Insects and Insecticides

Written evidence submitted by Professor Graham Stone, University
of Edinburgh

Summary points:

1. The value of the pollination ecosystem service to UK agriculture and biodiversity is enormous.

2. Pollination services require healthy pollinator populations of suitable species that are both growing (or at least stable), and functioning efficiently.

3. Pesticides, including neonicotinoids, have been designed to target fundamental insect systems. Our default expectation must be that, even at sub-lethal doses, their impacts on beneficial insects will never be good.

4. Impacts on pollinators can be complex and delayed.

5. There is reason to expect that combinations of pesticides could have synergistic effects on insect health.

6. We know neonicotinoids reduce UK bee performance, but we don’t really know why.

7. Impacts of pesticides are very likely to vary among pollinator groups.

Conclusions.

1. We know too little about non-target impacts of neonicotinoids to assume that there is little or no risk to UK pollinators under current application regimes.

2. Given the value of pollination services, there is an urgent need to invest in the research necessary to address the ‘known unknowns’.

3. It would probably be unwise to extrapolate from research on bees to behavioural and population effects on non-bee pollinators.

Each summary point, expanded.

1. The value of the pollination ecosystem service to UK agriculture and biodiversity is enormous, and could not be achieved without insect pollinators (POST 2010; Breeze et al 2012). It is prudent therefore to know about non-target effects before deploying any pesticides. History shows that failure to understand impacts of toxins on non-target species and natural communities only ever has an unhappy ending.

2. Pollination services require healthy pollinator populations of suitable species that are both growing (or at least stable), and functioning efficiently (healthy) (Breeze et al 2012).

3. Pesticides, including neonicotinoids, have been designed to target fundamental insect systems (Nauen and Denholm 2005; Aliouane et al 2009).

Our default expectation for such toxins must be that, even at sub-lethal doses, their impacts on beneficial insects will never be good (Desneux et al 2007). That they do not cause harm should be based on evidence, rather than absence of evidence – and there are a lot of important things we don’t know very much about.

4. Impacts on pollinators can be complex and delayed. Beyond rapid killing of insects, neonicotinoids are known to have complex and longer-term effects on individual and colony performance. In social bees, exposure to neonicotinoids reduces pollen collecting ability and ability to return safely to the nest from foraging trips (Gill et al 2012; Henry et al 2012). Reduced pollen-collecting ability may explain why neonicotinoid-exposed bumblebee colonies are less able to invest resources in queens for the next generation (Whitehorn et al 2012). While argument continues over the magnitude of these effects in fully natural situations, these effects can only ever have negative impacts on the quality of pollination service delivered, and the status of bee (and other pollinator) populations.

5. There is reason to expect that combinations of pesticides could have synergistic effects on insect health because different pesticide groups target different fundamental systems. Neonicotinoids target systems using one type of nerve transmission (cholinergic), while phenylpyrazoles such as Fipronil target another (glutamergic) (Pfluger and Duch 2011). These nervous systems fulfil different roles in the body: for example, cholinergic nerves are involved in collection of information and processing by the insect brain (Pfluger and Duch 2011), while glutamergic nerves are involved in operation of the main flight muscles (which in social bees are also associated with generation of heat for nest incubation, and in solitary bees, large hoverflies and some butterflies are required for essential pre-flight warm-up) (Heinrich 1993). Because foraging and other pollinator behaviours often involve both information processing and flight, we should explore the extent to which different pesticide combinations interfere with them.

Recommendation: impacts of combined pesticide exposure should be studied as a matter of urgency.

6. We know neonicotinoids reduce UK bee performance, but we don’t really know why. Though some of the impacts of neonicotinoid pesticides on insect physiology are known, we still cannot explain the observed effects on honeybee and bumblebee behaviour.

We know which physiological systems are most likely to be targeted by neonicotinoids (see evidence submission from Dr. Chris Connolly, Dundee University; Desneux et al 2007), and we also know about some impacts on individual bee behaviour (e.g. Gill et al 2012). Neonicotinoid exposure is associated with longer foraging trips, lower rates of pollen harvesting, and higher forager mortality through non-return to the nest (Henry et al. 2012). These changes reduce the resources flowing into a bee colony, and result in reduced queen production in bumblebees (Whitehorn et al 2012).

The decline in foraging success could be attributable to collapse of a key metabolic system (such as the flight muscles, whose ability to generate internal heat is essential for flight and warming of the nest) or to neural processing of information (ability to recognise flowers and rewards, ability to communicate information to nest mates, and to navigate home safely) (Desneux et al 2007; Henry et al 2012), or any combination of these and other systems. We urgently need more research on the organ-system and whole animal level impacts of pesticides on bees and other pollinators.

Recommendation: System-level effects of neonicotinoids singly and in combination with other pesticides should be explicitly studied.

7. Impacts of pesticides are very likely to vary among pollinator groups. We should not extrapolate to other groups from known impacts on social bees.

Pollinator groups (e.g. social bees, solitary bees, hoverflies, butterflies) differ in how individual foraging success is linked to reproductive success, and face different routes of pesticide exposure.

(a) Social bees versus solitary bees. To date, almost all work on the effects of neonicotinoids has been carried out on honeybees and bumblebees (see DEFRA research programs at http://randd.defra.gov.uk/). These social species can respond to challenging conditions by altering the proportion of workers doing different jobs, and how much resource they invest in making workers versus making reproductive adults (e.g. Whitehorn et al 2012 and Gill et al 2012 for bumblebees). However, solitary bee females are required to carry out all of these roles, building and stocking each cell with collected provisions before laying their egg (Stone 1994). They cannot make the same resource allocation decisions as social bees, or benefit from warmth/nectar gathered by nestmates, and may be more vulnerable to non-lethal pesticide effects. We also need to know how neonicotinoids impact on the courtship and mating behaviours of male solitary bees, which are far more diverse than those seen in social species, and directly linked to successful reproduction.

Recommendation: neonicotinoid impacts on solitary bees should be explicitly investigated using model systems such as the red mason bee, Osmia bicornis (= O. rufa).

(b) Bees versus other pollinators. Bees differ from other pollinators in that their reproductive output depends directly on how much pollen the adult females can collect. Any factor that reduces a bee’s ability to recognise, harvest or carry pollen back to its nest will influence its reproductive rate. Exposure to pesticides through food is via nectar (adults) and pollen (larvae).

Other pollinators have different links between the food they harvest from flowers and their reproductive rate. For example, adult female hoverflies feed on pollen and/or to mature their eggs (and so are exposed to systemic pesticides in pollen/nectar) (Gilbert 1981), but this is not directly linked to how many offspring they have. The larvae of many hoverflies feed on other insects, and have additional potential routes of pesticide intake (for example, from aphids feeding on a sprayed or seed-dressed plant). Butterflies are different again, and do not need the nectar they feed on to mature their eggs. They are exposed as adults to pesticides in nectar, and as larvae to any pesticides in their food plant.

Recommendation: this simple overview suggests that it would be unwise to extrapolate from research on bees to behavioural and population effects on non-bee pollinators.

Literature cited.

Aliouane Y et al. (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behaviour. Environmental Toxicology and Chemistry 28, 113-122.

Breeze TD, Roberts SPM and Potts SG (2012) The Decline of England’s Bees

Policy Review and Recommendations. Friends of the Earth/ Reading University.

Desneux N et al (2007) The sublethal effects of pesticides on beneficial arthropods. Annual review of Entomology 52, 81-106.

Gilbert FS (1981) Foraging ecology of hoverflies: morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species. Ecological Entomology 6, 245-262.

Gill RJ et al (2012) Combined pesticide exposure severely affects individual- and colony-level traits

Heinrich BE (1993) The Hot-blooded Insects. Springer.

Henry M. et al. (2012) A common pesticide decreases foraging success and survival in honeybees. Science 336, 348–350.

Nauen R and Denholm I (2005) Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Archives of insect Biochemistry and Physiology 58, 200-215.

Parliamentary Office of Science and Technology (2010) Insect Pollination. January 2010 Number 348.

Pfluger HJ and Duch C (2011) Dynamic neural control of insect muscle

metabolism related to motor behavior. Physiology 26, 293-303.

Stone GN (1994). Activity patterns of females of the solitary bee Anthophora plumipes in relation to temperature, nectar supplies and body size. Ecological Entomology 19, 177-189.

Whitehorn PR et al (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352.

20 November 2012

Prepared 23rd November 2012