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As a service to bees and other pollinators, the Pollinator Partnership provides a synopsis and abstract from recent published research papers on our website, and it is updated periodically. Your suggestions are welcome; please send them to

Updated May 25, 2012

Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria.
By James E. Cresswell, Nicolas Desneux, and Dennis vanEngelsdorp in Pest Management Science, 68(6):819–827, June 2012.

Abstract: Honey bees are important pollinators of both crops and wild plants. Pesticide regimes that threaten their sustainability therefore should be assessed. As an example, we examine the evidence that the agricutral use of the neonicotinoid pesticides is a cause of the recently observed declines in honey bees. We aim to define exacting demographic conditions for a detrimental factor to precipitate a population decline and we employ Hill’s epidemiological ‘causality criteria’ as a structured process for making an expert judgement about the proposition that trace dietary neonicotinoids in nectar and pollen cause population declines in honey bees.

Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment.
By Tjeerd Blacquière, Guy Smagghe, Cornelis A. M. Gestel, and Veerle Mommaerts in Ecotoxicology, 21(4):973–992, May 2012.

Abstract:  Neonicotinoid insecticides are successfully applied to control pests in a variety of agricultural crops; however, they may not only affect pest insects but also non-target organisms such as pollinators. This review summarizes, for the first time, 15 years of research on the hazards of neonicotinoids to bees including honey bees, bumble bees and solitary bees. The focus of the paper is on three different key aspects determining the risks of neonicotinoid field concentrations for bee populations: (1) the environmental neonicotinoid residue.

A common pesticide decreases foraging success and survival in honey bees.
By Mickaël Henry, Maxime Béguin, Fabrice Requier, Orianne Rollin, Jean-François Odoux, Pierrick Aupinel, Jean Aptel, Sylvie Tchamitchian, and Axel Decourtye in Science, 336(6079):348–350, April 2012.

Abstract: Nonlethal exposure of honey bees to thiamethoxam (neonicotinoid systemic pesticide) causes high mortality due to homing failure at levels that could put a colony at risk of collapse. Simulated exposure events on free-ranging foragers labeled with a radio-frequency identification tag suggest that homing is impaired by thiamethoxam intoxication. These experiments offer new insights into the consequences of common neonicotinoid pesticides used worldwide.

Do pathogen spillover, pesticide use, or habitat loss explain recent north american bumblebee declines? 
By Nora D. Szabo, Sheila R. Colla, David L. Wagner, Lawrence F. Gall, and Jeremy T. Kerr in Conservation Letters, April 2012.

Abstract: Several North American bumblebee species have recently undergone dramatic declines. The use of managed, pathogen-carrying bumblebees for pollination of greenhouse crops began shortly before these declines, and wild bumblebees near greenhouses now have high pathogen loads. This has led to speculation that pathogen spillover from commercial bumblebees caused declines of these species. We test this hypothesis using a large dataset of bumblebee occurrence records and agricultural census data. We find support for the pathogen spillover hypothesis for two species but no evidence that pathogen spillover caused the near disappearance of the previously widespread Bombus affinis. Furthermore, we show that pesticide use and habitat loss are unlikely to be major causes of decline for any of the Bombus species examined. Collectively, our analyses underscore that there remains an urgent need to identify causes of pollinator population losses.

Neonicotinoid pesticide reduces bumble bee colony growth and queen production.
By Penelope R. Whitehorn, Stephanie O’Connor, Felix L. Wackers, and Dave Goulson in Science, 336(6079):351–352, April 2012.

Abstract: Growing evidence for declines in bee populations has caused great concern because of the valuable ecosystem services they provide. Neonicotinoid insecticides have been implicated in these declines because they occur at trace levels in the nectar and pollen of crop plants. We exposed colonies of the bumble beeBombus terrestris in the laboratory to field-realistic levels of the neonicotinoid imidacloprid, then allowed them to develop naturally under field conditions. Treated colonies had a significantly reduced growth rate and suffered an 85% reduction in production of new queens compared with control colonies. Given the scale of use of neonicotinoids, we suggest that they may be having a considerable negative impact on wild bumble bee populations across the developed world.

Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee.
By Julie Aufauvre, David G. Biron, Cyril Vidau, Régis Fontbonne, Mathieu Roudel, Marie Diogon, Bernard Viguès, Luc P. Belzunces, Frédéric Delbac, and Nicolas Blot in Scientific Reports, 2, March 2012.

Abstract: In ecosystems, a variety of biological, chemical and physical stressors may act in combination to induce illness in populations of living organisms. While recent surveys reported that parasite-insecticide interactions can synergistically and negatively affect honeybee survival, the importance of sequence in exposure to stressors has hardly received any attention. In this work, Western honeybees (Apis mellifera) were sequentially or simultaneously infected by the microsporidian parasite Nosema ceranae and chronically exposed to a sublethal dose of the insecticide fipronil, respectively chosen as biological and chemical stressors. Interestingly, every combination tested led to a synergistic effect on honeybee survival, with the most significant impacts when stressors were applied at the emergence of honeybees. Our study presents significant outcomes on beekeeping management but also points out the potential risks incurred by any living organism frequently exposed to both pathogens and insecticides in their habitat.

Multiple routes of pesticide exposure for honey bees living near agricultural fields.
By Christian H. Krupke, Greg J. Hunt, Brian D. Eitzer, Gladys Andino, and Krispn Given in PLoS ONE, 7(1):e29268+, January 2012.

Abstract: Populations of honey bees and other pollinators have declined worldwide in recent years. A variety of stressors have been implicated as potential causes, including agricultural pesticides. Neonicotinoid insecticides, which are widely used and highly toxic to honey bees, have been found in previous analyses of honey bee pollen and comb material. However, the routes of exposure have remained largely undefined. We used LC/MS-MS to analyze samples of honey bees, pollen stored in the hive and several potential exposure routes associated with plantings of neonicotinoid treated maize. Our results demonstrate that bees are exposed to these compounds and several other agricultural pesticides in several ways throughout the foraging period. During spring, extremely high levels of clothianidin and thiamethoxam were found in planter exhaust material produced during the planting of treated maize seed. We also found neonicotinoids in the soil of each field we sampled, including unplanted fields. Plants visited by foraging bees (dandelions) growing near these fields were found to contain neonicotinoids as well. This indicates deposition of neonicotinoids on the flowers, uptake by the root system, or both. Dead bees collected near hive entrances during the spring sampling period were found to contain clothianidin as well, although whether exposure was oral (consuming pollen) or by contact (soil/planter dust) is unclear. We also detected the insecticide clothianidin in pollen collected by bees and stored in the hive. When maize plants in our field reached anthesis, maize pollen from treated seed was found to contain clothianidin and other pesticides; and honey bees in our study readily collected maize pollen. These findings clarify some of the mechanisms by which honey bees may be exposed to agricultural pesticides throughout the growing season. These results have implications for a wide range of large-scale annual cropping systems that utilize neonicotinoid seed treatments.

Pesticide exposure in honey bees results in increased levels of the gut pathogen nosema.
By Jeffery S. Pettis, Dennis vanEngelsdorp, Josephine Johnson, and Galen Dively in Naturwissenschaften, 99(2):153–158, January 2012.

Abstract: Global pollinator declines have been attributed to habitat destruction, pesticide use, and climate change or some combination of these factors, and managed honey bees, Apis mellifera, are part of worldwide pollinator declines. Here we exposed honey bee colonies during three brood generations to sub-lethal doses of a widely used pesticide, imidacloprid, and then subsequently challenged newly emerged bees with the gut parasite, Nosema spp. The pesticide dosages used were below levels demonstrated to cause effects on longevity or foraging in adult honey bees. Nosema infections increased significantly in the bees from pesticide-treated hives when compared to bees from control hives demonstrating an indirect effect of pesticides on pathogen growth in honey bees. We clearly demonstrate an increase in pathogen growth within individual bees reared in colonies exposed to one of the most widely used pesticides worldwide, imidacloprid, at below levels considered harmful to bees. The finding that individual bees with undetectable levels of the target pesticide, after being reared in a sub-lethal pesticide environment within the colony, had higher Nosema is significant. Interactions between pesticides and pathogens could be a major contributor to increased mortality of honey bee colonies, including colony collapse disorder, and other pollinator declines worldwide.

Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: A novel way of intoxication for bees.
By V. Girolami, L. Mazzon, A. Squartini, N. Mori, M. Marzaro, A. Di Bernardo, M. Greatti, C. Giorio, and A. Tapparo in Journal of Economic Entomology, 102(5):1808–1815, September 2009.

Abstract: The death of honey bees, Apis mellifera L., and the consequent colony collapse disorder causes major losses in agriculture and plant pollination worldwide. The phenomenon showed increasing rates in the past years, although its causes are still awaiting a clear answer. Although neonicotinoid systemic insecticides used for seed coating of agricultural crops were suspected as possible reason, studies so far have not shown the existence of unquestionable sources capable of delivering directly intoxicating doses in the fields. Guttation is a natural plant phenomenon causing the excretion of xylem fluid at leaf margins. Here, we show that leaf guttation drops of all the corn plants germinated from neonicotinoid-coated seeds contained amounts of insecticide constantly higher than 10 mg/1, with maxima up to 100 mg/1 for thiamethoxam and clothianidin, and up to 200 mg/1 for imidacloprid. The concentration of neonicotinoids in guttation drops can be near those of active ingredients commonly applied in field sprays for pest control, or even higher. When bees consume guttation drops, collected from plants grown from neonicotinoid-coated seeds, they encounter death within few minutes.

Quantification of imidacloprid uptake in maize crops.
By J. M. Bonmatin, P. A. Marchand, R. Charvet, I. Moineau, E. R. Bengsch, and M. E. Colin in J. Agric. Food Chem., 53(13):5336–5341, June 2005.

Abstract: The systemic imidacloprid is one of the most used insecticides in the world for field and horticultural crops. This neurotoxicant is often used as seed-dressing, especially for maize, sunflower, and rape. Using a LC/MS/MS technique (LOQ = 1 μg/kg and LOD = 0.1 μg/kg), the presence of imidacloprid has been measured in maize from field samples at the time of pollen shed, from less than 0.1 μg/kg up to 33.6 μg/kg. Numerous random samples were collected throughout France from 2000 to 2003. The average levels of imidacloprid measured are 4.1 μg/kg in stems and leaves, 6.6 μg/kg in male flowers (panicles), and 2.1 μg/kg in pollen. These values are similar to those found previously in sunflower and rape. These results permit evaluation of the risk to honeybees by using the PEC/PNEC ratios (probable exposition concentrations/predicted no effect concentration). PEC/PNEC risk ratios were determined and ranged between 500 and 600 for honeybees foraging on maize treated with imidacloprid by seed dressing. Such a high risk factor can be related to one of the main causes of honeybee colony losses.

Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees.
By Agnes Rortais, Gerard Arnold, Marie-Pierre Halm, and Frederique Touffet-Briens in Apidologie, 36(1):71–83, January 2005.

Abstract: The hazard posed to honeybees by systemic insecticides is determined by toxicity tests that are designed to study the effects of insecticides applied on the aerial parts of plants, but are not adapted to systemic substances used as soil or seed treatments. Based on the available data found in the literature, this paper proposes modes of honeybees exposure to systemic insecticides by estimating their pollen and nectar consumption. Estimates are given for larvae and for the categories of adults which consume the highest amounts of - pollen, the nurse bees, and - nectar, the wax-producing bees, the brood attending bees, the winter bees, and the foraging bees. As a case study, we illustrate these estimates with the example of imidacloprid because its concentrations in sunflower nectar and in sunflower and maize pollens of seed-dressed plants have been precisely determined, and because its levels of lethal, sublethal, acute, and chronic toxicities have been extensively investigated. doi:10.1051/apido:2004071


Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera.
By Severine Suchail, David Guez, and Luc P. Belzunces in Environmental Toxicology and Chemistry, 20(11):2482–2486, November 2001.

Abstract: Imidacloprid is a systemic nitroguanidine insecticide that belongs to theneonicotinoid family. As an agonist of the acetylcholine receptor, it attacks the insect nervous system and is extremely effective against various sucking and mining pests. Oral acute and chronic toxicity of imidacloprid and its main metabolites (5-hydroxyimidacloprid, 4,5-dihydroxyimidacloprid, desnitroimidacloprid, 6-chloronicotinic acid, olefin, and urea derivative) were investigated in Apis mellifera. Acute intoxication by imidacloprid or its metabolites resulted in the rapid appearance of neurotoxicity symptoms, such as hyperresponsiveness, hyperactivity, and trembling and led to hyporesponsiveness and hypoactivity. For acute toxicity tests, bees were treated with doses of toxic compounds.

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