by the 7-spot ladybird, Coccinella septempunctata, increase their foraging efficiency?
Girling, Robbie D., Hassall, Mark and Turner, John G.. 2007. "Do turning biases by the 7-spot ladybird, Coccinella septempunctata, increase their foraging efficiency?" Behaviour: an international journal of behaviourial biology. 144 (2), pp. 143-163. https://doi.org/10.1163/156853907779947337
Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae
Girling, R.D., Hassall, M., Turner, J.G. and Poppy, G.M.. 2006. "Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae." Entomologia Experimentalis et Applicata. 120 (1), pp. 1-9. https://doi.org/10.1111/j.1570-7458.2006.00423.x
Analysis and manipulation of odor-plume structure from a piezo-electric pheromone release system and its effects on upwind flight of male moths to pheromone
Girling, R.D. and Cardé, R.T.. 2006. "Analysis and manipulation of odor-plume structure from a piezo-electric pheromone release system and its effects on upwind flight of male moths to pheromone." International Society of Chemical Ecology Annual Meeting 2006. Barcelona, Spain 15 - 19 Jul 2006 Spain.
Analysis of the Courtship Behavior of the Navel Orangeworm, Amyelois transitella (Walker) (Lepidoptera: Pyralidae), with a Commentary on Methods for the Analysis of Sequences of Behavioral Transitions
Girling, Robbie D. and Cardé, Ring T.. 2006. "Analysis of the Courtship Behavior of the Navel Orangeworm, Amyelois transitella (Walker) (Lepidoptera: Pyralidae), with a Commentary on Methods for the Analysis of Sequences of Behavioral Transitions." Journal of Insect Behavior. 19 (4), pp. 497-520. https://doi.org/https://link.springer.com/article/10.1007/s10905-006-9041-4
Mating and mate finding behavior of the navel orangeworm
Girling, Robbie and Cardé, Ring T.. 2005. "Mating and mate finding behavior of the navel orangeworm." Entomological society of america pacific branch 89th annual meeting. Pacific Grove, California, United States 27 Feb - 02 Mar 2005 United States.
Responses of Diaeretiella rapae to volatiles induced by aphids from Arabidopsis thaliana mutants
Girling, R.D., Hassall, M., Poppy, G.M. and Turner, J.G.. 2003. "Responses of Diaeretiella rapae to volatiles induced by aphids from Arabidopsis thaliana mutants ." Royal Entomological Society’s 22nd Annual Meeting. Reading, UK 2003 - 2004
‘Handedness’ in the 7-spot ladybird beetle, Coccinella septempunctata: a problem for y-tube olfactometry
Girling, Robbie and Hassall, Mark. 2002. "‘Handedness’ in the 7-spot ladybird beetle, Coccinella septempunctata: a problem for y-tube olfactometry." International Society of Chemical Ecology Annual Meeting 2002. Hamburg, Germany 03 - 07 Aug 2002 Germany.