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Many different species of insects and other invertebrates prey on the plant-feeding insects which attack crops. Ladybird beetles and spiders are familiar garden examples. There are also parasitic insects, which lay their eggs in or on pests (such as aphids or caterpillars), from which the hatching larvae slowly consume their host. Along with insect-feeding birds, bats, frogs and others, these invertebrates are known as ‘natural enemies’ and perform the very important but often underestimated service of providing biological control of pests. Insect natural enemies can make a significant contribution to keeping pests in check in farmers’ fields but they are often highly sensitive to pesticides and easily harmed by applications of many commonly used products. This factsheet looks at recent research showing that the neonicotinoid group of insecticides may be harming valuable natural enemies, as well as pollinators.

Ladybirds mating on a cotton leaf. Credit: PAN Ethiopia


June 2017

Bee Declines & Pesticides factsheet 10

Pesticide Action Network UK Neonicotinoids and harm to natural enemies of pests


Key Points • Neonicotinoid insecticides can be highly toxic to many natural enemies via direct contact or residues on treated or contaminated soil or vegetation where they forage, shelter or nest. • Natural enemies can also be harmed indirectly when they consume plantfeeding insects which have fed on crop plants grown from seed treated with neonicotinoids. • Some natural enemies rely on nectar, pollen or other plant tissue for part of their diet. As with pollinators, they can be harmed when feeding on floral resources containing neonicotinoid residues. • At sub-lethal doses, neonicotinoids may disturb the feeding behaviour or reproduction of natural enemies. • Neonicotinoid seed treatments do not protect natural enemies. They can be as harmful to predatory insects as other insecticides sprayed onto crops or soil. • By disrupting natural biological control, neonicotinoids may actually increase levels of some pests, reducing yields and farmers’ profits. • Neonicotinoids should not be considered as ‘reduced risk’ products to natural enemies and they may be incompatible with Integrated Pest Management strategies for many crops.

Recently discovered routes of exposure An excellent report1 by the Xerces Society for Invertebrate Conservation in the US first drew popular attention to growing evidence that neonicotinoids can be very harmful to natural enemies.These compounds are

very highly toxic to a broad spectrum of insect groups, not only the pest groups they are intended to target, so it is not surprising that direct contact of natural enemies caught in spray or in touch with neonicotinoid residues on treated foliage can be lethal. For example, in lab studies, exposure to spray applications at the recommended dose of acetamiprid, clothianidin and dinotefuran killed 100% of adult Cryptolaemus montrouzieri ladybirds, an important predator of mealybugs, after 48 hours2. Soil or turf treatments can also be a lethal exposure route for natural enemies that hunt at the soil surface, such as predatory ground-dwelling beetles: one study found that imidacloprid granules applied to turf at label rates reduced ground beetle populations by up to 84% shortly after application and these did not recover within a year3. What recent research reveals is that, just as in the case of pollinators, natural enemies can also be exposed unintentionally to neonicotinoids in less obvious ways, such as: • seed treatment leading to neonicotinoid residues in nectar, pollen or other plant tissue • contaminated seed dust released into fields via mechanical abrasion at seed drilling • neonicotinoid-contaminated soil, used by natural enemies for nesting/shelter • contaminated field border vegetation, which provides essential habitat for shelter, foraging, nesting or overwintering of various natural enemy groups


which may feed on plant tissue when prey is scarce, suffered high mortality when confined on thiamethoxam-treated plants even when prey was available.This study also documented adverse effects on other predatory bugs and on Chrysopa species lacewings in treated plots in the field. Several other studies show reduced lifespan of omnivore natural enemies when feeding on floral resources from treated crops or trees. For example, the parasitic wasp Anagyrus pseudococci had reduced survival rate after chronic exposure to nectar from plants soiltreated with imidacloprid5.

Hoverfly adult on a strawberry leaf. Credit: Stephanie Williamson

• indirect toxicity via feeding on prey which have fed on treated crops • drinking contaminated surface water • drinking guttation droplets exuded from the leaf tips of treated plants While all natural enemies are carnivorous at some stage in their life cycle, many also rely to some extent on plant material for part of their diet. Parasitic wasps and hoverflies are good examples - the adults need to feed on nectar from wild flowers or crops in bloom, while the larvae are the predatory stage.The group of tiny predatory pirate bugs will often take a snack of pollen or nectar for an energy boost, as well as feeding on their usual soft-bodied prey. This feeding behaviour leaves some natural enemies exposed to neonicotinoid residues in floral resources, including when field border plants have taken up the insecticides in nearby soil or water. One US study4 of imidacloprid and thiamethoxam seed treatment of soybean found that the juvenile stage of minute pirate bug Orius insidiosus, an important predator of soybean aphids,

Almost nothing is known about the levels of natural enemy exposure via contaminated soil, water sources or field border vegetation or of the likely effects. As scientific understanding expands of the widespread occurrence of neonicotinoid residues beyond their site of application (see PAN UK Factsheet 9. on persistence), probable exposure of bumblebee and solitary bees has been highlighted as a serious concern for those species that rely on soil, water and plant resources in and around cultivated fields. Similar exposure concerns would also be relevant for key natural enemies of pests.This exposure route is currently ignored in pesticide environmental risk assessment for pollinators and “The large scale for natural bioavailability of these enemies.

insecticides in th e global environment at levels that are known to cause lethal and sub-le thal effects …poses risks to ecosyste m functioning and services… includ ing biological pest co ntrol…” Worldwide Integrat ed Assessment of th e Impacts of Systemic Pesticides on Biodiversity & Ecos ystems, 2014.


Vedalia beetle. Credit Katja Schulz, CC BY 2.0

Sub-lethal and indirect effects on natural enemies While neonicotinoid exposure may not be fatal in many situations, it can result in sub-lethal effects for predatory or parasitic natural enemies, reducing or disrupting their mobility, hunting, feeding or reproduction. Some examples from the scientific literature cited in the Xerces report are: • Pink ladybirds Coleomegilla maculata showed reduced mobility and survival when exposed long-term to imidacloprid residues in soil-treated sunflowers6 • Parasitic wasps Avetianella longoi, which prey on stem-boring beetle pests, had reduced survival and reproduction after feeding on nectar from eucalptyus trees treated with imidacloprid 5 months before bloom7

• Predatory mites Neoseiulus californicus suffered reduced fecundity when exposed to imidacloprid, while their pest prey, the two-spotted mite Tetranychus urticae, increased its reproductive rate8 Several studies reported indirect effects on natural enemies from consuming prey individuals that have fed on plants treated with neonicotinoids, for example: • Vedalia beetle Rodolia cardinalis, a biocontrol agent used in US citrus against cotton cushiony scale pest, showed lower adult survival and fertility after feeding on scales on neonic-treated plants and high mortality of beetle larvae9 • Hippodamia undecimnotata ladybirds had reduced survival, lifespan and egg production after feeding on aphids


reared on bean plants treated with soil application of imidacloprid10 However, not all natural enemies are equally affected by neonicotinoids – ants, spiders and some predatory mites are generally much less susceptible than other predator groups or parasitic wasps. For a particular species, it may be the adult or the juvenile stage that is more at risk from lethal or sub-lethal effects. The literature also indicates that there is considerable variation in toxic effects of different neonicotinoid compounds. Along with scant information on exposure levels in the field, it is hard therefore to predict to what extent natural enemies are being affected by neonicotinoid use.

Latest research findings of harmful effects Table 1 summarises findings from ten studies published since 2014, which report some level of harmful effects of neonicotinoids on natural enemy survival, feeding or reproduction. As part of a study on neonicotinoid levels found in wild plants near treated arable crops in SE England21, researchers at Sussex University looked at how the levels they detected relate to standard lethal toxicity values (LC50, the dose at which 50% of test insects are killed in lab tests) and to EU pesticide risk assessment parameters (hazard quotients) for nontarget terrestrial arthropods, such as predatory insects. They found that levels often exceeded the concentration of 5-10 parts per billion considered as sufficient to protect crops from pests and sometimes as high as the LC50 values for some non-target insects. At the highest levels

“Hedgerows and field margins contribu te to enhance crop yiel ds by providing nest sites, forage resources for pollinators and ac ting as reservoirs for natural enem ies of crop pests… .The widespread pres ence of [neonico tinoid] compounds in fie ld margin wild pl ants raises concerns over th e potential effect s of exposure for nontarget wildlife….” Cristina Botías & co lleagues, University of Sussex , 2016

detected in field side flowers or shrubs important natural enemies of cereal pests, such as the predatory bug Orius laevigatus and the parasitic wasp Aphelinus mali, could well suffer acute toxicity effects according to the EU risk parameters. In addition, chronic exposure at the lower levels found could result in sub-lethal effects, as could exposure to multiple residues (46% of foliage samples contained two or more neonicotinoid compounds). Neither chronic nor multiple exposures are considered in current risk assessment procedures for natural enemies.

IPM compatibility concerns Not all published studies show negative effects of neonicotinoids on natural enemy survival, feeding or other behaviour. One field study in Austria on combining use of biopesticides with maize seed treatment with clothianidin and cypermethrin for control of the root-feeding beetle Diabrotica virgifera did not show any significant impact of either the biopesticide or chemical treatments on abundance or diversity of predatory beetles or spiders22. Interestingly for


Table 1. Test Crop type PP soybean

Neonic compound imidacloprid thiamethoxam


field crops



aphid pests



apple, pear



ornamental flowers



whitefly pests



sun-flower nectar




clothianidin & nitenpyram


aphid pests in field & green-house




acetamiprid imidacloprid thiacloprid thiamethoxam

Natural enemies Parasitic wasp Aphelinus certus


Wasp was able to parasitize soybean aphids feeding on treated plants 5 and 6 weeks after planting but up to 10 wk after planting, overall parasitism rates were reduced by 69 – 88% compared with control. Predatory bug Among 6 insecticides tested, thiacloprid caused Macrolophus 100% mortality to predator via direct, residue pygmaeus contact and oral exposure. At sublethal rates, thiacloprid reduced predation rate. Ladybird beetle A single application to ladybird 2nd instar larvae Coccinella affected survival, egg production and hatching. septempunctata Survival & development time were the most sensitive endpoints. Negative effects were reported at rates well below field application rates in cotton. Earwig Forficula Of 8 pesticides tested (different chemical groups), auricularia, generalist only 3 could be considered as ‘earwig safe’.Thiacloprid predator (+ 4 other non-neonic compounds) reduced growth of earwig larvae.Thiacloprid reduced earwig foraging in orchard trees at night. Earwig numbers were significantly negatively affected in orchards with conventional spray programme, compared with compatible spray programme. Ladybird beetles Soil-applied treatment resulted in very high residues Coleomegilla in tropical milkweed flowers, leading to significant maculata; Harmonia mortality and reduced survival of 3 ladybird species, axyridis; Hippodamia except C. septempunctata. convergens; Coccinella septempunctata Ladybird beetle Thiamethoxam can strongly affect predatory activity Serangium japonicum of this biocontrol agent for sucking pest control. Predation more affected by systemic exposure route (rather than residue contact or egg dip). Sub-lethal effects of systemic or foliar application both impaired biological control function. Ladybird beetles Larvae of C. maculata exposed via stems of seedColeomegilla treated plants took longer to adult emergence. H. maculata & convergens exposed as larvae had reduced egg viability Hippodamia as adults.Thiamethoxam had negative, sub-lethal effects convergens on predator biology when these feed on extrafloral nectar of sunflowers grown from treated seed. Ladybird beetles Granular treatments at sowing reduced ladybird Harmonia axyridis & population densities, although effect may be more due Propylea japonica to insecticides reducing aphid prey than to toxicity to predators. Ladybird beetle Sub-lethal concentrations shortened adult longevity by Coccinella 24-29% and reduced fecundity by 53-56%. Offspring septempunctata of exposed beetles were also affected, developing more slowly and had shorter egg-laying period and reduced fecundity. Parasitic wasps All 4 neonics (+ 5 other insecticides tested) Encarsia guadeloupe significantly reduced emergence of parasitic wasps & E. meritoria & % parasitism rate of spiralling whitefly. Only one Predatory beetles compound (non-neonic) could be considered safe to Cybocephalus spp. predators, due to relatively less toxic effects. Green lacewing Mallada astur

Test type: Lab test (L); Plant Pot experiment (PP) or Field study (F)

Ref. 11











IPM considerations, this study also found that the treatments did not influence grain yield and that maize can tolerate considerably higher Diabrotica numbers without damage than the standard economic threshold of one beetle per plant. In the US, experiments23 with reduced rate soil drenching of ash trees with imidacloprid did not impede parasitism of the emerald ash borer beetle, an invasive pest, or harm reproduction of two of three predatory mite biocontrol agents. Reviewing environmental impact of neonicotinoid seed treatment of sugar beet in Europe, researchers estimated that exposure of non-target organisms via dust drift at sowing or guttation fluids from treated plants seemed unlikely, although they also highlighted the potential to reduce the area treated with neonicotinoids as damaging pest levels do not occur in every field each year24. Nevertheless, several research teams raise concerns about what their results mean for Integrated Pest Management. Krischik and colleagues15 draw attention to the extremely high level of neonicotinoid residues that are found in treated ornamentals in US plant nurseries and urban landscapes compared with cereal seed treatments, with imidacloprid concentrations measured in ornamental flowers between several hundred and more than a thousand times the levels in oilseed rape pollen. They warn that use of systemic neonicotinoids at current greenhouse/nursery rates reduces survival of beneficial insects which feed partially on pollen and nectar and is incompatible with the principles of IPM. Looking at effects of 14 different insecticides used in blueberry production on four natural enemy species

“Neonicotinoid use may not be com patible with conserving pollinators and biological contro l organisms, whi ch are vital compo nents of IPM prog rams. Reducing neonic otinoid use on flo wering plants grown in greenhouse, nurs ery, and landscapes mer its additional re search and advocacy.” Vera Krischik & co lleagues, University of Minne sota, 2015

available as commercial biocontrol agents, Roubos and colleagues25 documented high mortality to all four species from the broad-spectrum insecticides assessed, compared with little effect from products approved for organic production and some selective products. However, they noted that the neonicotinoid acetamiprid, although registered in the US as a ‘reduced risk’ insecticide, consistently caused significant acute effects to natural enemies exposed via treated surfaces even 14 days after application. In the European context, acute toxicity effects of thiacloprid on the predatory bug Macrolophus pygmaeus reached 100% mortality in pot plant tests12, warranting its classification as ‘Harmful’ according to the rating scheme of the International Organisation for Biological Control for pesticide side-effects on natural enemies, while four non-neonicotinoid insecticides were rated as ‘Harmless’ or ‘Slightly Harmful’. Considering also thiacloprid’s sublethal effects on the predator’s feeding and other behaviour, these authors highlighted that thiacloprid use is not compatible with this common generalist predator in Mediterranean agroecosystems.


In China, researchers16 raised caution about the compatibility of thiamethoxam with IPM strategies for major whitefly pest Bemisia tabaci, given its high toxicity and effects on feeding behaviour of the ladybird Serangium japonicum which is increasingly available as a biocontrol agent. Another Chinese team13 concluded from their research on ladybirds that current application rates of imidacloprid in cotton cultivation in China are likely to pose risks to these natural enemies, which play an important role in keeping pests under control in cotton systems.

Economic relevance for pest management There is now evidence building that neonicotinoids can disrupt biological control processes in the field. One study from Californian citrus groves9 documented how both foliar sprays and systemic treatment with imidacloprid suppressed populations of key natural enemies (parasitic wasps, ladybirds and predatory mites). The foliar applications had little effect on major pests but the reduction of their natural enemies allowed scales and mites to maintain higher populations in the treated areas compared with untreated areas and the authors concluded that imidacloprid was not therefore compatible with citrus Integrated Pest Management (IPM) strategies. Investigations on landscape trees in New York parks26 following trunk or root injections with imidacloprid to control beetle pests revealed another case of unintended impact on predators. In this case, a previously harmless spider mite species rose to outbreak levels, partly due to reduced consumption by predator

Praying mantis in cotton foliage. Credit: PAN Ethiopia

species which had been poisoned by eating contaminated prey. Imidacloprid was also shown to increase the breeding rate of the spider mite. In 2015, an important new study27 provided clear evidence of natural enemy disruption in soybean fields in Pennsylvania, USA. The researchers looked at how soybean plants grown from thiamethoxamtreated seed might be consumed by the grey garden slug Deroceras reticulatum, which often attacks young plants. Slugs, along with some snail species, are not generally affected by neonicotinoids. They are commonly preyed on by predatory ground beetles so the question was whether the seed treatment might affect these, or other predators, at the next level up from slugs in the food chain. Lab studies showed that slugs readily ate soybean seedlings treated with popular products containing a mixture of fungicide and thiamethoxam, but without harmful effects to slug survival, growth or behaviour.


Ground beetles Chlaenius tricolor were then enclosed with slugs that had fed on untreated, fungicidetreated or thiamethoxamtreated seedlings. There were no ill effects for beetles from consuming the first two treatments but the majority of beetles that consumed slugs from either high or low dose thiamethoxam treatments were impaired, with symptoms ranging from mild motor control difficulty, through to partial paralysis or death. The team then ran field trials to see whether similar food chain effects could be seen in real life settings. In the first 5 weeks after planting soybean, slug predating beetle activity-density dropped by 31% in bean plots treated with thiamethoxam, and reduced predation by 33%, while the activity-density of slugs increased by 67%. The neonicotinoid seed treatment had a long-lasting effect too, with slug numbers higher in treated plots up till the end of the crop season. This resulted in a decrease in soybean yields, compared with untreated plots. This important study has revealed a previously unconsidered ecological pathway through which neonicotinoid use can unintentionally reduce biological control and crop yield (Box 1). It also challenges the notion that seed-applied neonicotinoids precisely target plant-feeding pests and highlights the need to consider predatory arthropods and soil communities in neonicotinoid risk assessment and stewardship28.

“In most cro pping systems, neo nicotinoid seed treatme nts are being used o utside of an IP M framework, a nd as we sho w, this indiscriminate use can have u nintended consequence s, with measu rable costs for farmers� Margaret Doug las & colleague s, University of Pe nnsylvania, 2015

The same researchers conducted a recent meta-analysis29 of published field studies from North America and Europe to answer the question whether natural enemy abundance was less affected by neonicotinoid seed treatment, as is often assumed, than alternative insecticide options, such as pyrethroids applied to soil or sprayed on foliage. Their results showed that seed-applied neonicotinoids reduced the abundance of predatory arthropod natural enemies, by around 10-20% compared to untreated controls. This level of reduction is similar to how predatory insects are impacted by commonly used pyrethroids, challenging the widely-held assumption that neonicotinoid seed coatings have little to no effect on predatory insect populations30. The authors concluded that substituting pyrethroids for seedapplied neonicotinoids, or vice versa, will have little net effect on natural enemy abundance. Their analysis also confirmed earlier findings that neonicotinoid seed treatments are generally less toxic to spiders and mites than to other invertebrate natural enemies.


Conclusions Natural enemies contribute billions of dollars a year to agriculture through their elimination of crop pests. A growing number of scientific studies show that neonicotinoid insecticides, applied to the soil, as foliar sprays or as seed treatments (their most widespread use), can affect natural enemies of insect pests. Lab studies have detailed acute toxicity effects and sub-lethal effects on feeding and reproduction, including via feeding on prey species which fed on treated plant tissue. Recent field research provides evidence that these unintended side- effects

can disrupt biological control in some situations, with economic consequences for farmers. Researchers are also questioning whether neonicotinoids can be used as part of an IPM programme or if they should be considered as incompatible with the use of naturally occurring or commercial biocontrol agents.

Box 1. Unintended ecological consequences: how seed treatments can end up reducing crop yields In their field experiments, Douglas and colleagues looked at the soybean plant density and yield in thiamethoxam-treated versus untreated plots and found a significant difference, with the crop density decreased by 19% and yield of beans 5% lower than in untreated plots. Analysing neonicotinoid residues within fieldcollected slugs showed very high levels (up to 500 parts per billion at bean seedling emergence) in those from treated plots. The authors highlight that their set of lab and field experiments reveals a new phenomenon of slugs passing neonicotinoids up the food chain from treated plants to their predators, at concentrations that can impair and even kill the predators. This disruptive effect on the level of biological control normally provided by beetles then resulted in a larger slug population, which hindered the establishment of soybean seedlings and ultimately decreased yield in fields treated with thiamethoxam. They note too how their results contradict claims that neonicotinoid seed treatments should have negligible effect on natural enemies because the insecticide is ‘targeted’ inside the plant. Instead, this research proves that natural enemies can be exposed indirectly via contaminated prey and they conclude that this type of exposure, via nontarget pests, could be especially disruptive to biological control because it affects precisely those natural enemies that eat the pests.

The environmental risk assessment process in use today for evaluating the risks of pesticides to bees (and other non-target organisms) was designed in an era before the widespread use of systemic pesticides.The ecotoxicity tests which pesticide manufacturers must submit before their pesticide is approved and the decision-making

procedures by governmental risk assessors were developed for older generation insecticides that were mainly applied by spraying crop foliage.These insecticides tended to degrade in the environment within a few days so the main exposure scenarios assessed for risks to honeybees were acute, contact toxicity during spraying or from contact with recently treated foliage1. This approach has come under fire


Pesticide Action Network UK Can restrictions on systemic insecticides help restore bee health? This fact sheet discusses why it is difficult to give a clear answer to this question, looking at France’s early suspensions of imidacloprid and possible reasons why these were not immediately accompanied by a decrease in hive losses. It then describes clearer results from Italy’s recent bans on maize seed treatment. It shows there is no evidence for adverse economic impacts to farmers from these neonicotinoid restrictions as soil pests rarely caused problems on maize grown from untreated seeds. The effectiveness of current EU and national risk mitigation measures for the increasing reliance on neonicotinoid products in seed and spray applications is questioned.

Credit: Graham White

Have any neonicotinoid seed treatment ‘bans’ stopped the harm to bees? This question has been raised by many people, including stakeholders who oppose the current use restrictions in countries such as France and Italy1. It is very difficult to answer properly

for several reasons. Firstly, honey bee losses and population declines are certainly multi-factored, involving reduction in adequate and good quality foraging sources, habitat degradation, reduced immune system defences to parasites and diseases, as well as increased exposure to


Pesticide Action Network UK Opportunities to expand and improve pollinator habitats This fact sheet looks at how farmers, gardeners and land managers can modify their practices to provide more food and water sources and improve habitat quality for for these insects. It highlights how moving to more bee-friendly practices can deliver other benefits too – for wildlife and for people.

Credit: Stephanie Williamson, PAN UK

Bee-friendly practices in farming The transformation of the farming landscape and practices over the last two generations has had profound impacts on wildlife and wild flowers. More intensive, specialised systems, aiming for high yield outputs through increased use of agrochemical, fossil fuel and other inputs, have contributed to the loss of many habitats and landscape features, natural resource degradation and decline of useful

biodiversity across Europe1. The intensification trend has also reduced landscape elements (e.g. hedgerows, ponds) and enlarged farm and field sizes2. However, there are several practical measures that farmers of all types can take to help restore ecological balance, by providing more resources for pollinating insects and reducing harm from pesticides. The following aspects mainly concern conventional farmers as organic systems tend to be much better for pollinators, however some of the


Pesticide Action Network UK Persistence of neonicotinoids and widespread contamination In 2012, Pesticide Action Network UK (PAN UK) produced a series of fact sheets looking at the impact that pesticides are having on bees and other pollinator species in the UK and globally. We have aimed to set out clearly for the general public and experts alike the facts on the issues based on the most up to date published scientific studies. The PAN UK factsheets look at key issues regarding pesticides and bee and pollinator species. They have covered topics such as the overuse of herbicides and the resulting loss of habitat for pollinators, alternatives to pesticides that farmers and others can use, contrasting policies in UK with other EU countries as well as the much debated issue of neonicotinoid insecticides and pollinator exposure via treated seed.

Credit: Graham White

In the four years since we published the first factsheets neonicotinoids and their use have been a particularly important issue, with much more evidence documented of their potential risks and harm. Many studies have linked the growth in the use


of neonicotinoids and some other systemic insecticides with serious harm to honey bee populations, declines in wild bee populations and harmful effects on a range of other species including many pollinators and other invertebrates and bird species.

July 2016

Sub-lethal toxicity to bees and other pollinators is the most likely exposure scenario in the field from neonicotinoid seed treatments1,2 because generally the concentrations that are found in pollen and nectar from seed-treated plants are too low to cause immediate

bee deaths from acute poisoning3,4. However, lethally toxic levels in seed coating dust released at sowing stage have been documented in several countries (see Factsheet 1 on exposure routes) and found in stored pollen in some US hives5. Sub-lethal effects reported in the scientific literature6 include a range of behavioural disturbances in honeybees:


Pesticide Action Network UK Different regulatory positions on neonicotinoids across Europe Over recent years, several EU countries have taken regulatory actions to restrict the use of specific neonicotinoids in order to protect honey bees. This fact sheet describes the current status of these pesticides and contrasts these precautionary, although limited measures, with the lack of regulatory action in the UK. It discusses how different national positions reflect uncertainties in understanding field impacts, disagreements among stakeholders on harmful effects and the controversies when decision makers take a non-transparent approach to looking at all the evidence. Latest events demonstrate how this policy environment is constantly changing.

Credit: Graham White

Current state of play on restricted neonicotinoids in different EU countries This section summarises specific restrictions imposed on neonicotinoid and other systemic insecticides (fipronil) in four EU countries, with brief information on how long


these have been in place and any earlier restrictions now lifted. Note that many on-line sources on bee declines incorrectly describe these as national bans on neonicotinoids. This is misleading as they are generally quite narrow restrictions on the use as seed treatments of specific active ingredients on specific crops.

Pesticide Action Network UK What could farmers do to rely less on neonicotinoids? This fact sheet discusses issues around reducing use of neonicotinoids. Many farmers have become over-reliant on neonicotinoids as an ‘insurance policy’ – a tactic which goes against the key Integrated Pest Management principle of only using chemicals based on actual need. Promising developments in reducing pesticide reliance in general in arable cropping systems are described, before looking at potential alternatives to neonicotinoids in oilseed rape. Challenges in reducing neonicotinoid reliance are identified, along with the need for farmer advisory support and policy measures.

Credit: Graham White

A wide range of pests are targeted with neonicotinoid applications in different cropping systems in Europe and the US. Seed treatments in maize, sunflower and oilseed rape (OSR) are used to protect seed and young plants from wireworms ,cutworms, western corn rootworm, aphids and leafhoppers1.

In the UK neonicotinoids are used for various soil-dwelling insect pests in wheat, maize and other cereals, in sugarbeet and OSR. Neonicotinoids may be sprayed against aphids and other sucking pests in UK apple and pear orchards and vegetables and fruits grown in greenhouses. They are also used as soil treatments in


Pesticide Action Network UK Action on neonicotinoid and other bee-toxic pesticides This factsheet brings readers up to date on the changing policy and lobbying context around pesticide links with pollinator declines. Consensus is growing that not only does the risk assessment for bees need to change radically but policy actions must be taken to reduce pollinator exposure to harmful pesticides. It looks at opportunities in the EU policy agenda, while recognising the obstacles posed by vested interests and their undue influence over decision makers. NGO campaigns and first steps by food supply chains are discussed. It concludes with twelve points for action called by PAN UK.

Credit: Graham White

Consensus growing on the need for action Over the last two years, voices at global and regional levels point to the need to address the issue of unintended pesticide harm, as one of the factors in the complex puzzle of pollinator declines1,2,3. With the publication of many of the scientific papers cited in these factsheets,

consensus has been growing that chronic, low dose exposure of pollinators to neonicotinoid pesticides is significant and that colonylevel impacts are likely to involve interactions between bee parasites and diseases, pesticide exposure from different sources and impaired ability of colonies to maintain a healthy immune response.


Pesticide Action Network UK Neonicotinoids and harm to natural enemies of pests Many different species of insects and other invertebrates prey on the plant-feeding insects which attack crops. Ladybird beetles and spiders are familiar garden examples. There are also parasitic insects, which lay their eggs in or on pests (such as aphids or caterpillars), from which the hatching larvae slowly consume their host. Along with insect-feeding birds, bats, frogs and others, these invertebrates are known as ‘natural enemies’ and perform the very important but often underestimated service of providing biological control of pests. Insect natural enemies can make a significant contribution to keeping pests in check in farmers’ fields but they are often highly sensitive to pesticides and easily harmed by applications of many commonly used products. This factsheet looks at recent research showing that the neonicotinoid group of insecticides may be harming valuable natural enemies, as well as pollinators.

Ladybirds mating on a cotton leaf. Credit: PAN Ethiopia


June 2017

Bee Declines & Pesticides factsheet 2

Subtle but important effects from doses that do not kill bees outright

Bee Declines & Pesticides factsheet 4

Credit: Graham White

An outdated approach to risk assessment

Credit: Graham White

Bee Declines & Pesticides factsheet 6

This factsheet summarises the main weaknesses in the current risk assessment process for neonicotinoid and other systemic pesticides as carried out in the EU and US. It discusses why the tests required before approving pesticides are inadequate to understand the special risks that systemic pesticides pose to bees and other pollinators. It also highlights the need to consider interactions between different pesticides and with bee diseases and parasites.

This factsheet summarises current knowledge about sub-lethal (i.e. non-fatal) effects of these insecticides and possible impacts of exposure to very low doses over time. It discusses the difficulties in extrapolating results which demonstrate harm in laboratory and semifield studies to the reality in the field - one of the main controversies in the neonics debate – and implications of the latest research findings.

Bee Declines & Pesticides factsheet 8

Pesticide Action Network UK Serious shortcomings in assessing risks to pollinators

Pesticide Action Network UK Sub-lethal and chronic effects of neonicotinoids on bees and other pollinators

Bee Declines & Pesticides factsheet 10


Bee Declines & Pesticides factsheet 3

This is the most well-known and obvious route, when insecticides are sprayed onto crop foliage. Bees are at high risk when spraying takes place when crops are in flower and bees are foraging in the crop or close by. They can be directly covered in the spray, pick up traces when in contact with recently treated foliage or get hit by spray drift. Because of this high

risk, many broad-spectrum insecticides (ones which are toxic to a broad range of insects) carry hazard warnings on the product label, recommending farmers to avoid spraying when crops or nearby weeds are in flower or when bees are foraging in the crop. Spraying early in the morning or in the evening or on cloudy days can also help to reduce the risk of harming honeybees, because they don’t tend to forage at these times. Bumblebees, however, forage at lower temperatures

Bee Declines & Pesticides factsheet 5

Credit: Stephanie Williamson, PAN UK

Route A: Direct contact via crop spraying

Bee Declines & Pesticides factsheet 7

Bees and other pollinators can be exposed to highly toxic pesticides by a variety of routes, some of which have only recently become apparent. Worryingly, several of these routes are not considered at all in the risk assessment process before a pesticide is approved. This factsheet summarises recent understanding of the different exposure routes (A to D below) for neonicotinoid and some other bee-toxic pesticides.

Bee Declines & Pesticides factsheet 9

Pesticide Action Network UK Different routes of pesticide exposure

Bee Declines & Pesticides factsheet 1


In this series If you would like to find out more about the relationship between pesticides and pollinator declines, all of these leaflets are available at www.pan-uk.org/recources Bee Declines and the Link with Pesticides. Summary leaflet. Fact sheets (2012): 1. Different routes of pesticide exposure 2. Sub-lethal and chronic effects of neonicotinoids on bees and other pollinators 3. Serious shortcomings in assessing risks to pollinators 4. Different regulatory positions on neonicotinoids across Europe 5. Can restrictions on systemic insecticides help restore bee health? 6. What could farmers do to rely less on neonicotinoids? 7. Opportunities for improving and expanding pollinator habitats 8. Action on neonicotinoid and other beetoxic pesticides Fact sheets (2016): 9. Persistence of neonicotinoids and widespread contamination Fact sheets (2017): 10. Persistence of neonicotinoids and widespread contamination

12 References 1. Hopwood, J. et al. (2013) Beyond the birds and the bees. Effects of neonicotinoid insecticides on agriculturally important beneficial invertebrates. Xerces Society, US.Via: http://www.xerces. org/2013/09/24/new-report-beyond-the-birds-and-the-bees/ 2. Cloyd, R.A. and Dickinson, A., 2006. Effect of insecticides on mealybug destroyer (Coleoptera: Coccinellidae) and parasitoid Leptomastix dactylopii (Hymenoptera: Encyrtidae), natural enemies of citrus mealybug (Homoptera: Pseudococcidae). Journal of Economic Entomology, 99 (5) 1596-1604. 3. Peck, DC. (2009) Long-term effects of imidacloprid on the abundance of surface- and soil-active nontarget fauna in turf. Agric. & Forest Entomology 11 405-419 4. Seagraves, M.P. and Lundgren, J.G., 2012. Effects of neonicitinoid seed treatments on soybean aphid and its natural enemies. Journal of Pest Science, 85(1) 125-132 5. Krischik,VA, Landmark, AL & Heimpel, GE. (2007), cited in Hopwood et al., 2013 6. Smith, SE & Krischik,VA. (1999), cited in Hopwood et al., 2013. 7. Paine, TD, Hanlon, CC & Byrne, FJ. (2011), cited in Hopwood et al., 2013 8. Castagnoli, M et al. (2005), cited in Hopwood et al., 2013 9. Grafton-Cardwell, EE & Gu, P. (2003), cited in Hopwood et al., 2013 10. Papachristos, DP & Milonas, PG.(2008), cited in Hopwood et al., 2013 11. Frewin, AJ, Schaafsma, AW & Hallett, RH. (2014) Susceptibility of Aphelinus certus (Hymenoptera: Aphelinidae) to Neonicotinoid Seed Treatments used for Soybean Pest Management. Journal of Economic Entomology 107 (4) 1450-1457 12. Martinou, F, Seraphides, N & Stavrinides, MC. (2014) Lethal and behavioral effects of pesticides on the insect predator Macrolophus pygmaeus. Chemosphere 96, 167–173 13. Yu, C, Lin, R, Fu, M, Zhou,Y, Zong, F, Jiang, H, Lu, N, Piao, X, Zhang, J, Liu,Y & Brock, TCM. (2014) Impact of imidacloprid on lifecycle development of Coccinella septempunctata in laboratory microcosms. Ecotoxicology and Environmental Safety 110, 168–173 14. Fountain, MT & Harris, AL. (2015) Non-target consequences of insecticides used in apple and pear orchards on Forficula auricularia L. (Dermaptera: Forficulidae) Biological Control 91 2733 15. Krischik V, Rogers M, Gupta G & Varshney, A. (2015) Soil-Applied Imidacloprid Translocates to Ornamental Flowers and Reduces Survival of Adult Coleomegilla maculata, Harmonia axyridis, and Hippodamia convergens Lady Beetles, and Larval Danaus plexippus and Vanessa cardui Butterflies. PLoS ONE 10(3): e0119133. 16. Yao, FL, Zheng,Y, Zhao, JW, Desneux, N, He,YX & Weng, QY. (2015) Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere 128 49–55 17. Moscardini,VF, Gontijo, PC, Michaud, JP et al. (2015) Sublethal effects of insecticide seed treatments on two nearctic lady beetles (Coleoptera: Coccinellidae). Ecotoxicology 24 (5) 1152–1161

18. Zhang, P, Zhang, XF, Zhao,Y, Ren,Y, Mu, W & Liu, F. (2015) Efficacy of granular applications of clothianidin and nitenpyram against Aphis gossypii (Glover) and Apolygus lucorum (Meyer-Dür) in cotton fields in China. Crop Protection 78 27–34 19. Xiao, D., Zhao, J., Guo, X. et al. (2016) Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology 25: 1782 20. Boopathi, T, Sankari Meena, K, Ravi,M & Thirunavukarasu, K. (2017) Impact of insecticides on spiralling whitefly, Aleurodicus dispersus (Hemiptera: Aleyrodidae) and its natural enemy complex in cassava under open field conditions. Crop Protection 94, 137–143 21. Botías C, David A, Hill EM and Goulson D. (2016) Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects. Science of the Total Environment 566–567 269–278 22. Rauch, H et al. (2017) Field efficacy of Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae), Metarhizium brunneum (Hypocreales: Clavicipitaceae), and chemical insecticide combinations for Diabrotica virgifera virgifera larval management. Biological Control 107 1–10 23. Davidson,W & Rieske, LK. (2016) Establishment of classical biological control targeting emerald ash borer is facilitated by use of insecticides, with little effect on native arthropod communities. Biological Control 101 78–86 24. Hauer, M et al. (2017) Neonicotinoids in sugar beet cultivation in Central and Northern Europe: Efficacy and environmental impact of neonicotinoid seed treatments and alternative measures. Crop Protection 93 132–142 25. Roubos, C.R., Rodriguez-Saona, C., Holdcraft, R., Mason, K.S. and Isaacs, R. (2014) Relative toxicity and residual activity of insecticides used in blueberry pest management: mortality of natural enemies. Journal of Economic Entomology 107 (1) 277-285. 26. Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ (2011) Neonicotinoid Insecticide Imidacloprid Causes Outbreaks of Spider Mites on Elm Trees in Urban Landscapes. PLoS ONE 6(5): e20018. doi:10.1371/journal.pone.0020018 27. Douglas, MR, Rohr, JR and Tooker, JF. (2015) Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield. J. Applied Ecology 52 250-260 28. JAE (2014) Editor’s Choice: Silent Spring redux? Insecticides cascade up a food chain to poison carnivores. Journal of Applied Ecology.Via: http://www.journalofappliedecology.org/view/0/ editorschoice521.html 29. Douglas, MR & Tooker, JF. (2016) Meta-analysis reveals that seedapplied neonicotinoids and pyrethroids have similar negative effects on abundance of arthropod natural enemies. PeerJ 4:e2776 30. Science Daily (2016) Common insecticides are riskier than thought to predatory insects. Science News release, December 7, 2016.Via: https://www.sciencedaily.com/ releases/2016/12/161207151257.htm

PAN UK’s vital work in the UK and in developing countries Pesticide Action Network UK is a registered charity dedicated to:• Eliminating the most hazardous pesticides, • Reducing dependence on chemical pesticides, • Promoting sustainable and equitable food systems and increasing the use of alternatives to chemical pest control in agriculture, urban areas, public health and homes and gardens

make a decent living without putting their own health, their families or their environment at risk. Populations of bees and other insect pollinators have fallen dramatically in recent years. The reasons for these declines are complex and wide ranging, but there is little doubt that pesticides are playing a key part. PAN UK has prepared these fact sheets to cut through the confusion and provide an up-to date and balanced explanation of the role of pesticides in pollinator declines. To find out more and what you can do, please visit http://bees.pan-uk.org

In the UK, we campaign for tighter regulatory controls on pesticides and encourage retailers to tackle pesticide problems in their supply chains. We provide advice on alternative ways to control pests and work with local communities to reduce public exposure to pesticides. In the developing world, we raise awareness about pesticide hazards and train farmers in organic and low input agricultural techniques to help them to

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Published by Pesticide Action Network UK. June 2017

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Bee Declines & Pesticides Factsheet 10  

June 2017

Bee Declines & Pesticides Factsheet 10  

June 2017

Profile for pan-uk