CE34 - Contaminants, écosystèmes et santé

Assessment of the effects of ionizing radiation in bees – BEERAD

Assessment of the effects of ionizing radiation in bees – BEERAD

Human activities linked to nuclear industry generate ionizing radiation. However, their ecotoxicological properties are poorly studied on non-human organisms. This project proposes using the honeybees as a model to study the effects of ionizing radiation on major physiological functions, and also at individual and population levels. Honeybees are insects of economic, agro-environmental, societal and scientific importance.

General objective and main issues of the BEERAD project

The risk assessment linked to the radiocontamination of the environment after a nuclear accident is a major ecological issue but is still surrounded by controversial results and conclusions on the real impact of such events on flora and fauna inhabiting the targeted zones. Moreover, the potential underlying mechanisms of the action of ionizing radiation are poorly known. Therefore, it is important to acquire data on the potential effects of ionizing radiation on ecosystems both in experimental and realistic conditions.<br />The objective of this project is, using a pluri-disciplinary approach, to increase the knowledge of effects and mechanisms of action of IR on physiology and populations of honeybees in the context of chronic exposure (i.e., exposure of a significant period of time relative to the lifespan of exposed organisms) and at low dose rates (sublethal ecotoxicity) in realistic conditions, i.e., on the field and in the laboratory. However, very few data exist on this subject, and it seems important to conduct studies which will serve as a basis to better evaluate the impacts of IR on animal health using honeybees. <br />The main objectives of the project are:<br />- To define the exposure conditions both in laboratory and field experiments (in order to compare results obtained via these two approaches) and measure in both conditions the real external dose rates experimented by the bees by means of carried micro-dosimeters; these values, in addition to the internal dose rates, will give an accurate estimation of the total dose rates absorbed by bees (WP1),<br />- To measure the physiological and toxico-pathological effects induced by IR at sub-individual levels including molecule, cell and tissue, particularly with response to an infectious agent (WP2),<br />- To measure the effects induced by IR at individual and populational levels through the effects on reproduction/development and cognitive process (WP3),<br />- To compare both types of exposure (laboratory/field), integrate the responses and extrapolate to other living organisms (other bee species, other pollinating insects) through modelling in order to conclude on the level of effects of IR on bees and other pollinating insects (WP4).

The project will be conducted by using skills of both INRAE (expertise of the biological model, analyses of and individual biomarkers, physiological disturbances and of population indicators) and IRSN laboratories (expertise in the radiological exposure, measurement of exposure to radionuclide and calculation of the total dose, tools for irradiating animals at increasing dose rates of gamma irradiation), in order to study the impact of IR on honeybees. The help of IER (Institute of Environmental Radioactivity) of Fukushima will be very precious for all the field approaches, including knowledge of the zones, obtaining authorizations to conduct the field experiments, monitoring the beehives and the bees during field experiments.
A double approach of experiments conducted in field and in laboratory is proposed.
WP1: in the laboratory, we will use the large scale and smaller scale irradiation facilities available in LECO. The delivered dose rates via this irradiation facility are precisely known and will be monitored using micro-dosimeters. In the field experiments, the study sites will be chosen on the basis of our research on the more recent data of dose rates of the Fukushima region (mission in July 2022 for identifying the sites). In each zone corresponding to an available irradiation level (control, low and high), it will be chosen 3 sites in which 5 beehives per site will be placed. The hives will be let in place during two apicultural seasons. For all experiments, all measured effects (physiological, population, etc.) will be analyzed in relation to the total dose rate absorbed by bees.
WP2&3: in both laboratory and field experiments, the effects of the radiation on the honeybees will be studied by combined approaches at molecular, cellular and tissue levels. We aim to determine the impacts of radiation on great physiological functions that conditioned key events for the survival of individuals and the colony (colony behavior, reproduction, development, cognitive performances). We will consider not only the direct physiological impacts in bees submitted to an irradiation stress but also the resilience of the bees and bee colonies after an irradiation period. We will also evaluate the effects of ionizing radiations on sensitivity of bees to pathogens.
WP4: we intend to conduct modelling studies with two different objectives: (i) to predict early adverse events that could occur in colonies exposed to radiation and (ii) to extrapolate the results obtained with the bees to other species.

Work has started on the site search aspects for the field experimentation part. Several meetings have been held with the IER. GIS mapping work was carried out with an IRSN collaborator. Thanks to this work, different data have been cross-referenced (exposure, access by road, type of habitat, dose rate) and a gradient of sites going north of the plant seems to emerge. A field mission is planned from July 2 to 15, 2022 in order to observe the sites in person, to take photos, to characterize the flowering and sunshine of these different sites. Thanks to our colleagues from the IER and also with the help of a researcher from the NIES (National Institute for Environmental Studies), professional beekeepers will be met during this mission to discuss the possibility of installing hives from March 2023 to October 2024.
Concerning the laboratory experiments, two irradiation experiments of 14 days each were carried out between April and May 2022. The objective was to evaluate the toxicopathological interactions of ionizing radiation on the honeybee by combined approaches at the molecular level, cell and tissue under controlled laboratory conditions. For this, newborn bees were infected to Nosema ceranae, an intestinal pathogen of bees, and then irradiated for 14 days in the laboratory at a high gamma irradiation dose rate (14 mGy/h). The bees were placed in cages (50 bees per cage) then arranged around a source of 137Cs. Several modalities were tested: infected and irradiated bees, only irradiated bees, only infected bees and neither irradiated nor infected bees. The results demonstrated a higher mortality in the case where the bees were both irradiated and infected. In addition, irradiated bees presented a higher pathogen load than non-irradiated bees. This result expresses the sensitivity and the weakening of the bees due to the combination of the two modalities. No difference in food consumption was noted. Physiological analyzes were carried out on the heads of bees and on the last day of exposure. Oxidative stress was observed with increased tissue activity of GST and SOD. A possible transient effect of AChE has been suggested. These data, supplemented by the analyzes planned later on the other compartments and the other sampling times (and also on a lower dose rate of 14 µGy/h), will make it possible to better understand the combined effects of irradiation and infection on bees.

The program is focused on the effects of IR on honeybee health as a global indicator of ecosystem health. The benefits of this program are expected at different levels:
- At scientific level, expected results cover a large broad of domains: (i) what are the accurate absorbed (external + internal) dose rates and doses experimented by bees, (ii) what are the modes of action by which IR induce adverse effects in bees, (iii) which physiological and toxico-pathological parameters are affected by IR, with a focus on combined effects of IR on sensitivity of bees to pathogens, (iv) which parameters are modified by IR at the colony level, including hive production (in relation with ecosystem services), (v) what is the resilience of hives exposed to IR during an apicultural season, (vi) if bees exposed in the field are more or less sensitive to IR than bees exposed in the laboratory (comparison of responses) and (vii) through modelling approaches, what can be the expected consequences of IR exposure on other pollinating insects. Our results will offer the possibility of a better risk assessment by a better prediction of the biological responses induced by IR on pollinating insects.
- At economic level, we will obtain data on the quantity of hive products (honey and pollen) in hives placed in the Fukushima exclusion zone along the contamination gradient. Therefore, the project will help to estimate the potential impacts of IR on the provisioning ecosystem service. Moreover, these data will be available for economists in order to take them into account and integrate them in models for a better evaluation the costs of a potential nuclear accident in France.
Important remark: the project will not include the economic aspects in terms of production of hive by-products or replacement of colonies because it is outside the field of competences of the consortium and also because this work will represent a full project on its own. However, the present project aims to improve the costs of a nuclear accident in France. Therefore, all of our data will be available for.
- At the agro-environmental level, the project will not allow to measure the direct impact of IR on pollination (ecosystem regulating service). However, we will be able to measure an indirect impact through the hive foraging activity and population in field (evolution of the weight of the colony) and through the food consumption in the laboratory. Moreover, this project will bring some new elements to explore if beehives (bees and bee products) could be useful to assess environmental quality, in Fukushima and in France.
- At the societal level, due to the emblematic image of the bee, the presentations of our results to different events, scientific and non-scientific, will take place in the frame of the cultural ecosystem services linked to bees. In addition, the honeybee will serve as a model species to estimate the potential impacts of IR on other species.

Transfer towards the scientific community
New results and methods developed in the project will be published in international peer-review journals to be rapidly accessible to international experts and beekeepers.
Results will be presented in national and international scientific conferences (Apimondia, EURBEE, ICP-BR, Symposiums of the Society of Environmental Toxicology & Chemistry, etc.) as oral or poster communications.
We will also render our data available for economists in order contribute to characterize the costs of a nuclear accident on apiculture. For an optimal use of our data by economists, we will clearly explain to economists the strengths and the limits of our data.
Transfer towards general and professional publics
The project and the results of this project will be presented to beekeeping organizations (GDSA, ADAs…) through oral communications in general assemblies, “Les Journées de la Recherche Apicole”, “les journées santé des abeilles” of ANSES and through transfer articles in different beekeeping journals such as “La Santé de l’Abeille” or “Abeilles & Fleurs” (non-exhaustive list) and different professional and transfer journals concerned by the honeybee biology and health, and by the environmental health.
In additions, results will be also presented as conferences for organizations involved in environmental health and biodiversity preservation.

Human activities linked to nuclear industry generate ionizing radiation (IR). However, their ecotoxicological properties are poorly studied on non-human organisms. In radio-contaminated areas, there is no scientific consensus concerning their effects on structure and functioning of the ecosystems, and the potential underlying mechanisms of their action are poorly known. Therefore, it is important to acquire data on the potential effects of IR on ecosystems both in experimental and realistic conditions. This project will try to estimate the environmental consequences of a major nuclear accident by studying an emblematic of pollinating insect, the honeybee, which presents scientific, economic and societal stakes, through the services provided by this species to the society and ecosystems. This project will also contribute to improve knowledge on effects and mechanisms of action of IR on honeybees, by using a combined approach of laboratory and field experiments and could allow to foresee more global consequences on pollinators responsible for a great part of vegetal biodiversity.

The main objectives of the project are:

- To define the exposure conditions both in laboratory and field experiments (in order to compare results obtained via these two approaches) and measure in both conditions the real external dose rates experimented by the bees by means of carried micro-dosimeters; these values, in addition to the internal dose rates, will give an accurate estimation of the total dose rates absorbed by bees (WP1),
- To measure the physiological and toxico-pathological effects induced by IR at sub-individual levels including molecule, cell and tissue, particularly with response to an infectious agent (WP2),
- To measure the effects induced by IR at individual and populational levels through the effects on reproduction/development and cognitive process (WP3),
- Compare both types of exposure (laboratory/field), integrate the responses and extrapolate to other living organisms (other bee species, other pollinating insects) through modelling in order to conclude on the level of effects of IR on bees and other pollinating insects (WP4).

Expected results cover a large broad of domains: (i) what are the accurate absorbed (external + internal) dose rates and doses experimented by bees, (ii) what are the modes of action by which IR induce adverse effects in bees, (iii) which physiological and toxico-pathological parameters are affected by IR, with a focus on combined effects of IR on sensitivity of bees to pathogens, (iv) which parameters are modified by IR at the colony level, including hive production (in relation with ecosystem services), (v) what is the resilience of hives exposed to IR during an apicultural season, (vi) if bees exposed in the field are more or less sensitive to IR than bees exposed in the laboratory (comparison of responses) and (vii) through modelling approaches, what can be the expected consequences of IR exposure on other pollinating insects. Our results will offer the possibility of a better risk assessment by a better prediction of the biological responses induced by IR on pollinating insects.

This project is innovative for several reasons. It proposes (i) to study the effects of IR on honeybees, very poorly known up to now, (ii) to establish a basis of knowledge on mechanisms of action of IR in honeybees and (iii) to relate responses observed at the cellular/organ scale to integrative process at the individual/population scale by studying reproduction and repercussions of effects at the colony level. Moreover, the project will combine experiments in the laboratory and in the field, more representative of the environment. This complementarity will serve to draw useful conclusions for the environmental radioprotection.

The benefits of this program can be expected at scientific, agro-environmental and socio-economic levels.

Project coordinator

Madame Beatrice Gagnaire (Pôle Santé Environnement - Direction Environnement)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

PSE-ENV Pôle Santé Environnement - Direction Environnement
INRAE PACA - A&E Institut National pour la Recherche, l'Agriculture et l'Environnement - Centre de recherche PACA - Abeilles et Environnement
IER Institute of Environmental Radioactivity

Help of the ANR 522,637 euros
Beginning and duration of the scientific project: December 2021 - 48 Months

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