Environmental Audit Committee - Pollinators and PesticidesWritten evidence submitted by Dr James Cresswell, University of Exeter

1. Executive Summary

1.1 There is insufficient evidence to establish with high certainty that the residues of neonicotinoid pesticides in nectar and pollen threaten the sustainability of bee populations and the pollination services that they provide to crops and wild plants. But there is sufficient evidence to raise concern about bumble bees.

1.2 No experiment has demonstrated that neonicotinoids threaten the viability of honey bee colonies when delivered at realistic dietary levels. Experiments that have demonstrated impacts on colonies used unrealistically high dosages. The lack of evidence for impact is consistent with the observation that the global stock of honey bees has increased by 12% in the last decade.

1.3 Two experiments suggest that neonicotinoids threaten the viability of bumble bee colonies when delivered at realistic levels and I have medium certainty that these findings apply to agricultural landscapes in the UK. Other widely cited experiments are flawed because they used unrealistically high dosages. While there have been observable declines in certain bumble bee species coincident with the increasing use of neonicotinoids, pathogens and habitat degradation are also plausible culprits.

1.4 In the UK, oilseed rape is the principal vehicle for delivery of neonicotinoids to bees. Bumble bees can rapidly recover from neonicotinoid exposure after the crop’s bloom subsides and also some/many colonies will escape the crop’s peak bloom. If concern over bumble bees is justified, these details offer avenues to mitigation through smart land management.

1.5 My recommendation is to fund further research to establish with high certainty whether bumble bees are affected by the dosages that originate from UK agriculture. If concern about bumble bees is justified, the government should fund investigations of smart mitigation strategies based on an understanding of the interplay of exposure, sensitivity, resilience and recovery.

2. Introduction to the Submitter’s Area of Expertise

2.1 I am an academic at the University of Exeter (Biosciences) and I lead an ecotoxicology laboratory that investigates the impacts of neonicotinoid pesticides on bees. I am a member of the European Food Safety Authority (EFSA) Working Group on Bee Risk Assessment. My research is funded in part by Syngenta (£137,000).

3. Factual Information to Support Conclusions

3.1 Below, the following words indicate judgmental estimates of certainty: very certain (98% or greater probability); high certainty (85–98% probability), medium certainty (65–85% probability), low certainty (52–65% probability), and very uncertain (50–52% probability).

3.2 My report examines only effects on bees from neonicotinoids in nectar and pollen. I do not consider effects from guttation fluid (leaf exudates). I consider only honey bees and bumble bees.

3.3 A population is unsustainable when the death rate exceeds the birth rate. Intrinsically, pesticides harm individual bees but they threaten a population only when they cause death rates to exceed birth rates by increasing death rates, decreasing birth rates, or both. I assess experimental evidence for effects on these demographic rates.

3.4 Evaluation of evidence from experiments on honey bees

Table 1. Summary of outcomes of experiments investigating the impact of neonicotinoids on honey bee colonies. Under increased death rates and decreased birth rates: √ = clear effect; 0 = no detectable effect. Under dose: √ = realistic dose; X = unrealistic dose.

Study	↑ death rate	↓ birth rate	Realistic dose
Henry et al. 2012	√	0	X
Lu et al. 2011	√	0	X
Cutler & Scott Dupree 2007	0	0	√
CRD reports: SXR/Am 004/005 (1999)	0	0	√

3.5 No study has demonstrated that neonicotinoids have the capacity to threaten the viability of a honey bee colony when delivered at realistic dietary levels (high certainty). Henry et al. (2012) delivered the aggregate daily dose in a single meal (like smoking 20 cigarettes at once), which would likely overwhelm the honey bee’s detoxification system (high certainty). Lu et al. (2011) delivered neonicotinoids in feeder syrup at an unrealistically high concentration (very certain).

3.6 The failure of some field experiments to detect an effect (eg Cutler & Scott-Dupree 2007) may originate in low statistical power (Cresswell 2011). We need trials that are more incisive and the new EFSA guidelines for risk assessments will remedy this.

3.7 The body of evidence that demonstrates that neonicotinoids impair learning in laboratory tests (proboscis extension response, PER) that I reviewed in my meta-analysis (Cresswell 2011) is not applicable to field conditions (low certainty). In the laboratory, the bees are restrained in a metal jacket and their metabolic rate probably drops, which impairs their detoxification system and increases their susceptibility to neonicotinoids (low certainty).

3.8 Evaluation of evidence from experiments on bumble bees

Table 2. Summary of outcomes of experiments investigating the impact of neonicotinoids on bumble bee colonies. Birth rate refers to capacity to produce individuals of either worker or sexual caste (queens and males). Under increased death rates and decreased death rates: √ = clear effect; 0 = no detectable effect. Under dose: √ = realistic dose; X = unrealistic dose; ? = uncertainty about the realism of the dose.

Study	↑ death rate	↓ birth rate	Realistic dose
Whitehorn et al. 2012	0	√	√?
Gill et al. 2012	0	√	X
Laycock et al. 2012	0	√	√

3.9 A laboratory study (Laycock et al. 2012) demonstrated that neonicotinoids can threaten the viability of a bumble bee colony when delivered at a realistic dietary level (very high certainty). But the dosages used in other experiments are questionable. Gill et al. (2012) used feeder syrup with a dosage (10 ppb) above realistic levels (high certainty). Whitehorn et al. (2012) used 6 ppb in pollen and 0.7 ppb in feeder syrup exclusive feeding for 14 days and their findings may apply to agricultural landscapes in the UK (medium certainty). However, Whitehorn et al. based their dosage on the peak level recorded in spring-sown oilseed rape that flowered in Minnesota, USA, in June (Scott-Dupree et al. 2001), which is higher that due to winter-sown oilseed rape in the UK (low certainty) flowering in April-May (c. 1 ppb in nectar and pollen; Cresswell, unpublished).

3.10 Epidemiological evidence of involvement in population declines

3.11 Honey bees are not in decline (Fig 1; very certain). According to the United Nation’s FAO database, the global stock of hives has increased by 12.4% during the 21^st century and the stock has decreased by only 0.5% in Europe (excluding Eastern Bloc). The global trade in honey is an important driver of change in stock sizes (high certainty). In most countries, national stocks of hives are largely unchanged in the 21^st century (Fig. 2). But increases are evident principally in countries that are net exporters of honey and declines are evident in wealthy countries that are net importers of honey (Fig. 2). Epidemiological evidence does not implicate neonicotinoids as a cause of regional honey bee declines (medium certainty; Cresswell et al. 2012).

Fig. 1. Change in the global stock of honey bee hives in the years 2000–2010. Figures based on FAOSTAT data for 117 countries

Fig. 2. Change in the national stocks of honey bee hives in the years 2000–2010 in 85 countries in relation to the net trade balance of each country for honey (value of honey exports minus value of honey imports). Net exporters of honey have a positive trade balance. Figures based on FAOSTAT data

3.12 There have been observable declines in certain bumble bee species coincident with the increasing use of neonicotinoids (Cameron et al. 2011) but neonicotinoids have not been implicated with any certainty and pathogens and habitat degradation are also plausible culprits.

3.13 Demographic resilience

3.14 Honey bee colonies will not collapse because foraging bees are intoxicated by neonicotinoid residues in nectar (high certainty). Although some foragers could be lost (Henry et al. 2012), a honey bee colony can produce about 1,000 new bees per day and thereby replace bees lost through pesticide-induced navigation failure (Cresswell & Thompson 2012).

3.15 Nobody has yet demonstrated that neonicotinoid exposure of bumble bees causes loss of foragers. Bumble bees are less able than honey bees to replace these losses (high certainty).

3.16 Physiological resilience through detoxification and recovery

Assertions that the effects of neonicotinoids on bees are irreversible (eg Tennekes & Sanchez-Bayo 2011) are false (very certain). In the case of imidacloprid, adult honey bees rapidly detoxify the neonicotinoid (very certain; Suchail et al. 2004; Cresswell et al. unpublished). Bumble bees are less able to clear ingested imidacloprid (very certain; Cresswell et al. unpublished) but the residues are rapidly cleared once the diet is clean and toxic effects are rapidly reversible within a few days (very certain; Laycock, Smith & Cresswell, unpublished).

3.17 Mitigation options

If it is established that neonicotinoids threaten bumble bee populations, a multifaceted mitigation strategy could hypothetically involve: moderation of the pesticide’s application rate; landscape-scale management of crop sowing time to synchronize flowering across fields and minimize the duration of exposure; and enhancement of pesticide-free alternative forage.

3.18 Recommendations for action by the Government

3.19 My recommendation is to fund further research to establish with certainty whether bumble bees are affected by the dosages that occur in UK agriculture.

3.20 If concern about bumble bees is justified, the government should fund investigations of smart mitigation strategies based on an understanding of the interplay of exposure, sensitivity, resilience and recovery.

3.21 Literature cited

Cameron, S A, Lozier, J D, Strange, J P, Koch, J B, Cordes, N, Solter, L F & Griswold, T L (2011). Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences of the United States of America, 108, 662–667.

Cresswell, J E (2011). A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology, 20, 149–157.

Cresswell, J E, Desneux, N & vanEngelsdorp, D (2012). Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Management Science, 68, 819–827.

Cresswell, J E, & Thompson, H M. 2012. Comment on “A common pesticide decreases foraging success and survival in honey bees”. Science 337:1453

Cutler, G C & Scott-Dupree, C D. 2007. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. Journal of Economic Entomology,100:765–72.

Gill, R J, Ramos-Rodriguez, O & Raine, N E (2012). Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature, doi:10.1038/nature11,585.

Henry, M, Béguin, M, Requier, F, Rollin, O, Odoux, J F, Aupinel, P, Aptel, J, Tchamitchian, S & Decourtye A (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336, 348–350.

Laycock, I, Lenthall, K M, Barratt, A T & Cresswell, J E (2012). Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology, 7, 1937–1945.

Lu, C, Warchol, K M, & Callahan, R A. 2012. In situ replication of honey bee colony collapse disorder. Bulletin of Insectology, 65, in press.

Scott-Dupree, C, Spivak, M, Bruns, G, Blenkinsop, C & Nelson, S. 2001. The impact of GAUCHO@ and TI-435 seed treated canola on honey bees, Apis mellifera L. http://www.epa.gov/pesticides/chem_search/cleared_reviews/csr_PC-044,309_19-Mar-03_45,422,435.pdf

Suchail, S, De Sousa, G, Rahmani, R & Belzunces, L P (2004). In vivo distribution and metabolisation of ¹⁴C-imidacloprid in different compartments of Apis mellifera L. Pest Management Science, 60, 1056–1062.

Tennekes, H A & Sanchez-Bayo, F (2011). Time-dependent toxicity of neonicotinoids and other toxicants: implications for a new approach to risk assessment. Journal of Environmental & Analytical Toxicology, S:4.

Whitehorn, P R, O’Connor, S, Wackers, F L & Goulson, D (2012). Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science, 336, 351–352.

8 November 2012