This document responds to the Science and Technology Committee’s call for evidence around insect decline and UK food security. It comments, primarily, on the effects of plant protection products on bees, with a focus on neonicotinoids. Various lines of evidence are discussed, linking the application of plant protection products to changes in biodiversity indicator populations. The document also comments on pollinator abundance in the UK, as well as on biodiversity initiatives intended to halt and later reverse species decline across England, with a primary focus on bee species.
Fera Science Ltd. (Fera) is a national and international centre of excellence for interdisciplinary investigation and problem solving across plant and bee health, crop protection, sustainable agriculture, food and feed quality and chemical safety in the environment, headquartered at York Biotech Campus. Fera is a specialist in the delivery of food security with over 100 years’ heritage of protecting the environment and supporting food production, both across the UK and globally.
In relation to pollinators, Fera has over 30 years’ experience in improving bee health and works closely with APHA’s National Bee Unit (also located on York Biotech Campus). In addition, Fera administers the Pesticide Usage Survey (national survey taken every 2-4 years) on behalf of the UK government, in collaboration with Science & Advice for Scottish Agriculture (SASA) and the Department of Agriculture, Environment and Rural Affairs (DAERA, Northern Ireland). This survey monitors a range of measures associated with the use of plant protection products, including the impact of their application on various biodiversity indicator species (e.g. bees). Fera, therefore, is a key stakeholder within UK bee health and is well placed to comment on their species decline.
This document was authored by Dr Alex Setchfield. It also includes contributing content from Rainford et al. (2023) – a recent report written by Fera for Defra, entitled “Evidence review of the impacts of plant protection products on species representative of English biodiversity”.
This document has not been published prior to this submission (dated 27th April 2023).
Global declines in flying insects over recent history have been the subject of numerous reviews – e.g. Shortall et al. (2009), Hallmann et al. (2017), Møller (2019) and Powney et al. (2019). Insect pollinators (e.g. bees, moths and butterflies), in particular, have been the focus of much of this work, owing to their direct role in pollination (a critical ecosystem service underpinning the productivity of agricultural systems) and maintenance of food security. For instance, a recent study of UK wild pollinator abundance, based on 353 wild bee and hoverfly species between 1980 and 2013, showed that a third of those species declined over the 33-year study period (Powney et al., 2019). The declines were most concentrated in solitary bees and other taxa which provide pollination services to wild communities, with upland species undergoing particularly severe declines (average = 55%). However, as noted by Graham et al. (2021), there is often a large degree of stochasticity in individual species trends, which increases the inherent complexity of linking population changes with specific drivers. As such, section 2 focusses specifically on the effects of plant protection products (PPPs) on bees (Nature’s most efficient pollinators), including honeybees, bumblebees and solitary bees.
Insect pollinators (bees in particular) are vital for the maintenance of ecosystem health and global food security, with 35% of global crop production, 75% of crop species and up to 88% of flowering plant species reliant upon insect pollinators to some degree. However, substantial concern exists around their current and future conservation status, with key threats related to agricultural intensification (e.g. habitat loss and the application of PPPs) (Powney et al., 2019).
PPPs are a fundamental part of modern-day agricultural practice, linked also to the maintenance of yield and food security (Cooper & Dobson, 2007; Popp et al., 2013). Here, they are defined as substances (or mixtures of substances) of a chemical or biological nature with pesticidal properties, that are deliberately applied to agricultural crops for the direct or indirect suppression of undesirable organisms. A recent review estimated that 10-28% of global wheat harvest is lost to pests and pathogens annually (Savary et al., 2019), with a wide range of other crops also affected. As such, PPPs are used by farmers and growers to mitigate against crop loss and increase the predictability and stability of crop yield (Carpentier & Reboud, 2018; Wilson & Tisdell, 2001).
This section of the document focusses specifically on the effects of PPPs on bees, including honeybees, bumblebees and solitary bees. Various lines of evidence are discussed, linking the application of PPPs to changes in biodiversity indicator populations, each with methodological advantages and disadvantages critically evaluated and comprehensively discussed in a recent report written by Fera for Defra (Rainford et al., 2023). The same review discusses the impacts of PPPs on Lepidoptera and a range of freshwater invertebrates, as well as breeding birds, bats, other mammals, and plants. It should be noted that much of the work on PPP derived impacts in the UK to-date has been conducted with either a national (drawing on the Pesticide Usage Survey) or highly localised focus. Consequently, impact assessments of PPPs on non-target and non-model species (most biodiversity indicators) are often disjointed and challenging to generalise beyond their original context. This, therefore, should be considered when drawing extrapolated conclusions from these data.
Here, a qualitative review is defined as an exploratory discussion of potential issues relating to the impact of PPPs on biodiversity markers, which serves as a hypothesis generation or discussion tool, but does not report quantitative measures of impact.
Pollinators have received significant attention regarding the potential impacts of PPPs on biodiversity. Honeybees (Apis mellifera), bumblebees and solitary bees are the subject of numerous reviews on the environmental impact of PPPs (David et al., 2016; Franklin & Raine, 2019; Gibbons et al., 2015; Godfray et al., 2015; Goulson et al., 2015; Main et al., 2020; Pisa et al., 2015; Woodcock et al., 2016; Woodcock et al., 2018), whilst the role that PPPs may have played in the decline of bee numbers is also a key topic in the wider discussion around global trends in invertebrate decline (Cardoso & Leather, 2019; Goulson, 2019; Hallmann et al., 2017; Sánchez-Bayo & Wyckhuys, 2019; Saunders et al., 2020; Wagner, 2020). PPPs have been shown to have a wide range of impacts on bees, including direct mortality, changes to colony structure (Doublet et al., 2015), population level change (Brittain et al., 2010; Woodcock et al., 2016) and behavioural changes (Sanchez-Bayo & Goka, 2016; Siviter et al., 2018).
Honeybees are the focus of so much attention around PPPs, largely because of their ecological importance as pollinators (an ecosystem service that has been valued at £400 mn per year in the UK alone) and role in maintaining food security. More recently, however, other non-domesticated species (e.g. bumblebees of the genus Bombus and solitary bees often represented by the genus Osmia) are increasingly playing a role as alternative model species in PPP risk assessments. The advantage here is that, in addition to their own ecological importance, results may be more comparable to other invertebrate groups, given that effects in honeybees may be confounded by their long-lived, colonial lifestyle (Franklin & Raine, 2019; Lewis & Tzilivakis, 2019).
In the UK, the links between the use of neonicotinoid seed treatments and their effects on mass flowering crops (specifically winter sown oil seed rape) have been the subject of historical focus. Such work has linked neonicotinoid use with reduced species richness in native UK bee communities (Main et al., 2020); a trend which is considered indicative of a wider diversity of different pollinating insects (Powney et al., 2019). However, neonicotinoids are far from the only group of PPPs that have been identified as of concern (Main et al., 2020; Stanley et al., 2015), with authors also highlighting indirect effects associated with the use of fungicides and herbicides (Cullen et al., 2019). For an in-depth discussion of the concerns around bees and the various ways in which these have been addressed in PPP risk assessments, see (among others) EFSA et al. (2022) and Uhl & Brühl (2019).
Here, a toxicological study is defined as an experimental setup in which an organism is directly exposed to a PPP (typically by ingestion or contact) and some physiological response is measured (e.g. mortality, inhibition of growth / reproduction), most commonly in an artificial laboratory setting. During the PPP authorisation process, simple toxicity tests are considered Lower Tier studies, and provide the most direct evidence of the relative amount of PPP to which an individual must be exposed to generate a specific experimental end point (e.g. mortality, diminished growth).
Honeybees are core model taxa for PPP risk assessments and serve as the primary model species for toxicity (Franklin & Raine, 2019), with basic acute toxicity data (oral and contact) and chronic toxicity data (e.g. developmental effects, sub-lethal effects) submitted as part of the product approvals process. Whilst this data is required for honeybees, tests on other bee species may be submitted as well. The amount of pesticide toxicity data known for non-honeybee models (most notably Bombus terrestris and Osmia spp.) is growing among recently authorised substances but remains in the minority for pesticides overall (Lewis & Tzilivakis, 2019). In a meta-analysis of published literature, Arena & Sgolastra (2014) compared the sensitivity to PPPs of honeybees (A. mellifera) and several other bee species (Apiformes). Authors concluded that the effects of PPPs on domestic and wild bees are dependent upon the intrinsic sensitivity of a particular species, as well as their specific life cycle, nesting activity and foraging behaviour. They also stressed the need for more comparative information between honeybees and non-Apis bees, as well as separate PPP risk assessment procedures for non-Apis bees. It should be noted, however, that some additional non-Apis OECD test guidelines have since been developed or are expected shortly (e.g. bumblebee acute toxicity (OECD Test No. 246 & 247) and acute test guideline on the solitary bee Osmia spp.)
Goulson et al. (2018) documented changing patterns of PPP use in arable and horticultural crops in the UK from 1990 to 2015. Over this 25-year period, the weight of PPPs used approximately halved, but the number of applications per field nearly doubled.
Authors calculated that the total potential kill of honeybees (total number of LD50 doses applied to the 4.6 million hectares of arable farmland in the UK each year) increased six-fold to approximately 3 × 1016 bees. The authors acknowledged that this calculation should not be interpreted as the actual number of bees that would be killed, but rather stated that the data suggest that the relative risk posed by PPPs to non-target insects (e.g. bees, other pollinators and natural enemies of pests) had increased considerably over the 25-year time period. However, it should be noted that this was prior to the withdrawal of neonicotinoids.
Bees are subject to some of the most complex and stringent guidance in terms of measurement of toxicity and risk assessment of any model group (see EFSA, 2022), though the practical adoption and application of such protocols remain in dispute. Furthermore, the most recent EFSA guidelines remain under review and have not yet been formally adopted by EU member states. The UK continues to base its risk assessment process for pollinators on the older EPPO (2002) framework which does not include some of the more recent and controversial measurements and models that have been proposed for the group. In general, the question of the appropriate treatment of toxicity data for bees during risk assessments remains one of the most contentious topics in wider discussions around PPPs, and remains an area of ongoing controversy and policy development.
Here, field, semi-field and higher tier studies are defined as experimental setups conducted under field or field-like conditions following lower tier toxicological studies (section 2.2), which explicitly compare different PPP application regimes in terms of their impacts on local populations (typically in terms of the abundance and diversity of wild species). Field studies are the most direct line of scientific evidence showing causative links between changes in PPP application patterns and changes in local populations. If implemented well, field or near field studies are the most appropriate tools for understanding how PPP pressures interact with other landscape variables under realistic conditions. As such, they are a key component of Higher Tier studies in the risk assessment process, including investigation of the exposure to, and effects of, PPPs on different non-target organisms.
The history of field trials exploring the impact of PPPs on bees is one of controversy and debate over the significance of findings, particularly in relation to the impact of neonicotinoids (Eisenstein, 2015; Pisa et al., 2015; Sanchez-Bayo, 2014; Sgolastra et al., 2020). Early work included that of Henry et al. (2012), Whitehorn et al. (2012) and Feltham et al. (2014); all of which were substantially criticised for not directly resolving the issue of variability in dosing (Carreck & Ratnieks, 2014; Henry et al., 2015). Later trials, which reported very little impact on bees foraging on treated crops (Cutler et al., 2014; Pilling et al., 2013), were strongly criticised for conflicts of interest (as they were conducted or funded by manufacturers) and inadequate test field sizes (Wood & Goulson, 2017). Whilst the scientific consensus is now in favour of neonicotinoids having a substantial negative effect on bees via various mechanisms (Sgolastra et al., 2020), the more general issue of how to use field trials to provide insights on PPP effects remains open. For instance, Breda et al. (2022) stress the need for a systems approach to the many different interactions and pressures that may apply simultaneously to bee health; a view stated increasingly by guidance documents (e.g. EFSA, 2021). Novel insecticides (e.g. flupyradifurone, sulfoxaflor) are increasingly entering the market following the withdrawal of the traditional neonicotinoids (Siviter & Muth, 2020); hence the question of how to design and interpret field studies for bees remains highly pertinent in ongoing policy developments.
Here, residue studies are defined as records of PPPs being recovered in wild organisms, in either targeted or ongoing monitoring programmes. A major source of UK monitoring data is the Wildlife Incident Investigation Scheme (WIIS), which is specifically charged with investigating suspicious deaths that may be linked to PPP poisoning. Residue studies are direct evidence of PPP exposure under natural conditions and, as such, provide an essential link between laboratory studies and the field. Residue detection, as part of ongoing monitoring, can also provide early warning of emerging threats, allowing for targeted policy development. However, it should be noted that extrapolation from residue studies is notoriously difficult (Köhler & Triebskorn, 2013; Rainford et al., 2023).
Investigation of bee exposure to PPPs in the environment has utilised two types of data – suspicious deaths, and indirect biomonitoring of relevant matrices such as pollen (Chauzat et al., 2006), honey (Woodcock et al., 2018) and beeswax (Wisniewski, 2016). Various studies have reviewed historical bee incidents in which PPP poisoning events were suspected in cause of death; discussed in detail by Rainford et al. (2023). For instance, Greg-Smith et al. (1994) reviewed the results of investigations in which dead bee samples were collected in England, Wales and Scotland in response to suspected poisoning events (1981–1991). An annual average of 50 incidents were confirmed as due to PPP poisoning, involving 30 pesticide active ingredients. In England and Wales, principal hazards were caused by the misuse of two insecticides – triazophos on oilseed rape, and dimethoate on a variety of arable crops. In Scotland, incidents were mostly associated with the use of fenitrothion on raspberries and gamma-HCH on oilseed rape (both insecticides). Authors stressed the importance of post-registration monitoring schemes as part of the PPP authorisation process, complementing pre-registration safety testing for bees (e.g. acute and chronic toxicological studies, field trials).
Fletcher & Barnett (2003) reviewed the number of reported bee incidents between 1988 and 2001 in the UK. Over this period, the number of incidents reported to the ‘Scheme’ (part of WIIS that investigates possible PPP poisoning in bees specifically) declined from over 100 to approx. 30 per year. The percentage of those found to involve PPP poisoning, however, remained at about the same level (25-30%). Overall, 38 different agricultural compounds were identified in bee poisoning cases and, in line with Greg-Smith et al. (1994), insecticides were the most likely compounds to cause deaths (organophosphates, pyrethroid, carbamate and organochlorine compounds). Authors identified several pathways through which the poisoning occurred, including approved use poisoning, misuse, abuse or unspecified (i.e. given the large areas over which bees forage, it was not possible to link the poisoning to a specific action). Similarly, Barnett et al. (2007) reviewed the WIIS data collected between 1994 and 2003. Over this period, suspected poisoning incidents declined (56 to 23 incidents per year), as well as the number of those attributed to PPP poisoning (25 to five incidents per year). Of the 124 incidents confirmed, the PPPs most frequently linked to bee poisoning were all insecticides – bendiocarb, dimethoate and pirimiphos-methyl.
In terms of indirect biomonitoring, Rondeau & Raine (2022) reviewed published literature from 76 studies which contained quantitative data on residue detections in various honeybee matrices, and a further 47 which provided qualitative information on exposure for a range of bee taxa. Authors reported that 90 different fungicide active ingredients and metabolites were detected in honey, beebread, pollen, beeswax and bees, with the greatest number detected in pollen (n = 76), followed by honeybees (n = 54), beeswax (n = 48), beebread (n = 44) and honey (n = 34).
In 2015, the EU implemented a moratorium on the use of three neonicotinoid seed dressings for mass-flowering crops in response to concerns around their potential impacts on bee heath. Woodcock et al. (2018) assessed the effectiveness of this policy in reducing the exposure risk to honeybees by collecting 130 samples of honey from beekeepers across the UK before (2014; n = 21) and after (2015; n = 109) implementation of the moratorium. Neonicotinoids were present in approx. half of the honey samples taken before the moratorium, and present in over a fifth of honey samples taken after, with clothianidin the most frequently detected. Most post-moratorium neonicotinoid residues were from honey harvested early in the year, coinciding with oilseed rape flowering, whilst neonicotinoid concentrations were correlated with the area of oilseed rape surrounding the hive location. Authors, therefore, concluded that mass flowering crops may contain neonicotinoid residues where they have been grown on soils contaminated by previously seed treated crops, including winter seed treatments applied to cereals which were exempt from EU restrictions.
Here, correlative studies are defined as a class of observational studies which attempt to correlate change in the population of one or more species with some metric of PPP usage (typically total amount applied or expected treated area). In some cases, correlative studies have been restricted to a single chemical group or class, and they may or may not have an explicit associated spatial structure. Correlative studies have direct links to the population trends used in national biodiversity indicators, and, in theory, are the fundamental link between all prior forms of assessment (sections 2.1-2.4) and the key outcomes of policy relevance (Johnson, 2019; Köhler & Triebskorn, 2013).
Woodcock et al. (2016) is an extremely influential study in the debate around neonicotinoids and their potential impact on bees, and largely avoids the issues of confounding variables related to wider agricultural intensification. This work uses a large-scale citizen science dataset generated, collected and verified by the ‘Bees, Ants and Wasps Recording Society’ to create a multi-species dynamic Bayesian occupancy model across 5 x 5 km grid squares in the UK over 18 years for 62 wild bee species. It has provided a substantial weight of evidence that exposure to neonicotinoid seed treatments have impacted upon the population persistence of wild bee communities foraging on oilseed rape, as well as influencing the development of methods and approaches to correlative studies more generally (Mancini et al., 2019). Critically, wild bee species that are known to forage on oilseed rape were three times as negatively affected by exposure to neonicotinoids than non-foragers, whilst no trend was identified with conventional spray applications of insecticides; both key lines of evidence for a causal role of neonicotinoid seed treatments in species population decline.
The complexity of PPP impacts in the environment, coupled with the incomplete nature of the associated datasets, makes forming a unified and comprehensive view of their impacts upon UK indicator bee species very challenging (Köhler & Triebskorn, 2013). This is further exacerbated by the challenges presented across the different lines of evidence (sections 2.1-2.5), each with methodological benefits and drawbacks (discussed by Rainford et al., 2023). Nevertheless, various studies have reported on the effects of PPPs on bees using a wide range of approaches, with correlative studies, such as Woodcock et al. (2016) for instance, highlighting the role of neonicotinoid seed treatments in the population decline of wild bee communities foraging on oilseed rape.
The Environment Act 2021 operates as the UK’s framework for environmental protection. It outlines a range of environmental targets for England, including halting the decline in biodiversity (e.g. of insects) by 2030, and subsequently improving upon the 2030 metric (by 10%) by 2042. Agri-environment schemes are key levers by which landowners and managers can be incentivised to manage their land in an environmentally beneficial way to improve biodiversity. Initiatives such as Environmental Land Management (ELM) schemes include aims around the restoration and creation of habitats and improving the abundance of a wide range of species, as well as the reduction of pressures from agricultural inputs (e.g. PPPs) and other related sources. The impacts of such agri-environment schemes on a range of biodiversity indicator species have been reviewed in the literature, including their effects on insect pollinator populations (e.g. bees, moths and butterflies). For instance, recent work by Redhead et al. (2022) showed evidence of significant positive trends in a range of butterfly species (e.g. Gatekeeper and Green-veined White) associated with the uptake of agri-environment scheme measures over a ten-year period at the Hillesden Estate, as well as accompanying declines in the pest species Pieris brassicae and P. rapae. In terms of bees specifically, Crowther & Gilbert (2020) showed that both abundance and species diversity were significantly higher on farms participating in agri-environment schemes, with only small or non-significant differences between entry-level stewardship and higher-level stewardship compliant farms. Actions with positive outcomes included the creation of non-crop field margins, hedgerow restoration, late-cut meadows and the sowing of nectar-rich flower mixes. Authors concluded that entry-level stewardship schemes (most widely used) have the ability to significantly increase the abundance and diversity of bee species with relatively low input from farmers, landowners and managers.
A current Defra project (‘Biodiversity Targets’), led by Fera in collaboration with a consortium of research institutions, is evaluating which policies / actions and what levels of uptake are required to reach the UK’s biodiversity targets. In this project, different modelling approaches will be evaluated (e.g. modelling habitat occupancy) with the aim of creating, i) a simplified policy orientated model which allows rapid evaluation of the impacts of policy driven actions on the reversal of biodiversity decline and its associated costs, and ii) a more detailed research-based model which can ultimately feed into, or replace, the policy-based model. The project will also assess data availability across the priority topics and will instigate the collection of additional monitoring data as required.
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