Acute exposure to urban air pollution impairs olfactory learning and memory in honeybees

  • Ryan J. LeonardEmail author
  • Thomas J. Pettit
  • Peter Irga
  • Clare McArthur
  • Dieter F. Hochuli


While the ecological effects of pesticides have been well studied in honeybees, it is unclear to what extent other anthropogenic contaminants such as air pollution may also negatively affect bee cognition and behaviour. To answer this question, we assessed the impacts of acute exposure to four ecologically relevant concentrations of a common urban air pollutant—diesel generated air pollution on honeybee odour learning and memory using a conditioned proboscis extension response assay. The proportion of bees that successfully learnt odours following direct air pollution exposure was significantly lower in bees exposed to low, medium and high air pollutant concentrations, than in bees exposed to current ambient levels. Furthermore, short- and long-term odour memory was significantly impaired in bees exposed to low medium and high air pollutant concentrations than in bees exposed to current ambient levels. These results demonstrate a clear and direct cognitive cost of air pollution. Given learning and memory play significant roles in foraging, we suggest air pollution will have increasing negative impacts on the ecosystem services bees provide and may add to the current threats such as pesticides, mites and disease affecting colony fitness.


Air pollution Honeybee Pollinator Proboscis extension reflex response Behaviour 



The authors thank T. Latty and C. Perry for feedback during manuscript writing.


Authors (RJL, TJP, PI, CM and DFH) received no funding for this project.

Authors’ contributions

RJL, TP, PI, CM and DFH conceived the project; RJL collected the data; TP and PI conducted chemical. analyses; RJL, TP, CM and DF wrote the manuscript. All authors gave final approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Amorim JH, Valente J, Cascão P, Pimentel C, Miranda AI, Borrego C (2013) Pedestrian exposure to air pollution in cities: modelling the effect of roadside trees. Adv Meteorol 964904Google Scholar
  2. Bitterman ME, Menzel R, Fietz A, Schafer S (1983) Classical-conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119CrossRefGoogle Scholar
  3. Brown A, Berman P (1970) Mechanism of excitation of Aplysia neurons by carbon dioxide. J Gen Physiol 56:543–558CrossRefGoogle Scholar
  4. Eigenbrod C, Gruda N (2015) Urban vegetable for food security in cities. A review. Agron Sustain Dev 35:483–498CrossRefGoogle Scholar
  5. Eiri DM, Nieh JC (2012) A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. J Exp Biol 215:2022–2029CrossRefGoogle Scholar
  6. Erber J (1976) Retrograde amnesia in honeybees (Apis mellifera carnica). J Comp Physiol Psychol 90:41CrossRefGoogle Scholar
  7. Faulkner M, Russell P (2010) Review of local air quality management: A report to Defra and the devolved administrations. Final report to UK Department for Environment, Food and Rural Affairs, January 2010. Retrieved from Retrieved from
  8. Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821CrossRefGoogle Scholar
  9. Garbuzov M, Ratnieks FL (2014) Quantifying variation among garden plants in attractiveness to bees and other flower‐visiting insects. Funct Ecol 28:364–374CrossRefGoogle Scholar
  10. Girling RD, Lusebrink I, Farthing E, Newman TA, Poppy GM (2013) Diesel exhaust rapidly degrades floral odours used by honeybees. Sci Rep 3:2779CrossRefGoogle Scholar
  11. Gulia S, Nagendra SS, Khare M, Khanna I (2015) Urban air quality management–a review. Atmos Pollut Res 6:286–304CrossRefGoogle Scholar
  12. Irga P, Burchett M, Torpy F (2015) Does urban forestry have a quantitative effect on ambient air quality in an urban environment? Atmos Environ 120:173–181CrossRefGoogle Scholar
  13. Irga P, Torpy F (2017) Reducing indoor air pollution through horticultural biotechnology. In Green infrastructure: nature-based solutions for sustainable and resilient cities. Orvieto, Italy, 2017. Retrieved from
  14. Kamyotra J, Mahwar R, Saxena R, Thirumurthy G, Puri M, Debroy R (2010) Status of the vehicular pollution control programme in India. Central Pollution Control Board, Ministry of Environment and Forests, Government of India: New Delhi, IndiaGoogle Scholar
  15. Kim K-H, Kabir E, Kabir. S (2015) A review on the human health impact of airborne particulate matter. Environ Int 74:136–143CrossRefGoogle Scholar
  16. Kirkerud NH, Wehmann H, Galizia CG, Gustav D (2013) APIS—a novel approach for conditioning honey bees. Front Behav Neurosci 7:29CrossRefGoogle Scholar
  17. Klein S, Cabirol A, Devaud JM, Barron AB, Lihoreau M (2017) Why bees are so vulnerable to environmental stressors. Trends Ecol Evol 32:268–278CrossRefGoogle Scholar
  18. Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci 274:303–313CrossRefGoogle Scholar
  19. Kumar MK, Nagendra SS (2015) Characteristics of ground level CO2 concentrations over contrasting land uses in a tropical urban environment. Atmos Environ 115:286–294CrossRefGoogle Scholar
  20. Kwak MM, Velterop O, Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1:37–54CrossRefGoogle Scholar
  21. Leonard RJ, Hochuli DF (2017a) The multifaceted nature of vulnerability in managed bees: a response to klein et al. Trends Ecol Evol 32:633–635CrossRefGoogle Scholar
  22. Leonard RJ, Hochuli DF (2017b) Exhausting all avenues: why impacts of air pollution should be part of road ecology. Front Ecol Environ 15:443–449CrossRefGoogle Scholar
  23. Leonard RJ, Vergoz V, Proschogo N, McArthur C, Hochuli DF (2019) Petrol exhaust pollution impairs honey bee learning and memory. Oikos 128:264–273CrossRefGoogle Scholar
  24. Lusebrink I, Girling RD, Farthing E, Newman TA, Jackson CW, Poppy GM (2015) The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction. J Chem Ecol 41:904–912CrossRefGoogle Scholar
  25. McFrederick QS, Kathilankal JC, Fuentes JD (2008) Air pollution modifies floral scent trails. Atmos Environ 42:2336–2348CrossRefGoogle Scholar
  26. Menzel R, Manz G, Menzel R, Greggers U (2001) Massed and spaced learning in honeybees: the role of CS, US, the intertrial interval, and the test interval. Learn Mem 8:198–208CrossRefGoogle Scholar
  27. Namdeo A, Colls J, Baker C (1999) Dispersion and re-suspension of fine and coarse particulates in an urban street canyon. Sci Total Environ 235:3–13CrossRefGoogle Scholar
  28. Omholt SW, Amdam GV (2004) Epigenetic regulation of aging in honeybee workers. Sci SAGE KE 2004:pe28Google Scholar
  29. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353CrossRefGoogle Scholar
  30. Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE 7:e30023CrossRefGoogle Scholar
  31. Seto KC, Fragkias M, Güneralp B, Reilly MK (2011) A meta-analysis of global urban land expansion. PLoS ONE 6:e23777CrossRefGoogle Scholar
  32. Stokstad E (2007) The case of the empty hives. Science 316:970–972CrossRefGoogle Scholar
  33. Tan K, Chen W, Dong S, Liu X, Wang Y, Nieh JC (2015) A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Sci Rep 5:10989CrossRefGoogle Scholar
  34. Varshney C, Padhy PK (1998) Total volatile organic compounds in the urban environment of Delhi. J Air Waste Manag Assoc 48:448–453CrossRefGoogle Scholar
  35. Walker J, Brown A (1970) Unified account of the variable effects of carbon dioxide on nerve cells. Science 167:1502–1504CrossRefGoogle Scholar
  36. Williams IH (1994) The dependence of crop production within the European Union on pollination by honey bees. Agric Zool Rev 6:229–257Google Scholar
  37. Williamson SM, Willis SJ, Wright GA (2014) Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology 23:1409–1418CrossRefGoogle Scholar
  38. Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216:1799–1807CrossRefGoogle Scholar
  39. Wright GA, Schiestl FP (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct Ecol 23:841–851CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ryan J. Leonard
    • 1
    Email author
  • Thomas J. Pettit
    • 2
  • Peter Irga
    • 3
  • Clare McArthur
    • 1
  • Dieter F. Hochuli
    • 1
  1. 1.School of Life and Environmental SciencesThe University of SydneySydneyAustralia
  2. 2.School of Life SciencesUniversity of Technology SydneySydneyAustralia
  3. 3.School of Civil and Environmental EngineeringUniversity of Technology SydneySydneyAustralia

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