A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators

(1) Wild and managed insect pollinators play a critical role in the production of a variety of different foods (and in the case of honeybees also produce various ‘hive products’ of which the most important is honey) and are an important functional and cultural component of biodiversity. Insecticides are applied to crops to control insect pests and make a very important contribution to achieving high yields. Insecticides kill insects and thus clearly have both positive and negative effects on different aspects of food security and the environment. Concern has been expressed by a number of bodies that neonicotinoid insecticides may be harming pollinators and a partial restriction on their use in the EU came into force across all 28 member states in December 2013 (to be reviewed after 2 years). Other bodies have criticized this decision, arguing that the benefits of neonicotinoid use outweigh their costs.

(2) The aim here is to provide a succinct summary of the evidence base relevant to policy-making in this area as of April 2014. It also provides a consensus judgement by the authors on the nature of the different evidence components; a consensus arrived at using the studies listed in the annotated bibliography. We use the following descriptions, which explicitly are not a ranking, indicated by abbreviated codes. Statements are considered to be supported by:

(3) The review focuses on the natural science evidence relevant to pollinator policy in the EU but includes relevant data from other regions; its scope does not include evidence from social sciences and economics. The statements are based on the evidence in the peer-reviewed scientific literature, though the annotated bibliography also notes the existence of information in non-reviewed reports and industry studies.

(4) Insect pollinators are required to achieve optimum yield and quality for a number of important food crops. The most economically significant crops in the UK include oilseed rape (canola), soft fruits (strawberry, raspberry, etc.), top fruits (apple, pear, plum, etc.) and vegetables (courgettes, runner beans, tomato, etc.), whereas in continental Europe sunflower, peaches, melon and other crops are also important. Insect pollinators are important for both field crops and those grown under glass, though in their absence some crops can, to differing extents, be wind- or self-pollinated without the involvement of insects. Many plant species in pastureland and non-agricultural habitats require insect pollinators for successful reproduction [D_ata].

(5) A lack of pollinators can reduce crop yields and quality [D_ata], and there is some evidence that pollinator diversity can reduce the variance in pollination and hence improve crop yield stability [S_{upp_ev}]. Where insect-pollinated crops are grown in glasshouses or ‘polytunnels’ the introduction of pollinators can be particularly important for both quality and quantity of yield [D_ata]. There is emerging evidence for the potential of economically significant pollination deficits in some UK field crops in some years [S_{upp_ev}], but data do not currently exist to determine whether observed changes in pollinator abundance and diversity (see para. 7) have affected the economic value of crop yields [E_{xp_op}].

(6) Pollination may be carried out by wild or managed insects. The most important pollinators for crops include honeybees, which are native to Europe (their status in the British Isles is unclear [E_{xp_op}]) but are now almost entirely managed, bumblebees, solitary bees and true flies (including hoverflies).¹ Other pollinators such as butterflies and moths are not as important for crop pollination, particularly in northern temperate regions, but do pollinate wild plant species. Wild pollinators can be viewed as an element of natural capital² that provides (with managed species) pollination, an ecosystem service of economic importance to society. Pollinators are also an important component of a nation's biodiversity [D_ata].

(7) Data from volunteer recording schemes that record species presence (but not abundance or absence) have revealed changes in the diversity and distribution of pollinators. In Great Britain, The Netherlands and Belgium (where the best data exist) the average numbers of species of bumblebees, butterfly and moths, and solitary bees in different areas have declined since the 1950s [D_ata]. There is some evidence of a recent slowdown in the rate of decline in species richness (for bumblebees in all three European countries) and also some increases (solitary bees in Great Britain and The Netherlands but not in Belgium where the decline continues) [D_ata]. The data for hoverflies are more complex with species richness reported to have increased, decreased or remained unchanged depending on location and the geographical scale of the analysis. Long-term published data on abundance are only available for butterflies and moths and show reductions in abundance of many, but not all, species [D_ata]. There are several potential (and non-exclusive) explanations for these observed changes in pollinator biodiversity with evidence suggesting habitat loss and alteration to be the most important causes of the decline [S_{upp_ev}]. There is not a consensus on the reason(s) for recent slowdowns or reversals in the rates of species loss [E_{xp_op}].

(8) Honeybees throughout Europe (and elsewhere) have been severely affected by the introduction of the Varroa destructor mite which both parasitizes bees and acts as a vector for a number of debilitating and paralytic honeybee viruses [D_ata]. In addition, honeybee colony losses have increased in frequency across Europe and the USA because of overwintering mortality [D_ata] which is thought to arise from multiple factors, including adverse weather, poor nutrition as well as parasites and disease [S_{upp_ev}]. Some of these losses in the USA have been ascribed to a particular syndrome, colony collapse disorder, though its precise nature is debated [E_{xp_op}]. Not all parts of the world have experienced recent increases in overwintering colony mortality [D_ata].

(9) Neonicotinoids are a relatively new class of insecticide, introduced in the early 1990s. They target the nicotinic acetylcholine receptor (nAChR) with high affinity for insect receptors and low affinity for mammalian receptors and have relatively low (but not zero) mammalian and bird toxicity. They can be used as sprays, applied to soils as drenches or in granular form, introduced into irrigation water or injected into trees. However, they are most frequently (approx. 90% by volume in the UK) applied as seed treatments with the insecticide being taken up systemically by the growing plant. The convenience and cost-effectiveness of seed treatments, the development of resistance to other classes of insecticide by many insect pests, and restrictions on the use of other compounds, have resulted in neonicotinoids capturing 28.5% of the global insecticides market (2011; worth US$3.6B) and their wide use in Europe [D_ata].

(10) Five neonicotinoids are approved for use in the EU: three from the N-nitroguanidine group—clothianidin, imidacloprid and thiamethoxam (metabolized to clothianidin in the plant, insect and environment); and two from the N-cyanoamidine group: thiacloprid and acetamiprid. Concern over their possible effects on pollinators has focused on the first three because they are the most used compounds, they have greater honeybee toxicity and they are used as seed treatments so can be present in the pollen and nectar of treated crops [D_ata].

(11) In Europe (and elsewhere), environmental risk assessments of pesticides including all neonicotinoids are required before a product can come to market. A tiered approach has been adopted to ensure cost-effectiveness and proportionality. The tiers start with laboratory tests to determine hazard to a standard set of seven non-target organisms (including honeybees) and, if potential hazards are identified, may progress through more complex semi-field experiments and modelling to simulate exposure under different more realistic conditions, culminating with full-scale toxicity assessments to identify potential risks in the field. Field trials were conducted during the original environmental risk assessment process for neonicotinoids. Extensive data are often generated during the registration process but typically is not placed in the public domain, except in summary form [D_ata].

(12) Neonicotinoids have been widely used in Europe as a seed treatment for oilseed rape, sunflowers, maize, potato, soya bean (and other crops such as cereals and beets not visited by pollinators).

(13) The plant absorbs some of the insecticide from the seed treatment and as it grows the insecticide spreads to all plant parts including the nectar and pollen that bees and other pollinators collect and consume [D_ata].

(14) Some plants secrete droplets of liquid (xylem sap) called guttation fluid at leaf tips or margins. High concentrations of neonicotinoids have been measured in the guttation fluid of seed-treated plants (up to 10⁴–10⁵ times that in nectar), especially when plants are young [D_ata]. There has been concern that were pollinators to use guttation fluid as a source of water they would ingest highly toxic levels of insecticides. The available evidence does not suggest that pollinators collect guttation fluid containing neonicotinoids to any great extent, in part because it chiefly is present at times of the year when crops are unattractive to pollinators and other sources of water are present [E_{xp_op}].

(15) Dust emitted from seed drilling machines can contain high concentrations of neonicotinoids; as well as being deposited on the soil, the dust can drift to contaminate neighbouring flowering crops and natural vegetation as well as surface waters. Sporadic incidents of mass honeybee mortality in several EU countries, the USA and Canada have been caused by dust from seed drilling machines [D_ata].

(16) Neonicotinoids introduced into the environment as seed treatments can affect soil insects and other invertebrates, effects considered in insecticide evaluation and registration. They persist in the environment with typical half-lives estimated to be of the order 15–300 days (with some longer estimates from laboratory studies and in the field under drought and freezing conditions). There is evidence that neonicotinoids can accumulate in soils when treated crops are grown repeatedly in the same field. Neonicotinoids can sometimes, but not always, be detected in weeds or in subsequent crops grown in the same soil, though when present the concentrations are considerably lower than in the target crop. Neonicotinoids have been detected in surface or groundwater around fields where they have been used as seed treatments [S_{upp_ev}].

(17) Bees bring pollen and nectar (which in social bees is often extensively modified post-ingestion) to their hives or nests to feed their developing larvae [D_ata] which thus may have different patterns of exposure and susceptibility compared with adults (see also para. 24) [S_{upp_ev}].

(18) The risk of exposure to neonicotinoids for different pollinator species will be influenced by many aspects of their biology and ecology including body size, flower preference, whether they are a social species, and whether the time of year at which they are active (or in the case of social species experiencing rapid colony growth) coincides with the flowering of neonicotinoid-treated crops. There may also be differences in the physiological susceptibility of different pollinator species to neonicotinoids [E_{xp_op}].

(19) The exposure of pollinators to neonicotinoids will be affected by the distribution of flowering crops in the landscape, the fraction that are treated with neonicotinoids, the length of time the treated crops are in flower, and the availability of alternative, suitable floral resources (including weeds and managed resources in floral strips, wildflower headlands, untreated crops, etc.) and whether they are contaminated with insecticide. Over multiple years the frequency of treated crops in agricultural rotations will affect long-term population exposure [E_{xp_op}].

(20) The distance between treated fields and nest sites or honeybee hives will affect insect exposure to neonicotinoids [E_{xp_op}].

(21) Summary. There are several proven pathways through which pollinators may be exposed to neonicotinoid insecticides applied as seed treatments (or in other ways). Quantitative information about the extent and significance of these different routes in the published literature is poor [E_{xp_op}].

(22) Estimates of LD₅₀s (see Endnote 4) for different neonicotinoid-pollinator combinations are available, although a majority of the studies have considered only the honeybee [D_ata.].

(23) Prolonged exposure of pollinators in the laboratory to doses of neonicotinoids that do not cause immediate death can reduce longevity (chronic toxicity). Because chronic effects can be estimated in many different ways, comparisons are harder than for acute toxicity [D_ata].

(24) Effects of neonicotinoids on adult pollinators have been detected in the laboratory at doses substantially below those that cause death. At the lowest doses responses involve metabolic changes (for example, in acetylcholinesterase activity) and subtle neurological and behavioural responses. As doses increase (including concentrations in food similar to that observed in the nectar and pollen of treated crops) olfactory learning, memory and feeding behaviour can be affected, though there is considerable variability in the results reported in different studies. When doses approach lethal concentrations substantial neurological and locomotory impairment can occur [D_ata].

(25) Sublethal effects on larval development and colony productivity have been identified in the laboratory.

(26) Stressed pollinators tend to be more susceptible to neonicotinoids (and vice versa), although data are largely restricted to honeybees [S_{upp_ev}].

(27) In interpreting these laboratory results, the following issues need to be considered:

(28) Summary. The strengths of laboratory studies are that they allow carefully controlled experiments to be performed on individual insects subjected to well-defined exposure. The weaknesses are that they are conducted under very artificial conditions (which may affect tolerance to external stress), any avoidance response by the insect is limited and hence the exposure dose and form is determined solely by the experimenter, and responses at the colony or population level are both difficult to study and to extrapolate to the field. Nevertheless, they provide important information about the range of concentrations where death or sublethal effects may be expected to occur [E_{xp_op}].

(29) Nectar and pollen collected from bees constrained to feed on treated crops have similar insecticide concentrations to those found in samples taken from the plant [D_ata].

(30) There have been few surveys of pesticide and metabolite levels in honeybees in the field. Two studies in Belgium (sample size, n = 48 and 99) and one in the USA (n = 140) found no honeybees with residues, while a survey in France conducted in 2002–2005 (n = 187) detected imidacloprid in 11% of honeybees (at concentrations of 0.03–1.0 ng per bee) [D_ata]. We are aware of no data on other pollinators [E_{xp_op}].

(31) Insecticide residues are more likely to be found in nectar and pollen collected by honeybees and in honey than in the insects themselves. Thus, the French study that found imidacloprid residues in 11% of the bees sampled also found residues in 22% of honey samples and 40% of pollen samples (mean and range: 0.9, 0.2–5.7 ng g⁻¹). Some large surveys (e.g. a Spanish study with n = 1021) found no contaminated pollen; a German study that surveyed hives (n = 215) after oilseed rape flowering found low incidence of those neonicotinoids used in seed treatments (though higher incidence of thiacloprid); an American study found imidacloprid in 3% of pollen (n = 350) and 1% of wax samples (n = 208) [D_ata].

(32) Summary. Neonicotinoids can be detected in wild pollinators as well as honeybee and bumblebee colonies but data are relatively few and restricted to a limited number of species. Studies to date have found low levels of residues in surveys of honeybees and honeybee products. Observed residues in bees and the products they collect will depend critically on details of spatial and temporal sampling relative to crop treatment and flowering [E_{xp_op}].

(33) This section discusses recent studies that have explored the consequences of providing bee colonies placed in the field with food containing insecticide, as well as experiments where the performance of colonies placed adjacent to fields treated or not treated with neonicotinoids are compared. Some earlier studies with limited statistical power are listed in the annotated bibliography [E_{xp_op}].

(34) Schneider et al. 2012 [10]. Individual honeybees were given single sublethal doses of imidacloprid or clothianidin and their foraging behaviour was monitored. Reductions in foraging activity and longer time foraging flights were not observed at field-relevant doses although negative effects were seen at doses greater or equal to 0.5 ng per bee (clothianidin) or 1.5 ng per bee (imidacloprid) [D_ata].

(35) Henry et al. 2012 [11]. Honeybees fed a single high dose of thiamethoxam (1.34 ng, equivalent to 27% of the LD₅₀) and then released away from the hive were significantly less likely to return successfully than controls. The return rate depended on the local landscape structure and the extent of the honeybees' experience of the landscape. The failure to return per trip was estimated to be up to twice the expected background daily mortality [D_ata].

(36) Whitehorn et al. 2012 [12]. Bumblebee (Bombus terrestris) colonies fed exclusively on imidacloprid-treated sugar water (at two concentrations: 0.7 or 1.4 ng g⁻¹) and pollen (either 6 or 12 ng g⁻¹) for two weeks in the laboratory before being placed in the field (for six weeks) showed reductions in growth rate and queen production. A subsequent study [13] using the same concentrations of imidacloprid found the bumblebees' capacity to forage for pollen (but not nectar) was impaired [D_ata].

(37) Gill et al. 2012 [14]. Bumblebee (B. terrestris) colonies given access to sugar water containing imidacloprid (10 ng g⁻¹) and allowed to forage for pollen and nectar in the field grew more slowly than controls; individual foragers from imidacloprid-treated colonies were less successful at collecting pollen, and treated colonies sent out more workers to forage and lost more foragers, compared to controls. Combined exposure to imidacloprid and a second pesticide of a different class (a pyrethroid) tended to reduce further colony performance and increase the chances of colony failure [D_ata].

(38) Thompson et al. 2013 [15]. Bumblebee (B. terrestris) colonies were placed adjacent to single oilseed rape fields grown from seeds that were treated with clothianidin, imidacloprid or had no insecticidal seed treatment. No relationship between the oilseed rape treatment and insecticide residues was observed, presumably because the bees were foraging over spatial scales larger than a field. Insecticide residues varied among colonies and the authors reported no evidence of a correlation with colony performance [D_ata].

(39) Pilling et al. 2013 [16]. Over a 4 year period, honeybee colonies (six per 2 ha field) were placed beside thiamethoxam-treated or control fields of maize (three replicates) or oilseed rape (two replicates) for between 5 and 8 days (first 3 years) or 19 and 23 days (fourth year) to coincide with the crop flowering period (at other times the colonies were kept in woodland presumed to have no local exposure to insecticides). Honeybees from treatment hives had higher concentrations of insecticide residues, but no differences in multiple measures of colony performance or overwintering survival were observed [D_ata].

(40) Summary. The experiments described in Paras. 33–37 involve bees artificially exposed to neonicotinoids and observed to forage in the field. They show the potential for neonicotinoids to affect the performance of individual pollinators and pollinator colonies in the field. The main issue for their interpretation is the extent to which the doses received by the bees are representative of what they will receive under normal use of neonicotinoids in the field. It appears that most studies have used concentrations at the high end of those expected in the field. The experiments described in Paras. 38 and 39 are true field experiments in the sense that the treatments involve the normal use of neonicotinoids, though only the Pilling et al. [16] study was successfully concluded and found no effects of neonicotinoids, but with limited statistical power to detect differences [E_{xp_op}].

(41) At the colony or population level, there may be processes that can compensate for the deaths of individual insects which would mitigate the potential effects of mortality caused by neonicotinoid insecticides. Thus, the deaths of individual pollinators may not lead to a simple proportionate decrease in the overall numbers of that pollinator species. In the case of rare species, extra mortality caused by insecticides could lead to a threshold population density being crossed below which the species declines to extinction, hence magnifying their effects. However, there is a weak evidence base to help understand the presence and magnitude of these effects in the field. Models of honeybee and bumblebee colony dynamics, as well as population-level models of all pollinators, are important tools to explore these effects [E_{xp_op}].

(42) There is evidence that some crops do not always receive sufficient pollination [D_ata], and further limited evidence that this has increased in recent decades [S_{upp_ev}]; but the information available does not allow us to determine whether or not this has been influenced by the increased use of neonicotinoids [E_{xp_op}]. Whether pollination deficits in wild plants have increased is not known [E_{xp_op}].

(43) Declines in the populations of many insect species in general and pollinators in particular have been observed (para. 7) although the decline in bees predate by some decades the introduction of neonicotinoid insecticides, and there is some evidence of a recent abatement in the rate of decline for some groups [D_ata]. Habitat alteration (especially in farmland) is widely considered to be the most important factor responsible. The evidence available does not allow us to say whether neonicotinoid use has had an effect on these trends since their introduction [E_{xp_op}].

(44) There have been marked increases in overwintering mortality of managed honeybee populations in recent decades (para. 8) [D_ata]. It has been suggested that insecticides (particularly neonicotinoids) may be wholly or partly responsible. The weak evidence base cannot at present resolve this question although honeybee declines began before the wide use of neonicotinoids and there is poor geographical correlation between neonicotinoid use and honeybee decline [E_{xp_op}]. Two studies using different structured methodologies have explored this question.

(45) Neonicotinoids are efficient plant protection compounds and if their use is restricted farmers may switch to other pest-management strategies (for example, different insecticides applied in different ways or non-chemical control measures) that may have effects on pollinator populations that could overall be more or less damaging than neonicotinoids. Alternatively, they may choose not to grow the crops concerned, which will reduce exposure of pollinators to neonicotinoids but also reduce the total flowers available to pollinators [E_{xp_op}].

(46) Summary. To understand the consequences of changing neonicotinoid use, it is important to consider pollinator colony-level and population processes, the likely effect on pollination ecosystem services, as well as how farmers might change their agronomic practices in response to restrictions on neonicotinoid use. While all these areas are currently being researched there is at present a limited evidence base to guide policy-makers [E_{xp_op}].