By J. van der Steen PhD – AlveusAB Consultancy, The Netherlands – The international INSIGNIA group
Honey bee colonies are well equipped as bio samplers of contaminants in the environment, and how beekeepers can cooperate optimally with scientists to map this contamination is currently being studied at the European Union level in the Insignia citizen science project (https://www.insignia-bee.eu). Regularly, new studies are published about how honey bees and hive products can be applied to detect environmental contaminants. This is a very promising development. Apiculture is a world-wide activity and with adequate tools and the help of apiculturist citizen science, a world-wide network can be built to search for contaminants.
An interesting study was published recently in July 2020. Kate Smith and co-workers published the article Honey maps the Pb fallout from the 2019 fire at Notre Dame cathedral, Paris: a geochemical perspective . The title tells that lead fallout after the Notre Dame fire was mapped by analysing honey. This is only a part of the paper and in hindsight this part could have been done better. The paper focuses on the environmental contamination by lead (Pb) due to the Notre Dame fire of 15 April 2019; about the possible altering of the lead profile in the Parisian soil; whether it is possible to map this contamination with honey bee colonies, and finally what the impact can be on the food security of honey. In this article I summarise the geo-chemical part and comment on the honey bee part.
The Notre Dame cathedral had a roof covered with hundreds of tons of lead. As we all have seen, the roof was destroyed and most of the lead melted during the fire. The melting and evaporation points of lead are 327.5 and 1,700oC respectively. As the highest estimated temperature of the fire was about 1,200oC, the lead therefore melted and did not evaporate. Estimation of the original amount of lead compared to what was traced back in and around the cathedral after the fire, however, reveals a loss of approximate 180 ton (180,000 kg) of lead. This lead passed into the atmosphere as aerosols. An aerosol is a droplet of gas containing solid parts whose size ranges from 0.2 to 200 micrometres. A micrometre is a 1/1000 of a millimetre. A plume is cloud of aerosols. What goes up must come down, and where and how far from the source depends on how high the plume is, how strong the wind is, what the wind direction is and the size of the aerosols. Lead is toxic; it has a negative impact of the neuro system development of children. Once it hits the soil, it is very hard to remove as it attaches chemically very firmly to soil particles. Natural soil contains no or very small amounts of lead and what is detected is what man has brought there; the anthropogenic origin of lead. There is a long history; for example the Romans used water pipes of lead and they were not the first. The mineral lead has four stable isotopes. These are different forms of the same element having the same characteristic but a slightly different molecular mass. The ratios between these isotopes (lead isotopic profile) differ regionally, reflect the lead contamination history and the lead ore; Australian lead has a different isotope ratio compared to European lead. The Parisian topsoil comprises a huge lead archive with a local typical Parisian isotopes ratio, built up over many many centuries of construction, industry and traffic.
The link to the honey bee colony is the interaction between honey bee colony and the environment, in particular, the topsoil. By soil erosion, tiny soil particles are deposited on flowers and are collected, along with pollen, nectar, propolis and water and accumulated in the hive. To give you a sense of what is eroded and deposited daily, I point to the dust on cars and window sills. This is the visible part, which is only a fraction of the total deposition. Focussing on lead and honey bee colonies, we know this metal is detectable in bees, pollen and honey. Nectar itself contains no lead, so what we see is the result of human activity . In the honey bee colony, most lead can be detected in the bee herself where it accumulates during her life time, then in pollen and the least in honey . This is the result of the continuous dilution by newly collected nectar and honey processing. In this process the vast majority of particles are filtered out of the nectar. What remains is the smallest fraction.
Back to 15th April 2019 in Paris. It is obvious that most lead from the plume would have been deposited on the pavements and roofs where it has been cleaned or washed away. The amount of lead deposited on vegetation and the bare soil would have been relatively low, yet, in 8 of the 36 honey samples collected in the summer of 2019 in the city centre and the Parisian suburbs/ banlieues, an elevated amount of lead was detected, which could directly be linked to the fire. The lead fallout could be mapped up to about 5 km from its source. This distance does not tell us the absolute border of the contamination, because the polluted area is undoubtedly much larger but may have amounts not detectable via honey. Nevertheless, using honey, roughly an area where the acute lead fallout occurred can be mapped. In the 2019 Parisian summer honey, on average 0.014 milligrams lead per kg honey was detected. Split up by wind direction, to the West, where the plume headed to, the mean amount was 0.023 milligrams, where the mean of the honey from central Paris was 0.008 milligrams. According to the EU food safety regulation the tolerable amount lead in honey is all below 0.10 milligrams lead per kg honey. So even the honey from the most contaminated area remained under this critical limit so can be eaten safely. In comparison, in honey collected simultaneously in Grenoble in the French Alps, the amount of lead was 0.004 milligrams and in the Parisian summer honey of 2018 it was 0.009 milligrams per kg honey. It remains an issue whether this lead fall out due the Notre Dame fire has permanently altered the Parisian soil lead profile. The answer is no; there were changes in the isotopic profile but all were within the local variation of the Paris area.
This study demonstrated clearly how important and how difficult the correct interpretation of bio-monitoring with honey bee colonies is. This is particularly true of heavy metals, as this depends on historical depositions that vary from day to day and over the centuries and from region to region . Furthermore it shows the limitation of honey as tool to demonstrate lead and other heavy metal pollution in the environment. Analyses of bees could certainly have shown higher amounts of lead and over a wider area. In comparable studies, 4 to 30 times more metals were detected in bees compared to honey [5, 6, 7]. However, killing bees for this goal encounters, for ethical reasons, justified objections. This shows the need for further development of non-biological passive sampling tools, applicable in a honey bee colony such as the APIStrip, which is applied to detect pesticides in the environment by honey bee colonies . Non-biological passive samplers can be applied widely, without any burden for the honey bee colony, in citizen science studies with beekeepers to map contaminants and to make the honey bee colony a broadly available bio monitoring instrument.
 Smith, K. E., Weis, D., Chauvel, C., & Moulin, S. (2020). Honey maps the Pb fallout from the 2019 fire at Notre-Dame Cathedral, Paris: a geochemical perspective. Environmental Science & Technology Letters.
 Walraven, N. 2014. Lead in rural and urban soils and sediments in The Netherlands: background, pollution, sources and mobility. PhD thesis Vrije Universiteit Amsterdam ISBN/EAN: 978-94-6259-259-9
 Steen, J.J.M. van der 2016. Beehold, the colony of the honeybee (Apis mellifera L.) as a bio-sampler for pollutants and plant pathogens. PhD thesis Wageningen University ISBN 978-6257-751-0. https://research.wur.nl/en/publications/beehold-the-colony-ofthe-honeybee-apis-mellifera-l-as-a-bio-samp
 Steen, J. J. M. van der, Cornelissen, B., Blacquière, T., Pijnenburg, J. E. M. L., & Severijnen, M. (2016). Think regionally, act locally: metals in honeybee workers in the Netherlands (surveillance study 2008). Environmental monitoring and assessment, 188(8), 463.
 Fakhimzadeh, K., & Lodenius, M. (2000). Honey, pollen and bees as Indicator of heavy metal pollution. Apiacta, 35: 85-95
 Leita, L., Muhlbachova, G., Cesco, S., Barbattini, R., & Mondini, C. (1996). Investigation of the use of honey bees and honey bee products to assess heavy metals contamination. Environmental Monitoring and assessment, 43(1), 1-9.
 Conti, M. E., & Botrè, F. (2001). Honeybees and their products as potential bioindicators of heavy metals contamination. Environmental monitoring and assessment, 69(3), 267-282.
 Murcia-Morales, M., Van der Steen, J. J., Vejsnæs, F., Díaz-Galiano, F. J., Flores, J. M., & Fernández-Alba, A. R. (2020). APIStrip, a new tool for environmental contaminant sampling through honeybee colonies. Science of The Total Environment, 138948