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. 2013 Oct 23;8(10):e77193.
doi: 10.1371/journal.pone.0077193. eCollection 2013.

A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam

Edward Pilling  1 , Peter Campbell, Mike Coulson, Natalie Ruddle, Ingo Tornier
Affiliations

A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam

Edward Pilling et al. PLoS One. .

Abstract

Neonicotinoid residues in nectar and pollen from crop plants have been implicated as one of the potential factors causing the declines of honey bee populations. Median residues of thiamethoxam in pollen collected from honey bees after foraging on flowering seed treated maize were found to be between 1 and 7 µg/kg, median residues of the metabolite CGA322704 (clothianidin) in the pollen were between 1 and 4 µg/kg. In oilseed rape, median residues of thiamethoxam found in pollen collected from bees were between <1 and 3.5 µg/kg and in nectar from foraging bees were between 0.65 and 2.4 µg/kg. Median residues of CGA322704 in pollen and nectar in the oilseed rape trials were all below the limit of quantification (1 µg/kg). Residues in the hive were even lower in both the maize and oilseed rape trials, being at or below the level of detection of 1 µg/kg for bee bread in the hive and at or below the level of detection of 0.5 µg/kg for hive nectar, honey and royal jelly samples. The long-term risk to honey bee colonies in the field was also investigated, including the sensitive overwintering stage, from four years consecutive single treatment crop exposures to flowering maize and oilseed rape grown from thiamethoxam treated seeds at rates recommended for insect control. Throughout the study, mortality, foraging behavior, colony strength, colony weight, brood development and food storage levels were similar between treatment and control colonies. Detailed examination of brood development throughout the year demonstrated that colonies exposed to the treated crop were able to successfully overwinter and had a similar health status to the control colonies in the following spring. We conclude that these data demonstrate there is a low risk to honey bees from systemic residues in nectar and pollen following the use of thiamethoxam as a seed treatment on oilseed rape and maize.

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Conflict of interest statement

Competing Interests: Peter Campbell, Mike Coulson and Natalie Ruddle are employed by Syngenta Ltd., which developed and markets the neonicotinoid insecticide thiamethoxam. Ed Pilling is employed by the consultancy JSC International and was paid by Syngenta Ltd. to write the manuscript. Ed Pilling was also once an employee of Syngenta (joined JSC International in May 2011), and was directly involved in the study design and conduct. Ingo Tornier is employed by Eurofins Agroscience Services and was paid by Syngenta Ltd. to conduct the field trials. Syngenta Ltd. has numerous patents covering the active ingredient thiamethoxam and formulated products containing this active ingredient. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

Figures

Figure 1
Figure 1. An overview of the 4 year multiple exposure field trial design in maize and oilseed rape.
Figure 2
Figure 2. Thiamethoxam and CGA322704 residue levels in plant tissue, bee pollen and bee bread stored in cells from the first year of seed treated maize exposure in tunnels.
The plot shows the median (•), upper and lower quartile and range values.
Figure 3
Figure 3. Thiamethoxam and CGA322704 residue levels in plant tissue, bee pollen and bee bread stored in cells from a two year seed treated maize rotation exposure in tunnels.
The plot shows the median (•), upper and lower quartile and range values.
Figure 4
Figure 4. Thiamethoxam and CGA322704 residue levels in plant tissue, bee pollen, bee nectar, bee bread stored in cells and hive nectar from seed treated oilseed rape exposure in tunnels.
The plot shows the median (•), upper and lower quartile and range values.
Figure 5
Figure 5. Thiamethoxam and CGA322704 residue levels in plant tissue, bee pollen, bee nectar, bee bread stored in cells and hive nectar from a seed treated oilseed rape following seed treated barley rotation exposure in tunnels.
The plot shows the median (•), upper and lower quartile and range values.
Figure 6
Figure 6. Mean number of dead bees per hive per day collected in the dead bee traps and on linen sheets in front of the hives in treated (dashed line) and control (solid line) oilseed rape fields in the Alsace region of France.
Figure 7
Figure 7. Mean number of forager bees per m2 flowering rape in treated (dashed line) and control (solid line) fields during the time of exposure in the Alsace region of France.
Figure 8
Figure 8. Strength of honey bee colonies exposed to treated (dashed line) and control (solid line) oilseed rape fields in the Alsace region of France during the four years of observations including the last overwintering.
Figure 9
Figure 9. Mean area on combs (%) of brood (eggs, larvae and pupae) and food (nectar and pollen) of 6 colonies exposed to treated oilseed rape in the Alsace region of France over 4 years.
Figure 10
Figure 10. Mean area on combs (%) of brood (eggs, larvae and pupae) and food (nectar and pollen) of 6 colonies exposed to control oilseed rape in the Alsace region of France over 4 years.
Figure 11
Figure 11. Mean hive weight (kg) during time of assessments of colonies in treated (dashed line) and control (solid line) oilseed rape fields in the Alsace region of France.
See this image and copyright information in PMC

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