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

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

[1]  C. Giorio,et al.  Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds. , 2012, Environmental science & technology.

[2]  J. Dushoff,et al.  Native bees provide insurance against ongoing honey bee losses. , 2007, Ecology Letters.

[3]  A. González-Porto,et al.  Overview of Pesticide Residues in Stored Pollen and Their Potential Effect on Bee Colony (Apis mellifera) Losses in Spain , 2010, Journal of economic entomology.

[4]  L. Velasco,et al.  Estimation of seed weight, oil content and fatty acid composition in intact single seeds of rapeseed ( Brassica napus} L.) by near-infrared reflectance spectroscopy , 1999, Euphytica.

[5]  S. Williamson,et al.  Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees , 2013, Journal of Experimental Biology.

[6]  L. Belzunces,et al.  Metabolism of imidacloprid in Apis mellifera. , 2004, Pest management science.

[7]  S. Cunningham,et al.  Spatial and temporal variation in pollinator effectiveness: do unmanaged insects provide consistent pollination services to mass flowering crops? , 2012 .

[8]  S. Droege,et al.  Detecting Insect Pollinator Declines on Regional and Global Scales , 2013, Conservation biology : the journal of the Society for Conservation Biology.

[9]  Sarah S. Greenleaf,et al.  Wild bee species increase tomato production and respond differently to surrounding land use in Northern California , 2006 .

[10]  L. Wiest,et al.  Multi-residue analysis of 80 environmental contaminants in honeys, honeybees and pollens by one extraction procedure followed by liquid and gas chromatography coupled with mass spectrometric detection. , 2011, Journal of chromatography. A.

[11]  Richard G. Jones,et al.  Declines of managed honey bees and beekeepers in Europe , 2010 .

[12]  F. Ratnieks,et al.  Long-range foraging by the honey-bee, Apis mellifera L. , 2000 .

[13]  T. Seeley The Wisdom of the Hive , 1995 .

[14]  A. Klein,et al.  Importance of pollinators in changing landscapes for world crops , 2007, Proceedings of the Royal Society B: Biological Sciences.

[15]  C. Giorio,et al.  Rapid analysis of neonicotinoid insecticides in guttation drops of corn seedlings obtained from coated seeds. , 2011, Journal of environmental monitoring : JEM.

[16]  E. Yang,et al.  Abnormal Foraging Behavior Induced by Sublethal Dosage of Imidacloprid in the Honey Bee (Hymenoptera: Apidae) , 2008, Journal of economic entomology.

[17]  M. Winston The Biology of the Honey Bee , 1987 .

[18]  G. Budge,et al.  Global Honey Bee Viral Landscape Altered by a Parasitic Mite , 2012, Science.

[19]  Sarah S. Greenleaf,et al.  Wild bees enhance honey bees’ pollination of hybrid sunflower , 2006, Proceedings of the National Academy of Sciences.

[20]  Richard J. Gill,et al.  Combined pesticide exposure severely affects individual- and colony-level traits in bees , 2012, Nature.

[21]  D. vanEngelsdorp,et al.  Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill's epidemiological criteria. , 2012, Pest management science.

[22]  M. Vighi,et al.  Field Trial for Evaluating the Effects on Honeybees of Corn Sown Using Cruiser® and Celest xl® Treated Seeds , 2010, Bulletin of environmental contamination and toxicology.

[23]  James T. Wilkes,et al.  A national survey of managed honey bee 2011–12 winter colony losses in the United States: results from the Bee Informed Partnership , 2013 .

[24]  M. Spiteller,et al.  Neonicotinoid insecticides translocated in guttated droplets of seed-treated maize and wheat: a threat to honeybees? , 2011, Apidologie.

[25]  A. Klein,et al.  Biodiversity buffers pollination from changes in environmental conditions , 2013, Global change biology.

[26]  J. Losey,et al.  The Economic Value of Ecological Services Provided by Insects , 2006 .

[27]  David B. Roy,et al.  Declines in forage availability for bumblebees at a national scale , 2006 .

[28]  P. Neumann,et al.  Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory , 2014 .

[29]  S. Potts,et al.  The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination , 2011 .

[30]  N. Carreck Are honey bees (Apis mellifera L.) native to the British Isles , 2008 .

[31]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[32]  James T. Wilkes,et al.  A national survey of managed honey bee 2010–11 winter colony losses in the USA: results from the Bee Informed Partnership , 2012 .

[33]  S. Zeggane,et al.  An assessment of honeybee colony matrices, Apis mellifera (Hymenoptera: Apidae) to monitor pesticide presence in continental France , 2011, Environmental toxicology and chemistry.

[34]  K Ann McKibbon,et al.  Current status and future prospects. , 2008, Health information and libraries journal.

[35]  W. Jordan,et al.  Molecular and spatial analyses reveal links between colony-specific foraging distance and landscape-level resource availability in two bumblebee species , 2012 .

[36]  J. Ellis,et al.  Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides , 2011 .

[37]  M. Aizen,et al.  Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. , 2007, Ecology letters.

[38]  Mickaël Henry,et al.  Crop-Emptying Rate and the Design of Pesticide Risk Assessment Schemes in the Honey Bee and Wild Bees (Hymenoptera: Apidae) , 2014, Journal of economic entomology.

[39]  T. Blacquière,et al.  Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment , 2012, Ecotoxicology.

[40]  Michelle T. Franklin,et al.  Effects of clothianidin on Bombus impatiens (Hymenoptera: Apidae) colony health and foraging ability. , 2004, Journal of economic entomology.

[41]  K. Walters,et al.  Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies , 2013, Apidologie.

[42]  T. Ricketts,et al.  Ecosystem services and dis-services to agriculture , 2007 .

[43]  H. Thompson,et al.  Comment on “A Common Pesticide Decreases Foraging Success and Survival in Honey Bees” , 2012, Science.

[44]  Marcelo A. Aizen,et al.  The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination , 2009, Current Biology.

[45]  J. Bonmatin,et al.  Quantification of imidacloprid uptake in maize crops. , 2005, Journal of agricultural and food chemistry.

[46]  M. Dacher,et al.  Effects of Sublethal Doses of Acetamiprid and Thiamethoxam on the Behavior of the Honeybee (Apis mellifera) , 2008, Archives of environmental contamination and toxicology.

[47]  L. Mazzon,et al.  Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication , 2012 .

[48]  S. Dorn,et al.  Long foraging distances impose high costs on offspring production in solitary bees. , 2010, The Journal of animal ecology.

[49]  Claire Kremen,et al.  Modelling pollination services across agricultural landscapes. , 2009, Annals of botany.

[50]  G. Guyatt,et al.  GRADE: an emerging consensus on rating quality of evidence and strength of recommendations , 2008, BMJ : British Medical Journal.

[51]  K. Walters DATA, DATA EVERYWHERE BUT WE DON'T KNOW WHAT TO THINK? NEONICOTINOID INSECTICIDES AND POLLINATORS , 2013 .

[52]  L. Gsell,et al.  The discovery of thiamethoxam: a second-generation neonicotinoid. , 2001, Pest management science.

[53]  A. Stork,et al.  Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. , 2001, Pest management science.

[54]  G. C. Cutler,et al.  Exposure to Clothianidin Seed-Treated Canola Has No Long-Term Impact on Honey Bees , 2007, Journal of economic entomology.

[55]  D. Goulson,et al.  Decline and conservation of bumble bees. , 2008, Annual review of entomology.

[56]  J. Odoux,et al.  Effects of sublethal doses. Impairment of olfactory learning performances in the honey bee after long term ingestion of imidacloprid , 2001 .

[57]  D. Macdonald,et al.  A restatement of the natural science evidence base relevant to the control of bovine tuberculosis in Great Britain† , 2013, Proceedings of the Royal Society B: Biological Sciences.

[58]  A. Vanbergen The Insect Pollinators Initiative , 2012 .

[59]  M. Blythe,et al.  Transient Exposure to Low Levels of Insecticide Affects Metabolic Networks of Honeybee Larvae , 2013, PloS one.

[60]  J. Ollerton,et al.  How many flowering plants are pollinated by animals , 2011 .

[61]  E. Yang,et al.  Impaired Olfactory Associative Behavior of Honeybee Workers Due to Contamination of Imidacloprid in the Larval Stage , 2012, PloS one.

[62]  R. Nauen,et al.  Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. , 2005, Archives of insect biochemistry and physiology.

[63]  Carl Wood,et al.  Current Status and Future Prospects , 1984 .

[64]  H. Tennekes The significance of the Druckrey-Küpfmüller equation for risk assessment--the toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time. , 2010, Toxicology.

[65]  Martin Wikelski,et al.  Space Use of Bumblebees (Bombus spp.) Revealed by Radio-Tracking , 2011, PloS one.

[66]  L. Mazzon,et al.  Aerial powdering of bees inside mobile cages and the extent of neonicotinoid cloud surrounding corn drillers , 2013 .

[67]  N. Smirnoff,et al.  Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). , 2012, Zoology.

[68]  A. Clark,et al.  Thrice Out of Africa: Ancient and Recent Expansions of the Honey Bee, Apis mellifera , 2006, Science.

[69]  K. F. Conrad,et al.  Long-term population trends in widespread British moths , 2004, Journal Of Insect Conservation.

[70]  S. Williamson,et al.  Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera , 2012, Invertebrate Neuroscience.

[71]  Alana L. Burley,et al.  A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. , 2013, Ecology letters.

[72]  Mickaël Henry,et al.  Response to Comment on “A Common Pesticide Decreases Foraging Success and Survival in Honey Bees” , 2012, Science.

[73]  Axel Decourtye,et al.  The sublethal effects of pesticides on beneficial arthropods. , 2007, Annual review of entomology.

[74]  V. Gary,et al.  Subchronic exposure of honeybees to sublethal doses of pesticides: Effects on behavior , 2009, Environmental toxicology and chemistry.

[75]  A. Squartini,et al.  Translocation of Neonicotinoid Insecticides from Coated Seeds to Seedling Guttation Drops: A Novel Way of Intoxication for Bees , 2009, Journal of economic entomology.

[76]  Richard J. Gill,et al.  Chronic sublethal stress causes bee colony failure , 2013, Ecology letters.

[77]  A. Klein,et al.  Wild pollination services to California almond rely on semi‐natural habitat , 2012 .

[78]  P. Campbell Declining European Bee Health: Banning the Neonicotinoids is Not the Answer , 2013 .

[79]  J. Cresswell,et al.  Repression and Recuperation of Brood Production in Bombus terrestris Bumble Bees Exposed to a Pulse of the Neonicotinoid Pesticide Imidacloprid , 2013, PloS one.

[80]  Adam J. Vanbergen,et al.  Frontiers inEcology and the Environment Threats to an ecosystem service : pressures on pollinators , 2013 .

[81]  Kristine M. Smith,et al.  Pathogens, Pests, and Economics: Drivers of Honey Bee Colony Declines and Losses , 2013, EcoHealth.

[82]  David J. Hawthorne,et al.  Killing Them with Kindness? In-Hive Medications May Inhibit Xenobiotic Efflux Transporters and Endanger Honey Bees , 2011, PloS one.

[83]  D. Nuyttens,et al.  Pesticide-laden dust emission and drift from treated seeds during seed drilling: a review. , 2013, Pest management science.

[84]  Pernille Thorbek,et al.  REVIEW: Towards a systems approach for understanding honeybee decline: a stocktaking and synthesis of existing models , 2013, The Journal of applied ecology.

[85]  P. Rosenkranz,et al.  Biology and control of Varroa destructor. , 2010, Journal of invertebrate pathology.

[86]  Mickaël Henry,et al.  A Common Pesticide Decreases Foraging Success and Survival in Honey Bees , 2012, Science.

[87]  Jeffrey D. Lozier,et al.  Patterns of widespread decline in North American bumble bees , 2011, Proceedings of the National Academy of Sciences.

[88]  J. Taséi,et al.  New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). , 2006, Environmental science & technology.

[89]  H. Thompson Interaction between pesticides and other factors in effects on bees , 2012 .

[90]  A. Decourtye,et al.  Landscape enhancement of floral resources for honey bees in agro-ecosystems , 2010, Apidologie.

[91]  P. Marchand,et al.  Insecticides systémiques : de nouveaux risques pour les insectes pollinisateurs , 2004 .

[92]  J. Biesmeijer,et al.  Combined effects of global change pressures on animal-mediated pollination. , 2013, Trends in ecology & evolution.

[93]  L. Belzunces,et al.  Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera , 2001, Environmental toxicology and chemistry.

[94]  Claire Kremen,et al.  Contribution of Pollinator-Mediated Crops to Nutrients in the Human Food Supply , 2011, PloS one.

[95]  Kirsty J. Park,et al.  Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency , 2014, Ecotoxicology.

[96]  H. Selim,et al.  Transport of Imidacloprid in Soils: Miscible Displacement Experiments , 2010 .

[97]  J. Osborne,et al.  An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species , 2005, Molecular ecology.

[98]  S. Martin,et al.  Honey bee colony collapse and changes in viral prevalence associated with Varroa destructor , 2010 .

[99]  A. P. Schaffers,et al.  Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands , 2006, Science.

[100]  D. Goulson REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides , 2013 .

[101]  Gladys K. Andino,et al.  Multiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields , 2012, PloS one.

[102]  E. Genersch,et al.  The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies , 2010, Apidologie.

[103]  Jacqueline de Chazal,et al.  Climate change 2007 : impacts, adaptation and vulnerability : Working Group II contribution to the Fourth Assessment Report of the IPCC Intergovernmental Panel on Climate Change , 2014 .

[104]  M. Giurfa,et al.  Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees. , 2012, Learning & memory.

[105]  Andrew P. Martin,et al.  Bumblebee flight distances in relation to the forage landscape. , 2008, The Journal of animal ecology.

[106]  J. Wu,et al.  Sub-Lethal Effects of Pesticide Residues in Brood Comb on Worker Honey Bee (Apis mellifera) Development and Longevity , 2011, PloS one.

[107]  R. Bommarco,et al.  Drastic historic shifts in bumble-bee community composition in Sweden , 2012, Proceedings of the Royal Society B: Biological Sciences.

[108]  R. Nauen,et al.  Thiamethoxam : A neonicotinoid precursor converted to clothianidin in insects and plants , 2003 .

[109]  R. Isaacs,et al.  Stability of pollination services decreases with isolation from natural areas despite honey bee visits. , 2011, Ecology letters.

[110]  A. Shenkute,et al.  Natural and within-farmland biodiversity enhances crop productivity. , 2011, Ecology letters.

[111]  R. Nauen,et al.  Overview of the status and global strategy for neonicotinoids. , 2011, Journal of agricultural and food chemistry.

[112]  J. Tautz,et al.  RFID Tracking of Sublethal Effects of Two Neonicotinoid Insecticides on the Foraging Behavior of Apis mellifera , 2012, PloS one.

[113]  Eric J. Hoffmann,et al.  Imidacloprid in Melon Guttation Fluid: A Potential Mode of Exposure for Pest and Beneficial Organisms , 2012, Journal of economic entomology.

[114]  A. Klein,et al.  Synergistic effects of non-Apis bees and honey bees for pollination services , 2013, Proceedings of the Royal Society B: Biological Sciences.

[115]  J. Casida,et al.  Neonicotinoid insecticide toxicology: mechanisms of selective action. , 2005, Annual review of pharmacology and toxicology.

[116]  P. Campbell,et al.  A Four-Year Field Program Investigating Long-Term Effects of Repeated Exposure of Honey Bee Colonies to Flowering Crops Treated with Thiamethoxam , 2013, PloS one.

[117]  D. Abrol Honeybees and Rapeseed: A Pollinator–Plant Interaction , 2007 .

[118]  A. Barron,et al.  A Quantitative Model of Honey Bee Colony Population Dynamics , 2011, PloS one.

[119]  D. vanEngelsdorp,et al.  Honey bee colony losses in Belgium during the 2008–9 winter , 2010 .

[120]  A. Steinemann,et al.  Chemistry and biology of thiamethoxam: a second generation neonicotinoid. , 2001, Pest management science.

[121]  D. Goulson,et al.  Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production , 2012, Science.

[122]  James Regetz,et al.  Landscape effects on crop pollination services: are there general patterns? , 2008, Ecology letters.

[123]  P. Marik,et al.  A Descriptive Study , 2015 .

[124]  C. Kremen,et al.  Resource diversity and landscape-level homogeneity drive native bee foraging , 2012, Proceedings of the National Academy of Sciences.

[125]  Jay D. Evans,et al.  Colony Collapse Disorder: A Descriptive Study , 2009, PloS one.

[126]  M. Aizen,et al.  Long-Term Global Trends in Crop Yield and Production Reveal No Current Pollination Shortage but Increasing Pollinator Dependency , 2008, Current Biology.

[127]  P. Raven,et al.  Child, Adolescent and Family Refugee Mental Health: A Global Perspective , 1996 .

[128]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[129]  K. Crailsheim,et al.  Nutrition and health in honey bees , 2010, Apidologie.

[130]  M. Winston,et al.  Effects of Novel Pesticides on Bumble Bee (Hymenoptera: Apidae) Colony Health and Foraging Ability , 2003 .

[131]  J. Faucon,et al.  A Survey of Pesticide Residues in Pollen Loads Collected by Honey Bees in France , 2006 .

[132]  L. Harder,et al.  Global growth and stability of agricultural yield decrease with pollinator dependence , 2011, Proceedings of the National Academy of Sciences.

[133]  J. Devillers,et al.  Comparative Sublethal Toxicity of Nine Pesticides on Olfactory Learning Performances of the Honeybee Apis mellifera , 2005, Archives of environmental contamination and toxicology.

[134]  P. Stork,et al.  Uptake, translocation and metabolism of imidacloprid in plants , 2003 .

[135]  J. Tautz,et al.  Automatic life-long monitoring of individual insect behaviour now possible. , 2003, Zoology.

[136]  Geraldine A. Wright,et al.  Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees , 2013, Nature Communications.

[137]  D. Guez A common pesticide decreases foraging success and survival in honey bees: questioning the ecological relevance , 2013, Frontiers in Physiology.

[138]  J. Brunet,et al.  Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera) , 2010, Environmental microbiology.

[139]  N. Calderone,et al.  Insect Pollinated Crops, Insect Pollinators and US Agriculture: Trend Analysis of Aggregate Data for the Period 1992–2009 , 2012, PloS one.

[140]  Lars Chittka,et al.  Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris , 2008, Behavioral Ecology and Sociobiology.

[141]  I. Steffan‐Dewenter,et al.  Pollination efficiency of wild bees and hoverflies provided to oilseed rape , 2012 .

[142]  D. Potter,et al.  Hazards of Insecticides to the Bumble Bees Bombus impatiens (Hymenoptera: Apidae) Foraging on Flowering White Clover in Turf , 2002, Journal of economic entomology.

[143]  Peter G. Kevan,et al.  The Economic Impacts of Pollinator Declines: An Approach to Assessing the Consequences , 2001 .

[144]  L. Mazzon,et al.  Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. , 2011 .

[145]  S. Cameron,et al.  Decline of bumble bees (Bombus) in the North American Midwest , 2009 .

[146]  Michael J. O. Pocock,et al.  Identifying key knowledge needs for evidence‐based conservation of wild insect pollinators: a collaborative cross‐sectoral exercise , 2013 .

[147]  K. Goh,et al.  Detections of the Neonicotinoid Insecticide Imidacloprid in Surface Waters of Three Agricultural Regions of California, USA, 2010–2011 , 2012, Bulletin of Environmental Contamination and Toxicology.

[148]  R. Nauen,et al.  Response to the publication: Tennekes, H.A. (2010): The significance of the Druckrey–Küpfmüller equation for risk assessment—The toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time , 2011 .

[149]  M. Harrison A Global Perspective , 2015, Bulletin of the history of medicine.

[150]  M. Winston,et al.  Lethal and Sublethal Effects of Imidacloprid on Osmia lignaria and Clothianidin on Megachile rotundata (Hymenoptera: Megachilidae) , 2008, Journal of economic entomology.

[151]  J. Biesmeijer,et al.  Agricultural Policies Exacerbate Honeybee Pollination Service Supply-Demand Mismatches Across Europe , 2014, PloS one.

[152]  P. Sikorski,et al.  Residues of Neonicotinoid Insecticides in Bee Collected Plant Materials from Oilseed Rape Crops and their Effect on Bee Colonies , 2012 .

[153]  J. Free Insect pollination of crops , 1970 .

[154]  J. Cresswell A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees , 2011, Ecotoxicology.

[155]  T. Blacquière Survival rate of honeybee (Apis mellifera) workers after exposure to sublethal concentrations of imidacloprid , 2010 .

[156]  J. Cresswell,et al.  Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. , 2014, Ecotoxicology and environmental safety.

[157]  R. Paxton,et al.  The conservation of bees: a global perspective , 2009, Apidologie.

[158]  B. Eitzer,et al.  Movement of Soil-Applied Imidacloprid and Thiamethoxam into Nectar and Pollen of Squash (Cucurbita pepo) , 2012, PloS one.

[159]  J. Frazier,et al.  Weighing Risk Factors Associated with Bee Colony Collapse Disorder by Classification and Regression Tree Analysis , 2010, Journal of economic entomology.

[160]  Peter Jeschke,et al.  Nicotinic acetylcholine receptor agonists: a milestone for modern crop protection. , 2013, Angewandte Chemie.

[161]  J. Frazier,et al.  Pesticides and Their Involvement in Colony Collapse Disorder , 2013 .

[162]  J. Brunet,et al.  Neural effects of insecticides in the honey bee , 2012, Apidologie.

[163]  L. Bortolotti,et al.  Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees , 2003 .

[164]  N. Smirnoff,et al.  Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). , 2014, Pest management science.

[165]  D. vanEngelsdorp,et al.  A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010 , 2011 .

[166]  J. Boyd,et al.  What are Ecosystem Services? The Need for Standardized Environmental Accounting Units , 2006 .

[167]  H. Baša Česnik,et al.  Residues of Pesticides in Honeybee (Apis mellifera carnica) Bee Bread and in Pollen Loads from Treated Apple Orchards , 2009, Bulletin of environmental contamination and toxicology.

[168]  J. Biesmeijer,et al.  Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success , 2014 .

[169]  M. Aizen,et al.  How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. , 2009, Annals of botany.

[170]  R. Paxton,et al.  Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. , 2015, Environmental microbiology.

[171]  J. Devillers,et al.  Ecotoxicity of neonicotinoid insecticides to bees. , 2010, Advances in experimental medicine and biology.

[172]  Teja Tscharntke,et al.  Functional group diversity of bee pollinators increases crop yield , 2008, Proceedings of the Royal Society B: Biological Sciences.

[173]  J. Casida,et al.  Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. , 2003, Annual review of entomology.

[174]  Udo Heimbach,et al.  Bee poisoning incidents in Germany in spring 2008 caused by abrasion of active substance from treated seeds during sowing of maize. , 2009 .

[175]  Michele R. Dudash,et al.  Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences , 2004 .

[176]  A. Decourtye,et al.  Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. , 2003, Pest management science.

[177]  W. Ohe,et al.  Colony losses - interactions of plant protection products and other factors. , 2010 .

[178]  C. Dormann,et al.  Spatial and Temporal Trends of Global Pollination Benefit , 2012, PloS one.

[179]  A. Kamel,et al.  Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. , 2012, Journal of agricultural and food chemistry.

[180]  J. Frazier,et al.  Comparative Toxicities and Synergism of Apple Orchard Pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski) , 2013, PloS one.

[181]  Achim Gathmann,et al.  Foraging ranges of solitary bees , 2002 .

[182]  G. Arnold,et al.  Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees , 2005 .

[183]  T. Seeley,et al.  FORAGING STRATEGY OF HONEYBEE COLONIES IN A TEMPERATE DECIDUOUS FOREST , 1982 .

[184]  S. Bougeard,et al.  Influence of Pesticide Residues on Honey Bee (Hymenoptera: Apidae) Colony Health in France , 2009, Environmental entomology.

[185]  Don R. Reynolds,et al.  A landscape‐scale study of bumble bee foraging range and constancy, using harmonic radar , 1999 .

[186]  Ingolf Steffan-Dewenter,et al.  Honeybee foraging in differentially structured landscapes , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[187]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[188]  M. Hoyle,et al.  Effect of pollinator abundance on self-fertilization and gene flow: application to GM Canola. , 2007, Ecological applications : a publication of the Ecological Society of America.

[189]  C. Kremen,et al.  Are ecosystem services stabilized by differences among species? A test using crop pollination , 2009, Proceedings of the Royal Society B: Biological Sciences.

[190]  S. Cunningham,et al.  Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop , 2009 .

[191]  J. Stark,et al.  Limitations to Use of Topical Toxicity Data for Predictions of Pesticide Side Effects in the Field , 1995 .

[192]  J. Casida,et al.  Neonicotinoid insecticides: molecular features conferring selectivity for insect versus mammalian nicotinic receptors. , 2000, Journal of agricultural and food chemistry.

[193]  J. P. van der Sluijs,et al.  Expert explanations of honeybee losses in areas of extensive agriculture in France: Gaucho® compared with other supposed causal factors , 2010 .

[194]  Insect pollination enhances seed yield, quality, and market value in oilseed rape , 2012, Oecologia.

[195]  H. Köhler,et al.  Wildlife Ecotoxicology of Pesticides: Can We Track Effects to the Population Level and Beyond? , 2013, Science.

[196]  J. P. Foster,et al.  Discovery of the Nitromethylene Heterocycle Insecticides , 1999 .

[197]  F. Sgolastra,et al.  A meta-analysis comparing the sensitivity of bees to pesticides , 2014, Ecotoxicology.

[198]  A. Dag Bee pollination of crop plants under environmental conditions unique to enclosures , 2008 .

[199]  C. Dormann,et al.  Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination , 2011, Proceedings of the Royal Society B: Biological Sciences.

[200]  J. Frazier,et al.  High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health , 2010, PloS one.

[201]  J. Settele,et al.  Economic valuation of the vulnerability of world agriculture confronted with pollinator decline , 2009 .

[202]  Johan Olausson,et al.  The Millennium Atlas of Butterflies in Britain and Ireland , 2007 .

[203]  H. Thompson,et al.  Extrapolating from Honeybees to Bumblebees in Pesticide Risk Assessment , 1999 .

[204]  T. Matsumoto Short- and long-term effects of neonicotinoid application in rice fields, on the mortality and colony collapse of honeybees (Apis mellifera) , 2013 .

[205]  V. T. Gajbhiye,et al.  Soil Dissipation and Leaching Behavior of a Neonicotinoid Insecticide Thiamethoxam , 2008, Bulletin of environmental contamination and toxicology.

[206]  J. Bonmatin,et al.  A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. , 2003, Analytical chemistry.

[207]  S. Potts,et al.  POLLINATION DEFICITS IN UK APPLE ORCHARDS , 2014 .

[208]  James Devillers,et al.  Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. , 2004, Ecotoxicology and environmental safety.

[209]  J. Cresswell,et al.  Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris) , 2012, Ecotoxicology.

[210]  Takashi Matsumoto,et al.  Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides , 2013 .

[211]  Kaja Peterson,et al.  An application of DPSIR framework to identify issues of pollinator loss , 2009 .

[212]  J. Devillers,et al.  Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.) , 2004 .

[213]  J. Ambrose,et al.  Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellife , 2004 .

[214]  J. Biesmeijer,et al.  Avoiding a bad apple: Insect pollination enhances fruit quality and economic value☆ , 2014, Agriculture, ecosystems & environment.

[215]  Peter Jeschke,et al.  Neonicotinoids-from zero to hero in insecticide chemistry. , 2008, Pest management science.

[216]  E. De Pauw,et al.  Development and validation of a multi-residue method for pesticide determination in honey using on-column liquid-liquid extraction and liquid chromatography-tandem mass spectrometry. , 2007, Journal of chromatography. A.

[217]  R. Nauen,et al.  Applied aspects of neonicotinoid uses in crop protection. , 2008, Pest management science.

[218]  G. Smagghe,et al.  Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior , 2010, Ecotoxicology.

[219]  J. Taséi,et al.  Hazards of Imidacloprid Seed Coating to Bombus terrestris (Hymenoptera: Apidae) When Applied to Sunflower , 2001, Journal of economic entomology.

[220]  D. Potter,et al.  Assessing Insecticide Hazard to Bumble Bees Foraging on Flowering Weeds in Treated Lawns , 2013, PloS one.

[221]  D. vanEngelsdorp,et al.  Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema , 2012, Naturwissenschaften.

[222]  Elinor M. Lichtenberg,et al.  Crop Pollination Exposes Honey Bees to Pesticides Which Alters Their Susceptibility to the Gut Pathogen Nosema ceranae , 2013, PloS one.

[223]  Francis L. W. Ratnieks,et al.  Clarity on Honey Bee Collapse? , 2010, Science.

[224]  G. Daily,et al.  Optimal design of agricultural landscapes for pollination services , 2008 .

[225]  C. Scott-dupree,et al.  Impact of Currently Used or Potentially Useful Insecticides for Canola Agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae) , 2009, Journal of economic entomology.

[226]  Andrew B. Barron,et al.  Modelling Food and Population Dynamics in Honey Bee Colonies , 2013, PloS one.

[227]  E. De Pauw,et al.  Does Imidacloprid Seed-Treated Maize Have an Impact on Honey Bee Mortality? , 2009, Journal of economic entomology.

[228]  R. Nauen,et al.  Pyrethroid resistance and thiacloprid baseline susceptibility of European populations of Meligethes aeneus (Coleoptera: Nitidulidae) collected in winter oilseed rape. , 2011, Pest management science.

[229]  M. Boily,et al.  Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments , 2013, Environmental Science and Pollution Research.

[230]  F. Nazzi,et al.  Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees , 2013, Proceedings of the National Academy of Sciences.

[231]  J. Taséi,et al.  Sub‐lethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae), during a laboratory feeding test , 2000 .

[232]  Henk A. Tennekes,et al.  Time-Dependent Toxicity of Neonicotinoids and Other Toxicants:Implications for a New Approach to Risk Assessment , 2011 .

[233]  T. Keitt Habitat conversion, extinction thresholds, and pollination services in agroecosystems. , 2009, Ecological applications : a publication of the Ecological Society of America.

[234]  S. Buckingham,et al.  Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. , 2001, Trends in pharmacological sciences.

[235]  D. Biron,et al.  Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees Previously Infected by Nosema ceranae , 2011, PloS one.

[236]  Roy A. Sanderson,et al.  Effects of land use at a landscape scale on bumblebee nest density and survival , 2010 .

[237]  C. Menzie,et al.  A Causal Analysis of Observed Declines in Managed Honey Bees (Apis mellifera) , 2013, Human and ecological risk assessment : HERA.

[238]  D. Goulson,et al.  Use of genetic markers to quantify bumblebee foraging range and nest density , 2004 .

[239]  S. Zeggane,et al.  Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. , 2005, Pest management science.

[240]  S. Dorn,et al.  Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances , 2010 .

[241]  Sarah S. Greenleaf,et al.  Bee foraging ranges and their relationship to body size , 2007, Oecologia.

[242]  M. Biocca,et al.  Potential Exposure of Bees, Apis mellifera L., to Particulate Matter and Pesticides Derived from Seed Dressing During Maize Sowing , 2012, Bulletin of Environmental Contamination and Toxicology.

[243]  Helen M Thompson,et al.  Risk assessment for honey bees and pesticides--recent developments and 'new issues'. , 2010, Pest management science.

[244]  A. Klein,et al.  Economic gain, stability of pollination and bee diversity decrease from southern to northern Europe , 2013 .