Pesticide risk assessment should look at the behaviour of bees, not just their survival - Interview with Simone Tosi, PhD, Associate Professor

A major shortcoming in the assessment of pesticides is that it only looks at the mortality rate of a limited number of insect species. But what is the effect if beneficial insects are weakened, can no longer find their nests and produce far fewer offspring? Professor Simone Tosi outlines the problem and makes recommendations for improvement of the protection of the species that are vital for ecosystems, food production and our survival.

In this campaign to protect arthropods from pesticides to restore biodiversity, we interview scientists, review new scientific research and highlight the importance of lesser-known arthropods. Our aim is to stimulate the discussion to achieve the urgent protection of the natural abundance on which our lives depend.

Who is Simone Tosi?

“My name is Simone Tosi. I am a Professor at the University of Torino in Italy. Where I teach beekeeping and biodiversity and management of pollinators, and where I also coordinate the bee lab research group that investigates the behaviour and health of pollinators. Especially bees.”

Can you tell us more about your research?

ST: “At the University of Torino, we focus on many different aspects of bee behaviour and bee health, including the amazing behaviours that bees have, like the abilities of queen bees to sing or the courtship and reproduction behaviour of bees.

We also do a lot of research on the reasons why these behaviours are impacted and why bee populations are in decline. Mostly focusing on the impact of pesticides. In terms of lethal and sublethal effects, but not just pesticides, because bees are exposed to many different stressors in the environment, such as malnutrition, climate change, and pathogens. And so we study them in an interaction with all these realistic impacts, and I've done a lot of research on these topics. From the exposure side, we've been using bees and their service, their ecosystem service, to monitor environmental contamination. And so we figure out how widespread the contamination of pesticides is and, especially, by multiple pesticides at the same time. How that impacts bees, but also many other organisms, including humans.

We've also done a lot of research in terms of the toxicity of these pesticides, and especially in terms of the behavioural impact that they have. Not just the impact on the behaviour of bees, but also the impact in the long term. We've demonstrated that short exposures that are typically included in the risk assessment are not as predictive of the impact as longer exposures that are still highly realistic.

We've also studied the impact of stressors in combination. For example, we demonstrated that pesticides in combination with malnutrition cause synergistic effects. Of course, we studied the synergistic effects caused by multiple pesticides at the same time. And I want to mention that these are extremely relevant effects because bees in the field are exposed to many different stressors at the same time, and we always focus on field-realistic exposures. We've studied in terms of the impaired behaviours that are caused by a set exposure. Their production, a key aspect of the health of bees and that allows the population to grow.

We demonstrated just last year that the very peculiar and interesting courtship behaviour, and mating behaviour that bees have - in this specific case, we've been studying wild bees-are impacted by pesticides. For example, we showed that realistic exposure increases the duration of the mating process, but at the same time reduces the sperm quantity and the ability of bees to courtship to try to manage to have a successful reproduction. This suggests that pesticides reduce the abilities of bees to reproduce. We've also been studying the contamination of pesticides at a wider scale.

In terms of regulation, we have published a paper on the emergency authorisation. It was one of the first to investigate more deeply the impacts of this process in terms of what types of pesticides are authorised as an emergency. We show that they are widely more toxic than those that are typically used. We also showed some weaknesses in the regulation, so that many of these pesticides that are authorised through emergency regulations have been authorised for longer periods than acceptable by the law.”

What are the effects of pesticides on the bee population?

ST: “A few years ago, we were focusing on neonicotinoids that were the most widely spread pesticides in the globe and we demonstrated for the first time the impact on the flight behaviour of bees. We demonstrated their impact on the locomotion and on the phototaxes of bees, showing that even field-realistic levels of exposure can lead to important alterations of the behaviour of bees. Of course, as you know, flight is a crucial behaviour that allows the pollination and reproduction of fruits and plants. And even if the bee is still alive, if this bee cannot fly, or they fly in a way that's not efficient. Of course, there is an impact at the level of their health, and of course the health of their colony. In the case of honey bees or bumblebees, which are social organisms. But also in terms of local agricultural production and finally at the level of their society.”

“So, the behaviour of bees is extremely important, and we have to protect them. And so we've shown effects on these behaviours after neonicotinoids, with focus on the new generation of pesticides after the neonicotinoids have been restricted. Such as flupyradifurone and sulfoxaflor.

We've been one of the first groups testing the adverse effects of flupyradifurone. It's important to mention that we started to test this compound to assess if it could have an adverse effect on bees. Indeed, we demonstrated an adverse effect on bees, while this pesticide was still defined as bee safe. So it was still allowed to use it in the fields while flowers were blooming, for example. And when you could see the active foraging of bees.

So, it was quite important, and we are quite proud to be providing more information on this topic, on the adverse effects that these supposedly bee-safe pesticides have on bees and pollinators.”

What is missing in the current risk assessment?

ST: “Pesticides have been developed and produced and commercialised because of their widespread use in the current agricultural system. And they indeed have many benefits for agriculture, at least in the short term. However, they can carry many adverse effects. And it feels that the progress in developing new pesticides and new compounds, new chemicals, new molecules that are more efficient and more selective, is not being balanced by the same amount of effort and energy and investments in figuring out what the adverse effects of these compounds are. It is pretty clear from history, starting from Rachel Carson, when in the 60s she published Silent Spring about the adverse effect of the widespread use of DDT.

In more recent times, similar processes have also been demonstrated for a new generation of pesticides. One important example is the neonicotinoids, which have been authorised and then restricted or banned in many countries. They are still used in the world, of course, for example, in the US. But in Europe, the regulations are more strict. And after neonicotinoids other generations of compounds arrived. For example, flupyradifurone, a pesticide that we have been studying, its use is now restricted in certain European countries.
The progress of developing new pesticides is pretty fast and efficient, but it must be aligned with an assessment of their adverse effects. That's why the risk assessments are in place. Risk assessments' goal is to figure out if the positive and negative effects of compounds are acceptable or not. The problem is to assess these effects, especially adverse effects. It's a pretty complicated topic. Especially, the current regulations use guidelines and guidances that are not as refined and updated as needed in terms of what researchers have found, in terms of effects of these compounds. 

For example, the regulations and protocols still do not include an appropriate impact of compounds on the behaviour of the bees. The focus is on the lethality, so whether the bees are alive or not. But as we mentioned before, it's very important to figure out if a living bee is also able to perform and to provide, for example, ecosystem services and make the colonies revive. They also marginally address the chronic effects we see with our monitoring studies, where we investigate the contamination in the environment and in the beehives. We found out like many other researchers in the world, that the contamination environment is very widespread in time. So throughout the season and the years. So bees are exposed to pesticides for long periods and this has to be tested while risk assessment procedures so far are focusing only on the short term.

Furthermore, this exposure that bees receive is not just limited to one stress or one pesticide at the time. They are exposed to multiple pesticides simultaneously. And the issue here is that this combined exposure can lead to synergistic effects. The effect of one pesticide is extremely amplified by the presence of another one. So if they were alone, this pesticide would maybe not cause so much effect, but wonder together the impact is much more risky and this is not implemented nor assessed in risk assessment process. Not just for bees. On the one side it is pretty complicated to assess these effects, but not assessing these effects can lead to a wide underestimation of the risks.”

“Furthermore, while we have been focusing in this talk about pesticides, we have to mention that there are many other stresses that bees are facing. For example, malnutrition. Bees are widely exposed to malnutrition because agricultural fields more often provide food for just brief periods of time. The biodiversity and availability of nectar and pollen are reduced. One of our studies demonstrated that there is a synergy between malnutrition and pesticide exposure at field-realistic levels. So if a bee is malnourished, it is widely more susceptible to the intoxication by pesticides. And these complex contexts where bees are exposed to many different stressors at the same time, that is pretty realistic and common, also, as human beings, we are constantly exposed to contaminants and to multiple stressors at the same time. This is not really captured in risk assessment and it can lead to an underestimation of the risks that the production and use of pesticides can cause to us, but also especially to bees and pollinators in this case.”

How to improve the current risk assessment?

ST: “Our lab, as well as various other labs in the world, developed protocols and experiments that are able to test different types of behaviours of bees. On our side, we know the complexity of risk assessment, as I've been collaborating for a long time in this field with EFSA and other agencies that are focusing on improving risk assessment. And we know the complexities of implementing behavioural studies, for example, in the risk assessment. That's why we're developing ring tests, which is a test that is developed at the same time by many countries and laboratories around the world. To standardise these methodologies. So there's effort, and there is an interest to standardise behavioural studies and other types of studies that can be implemented in risk assessment. It's important to make this successful and to make regulation on the production and use of pesticides as protective for bees and environment, and that there is an effort also from the Member States to make sure that this field is growing and is producing what is needed so that the risk assessment can be refined and improved and protect also the behaviour of bees, not just their survival.”

Full Interview with Simone Tosi

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Pesticide Action Network Europe (PAN Europe) gratefully acknowledges the financial support from the European Union, European Commission, DG Environment, LIFE programme. Sole responsibility for this publication lies with the authors and the funders are not responsible for any use that may be made of the information contained herein.