Seed coating with a neonicotinoid insecticide negatively affects wild bees

Journal name:
Nature
Volume:
521,
Pages:
77–80
Date published:
DOI:
doi:10.1038/nature14420
Received
Accepted
Published online

Understanding the effects of neonicotinoid insecticides on bees is vital because of reported declines in bee diversity and distribution1, 2, 3 and the crucial role bees have as pollinators in ecosystems and agriculture4. Neonicotinoids are suspected to pose an unacceptable risk to bees, partly because of their systemic uptake in plants5, and the European Union has therefore introduced a moratorium on three neonicotinoids as seed coatings in flowering crops that attract bees6. The moratorium has been criticized for being based on weak evidence7, particularly because effects have mostly been measured on bees that have been artificially fed neonicotinoids8, 9, 10, 11. Thus, the key question is how neonicotinoids influence bees, and wild bees in particular, in real-world agricultural landscapes11, 12, 13. Here we show that a commonly used insecticide seed coating in a flowering crop can have serious consequences for wild bees. In a study with replicated and matched landscapes, we found that seed coating with Elado, an insecticide containing a combination of the neonicotinoid clothianidin and the non-systemic pyrethroid β-cyfluthrin, applied to oilseed rape seeds, reduced wild bee density, solitary bee nesting, and bumblebee colony growth and reproduction under field conditions. Hence, such insecticidal use can pose a substantial risk to wild bees in agricultural landscapes, and the contribution of pesticides to the global decline of wild bees1, 2, 3 may have been underestimated. The lack of a significant response in honeybee colonies suggests that reported pesticide effects on honeybees cannot always be extrapolated to wild bees.

At a glance

Figures

  1. Paired design with replicated landscapes.
    Figure 1: Paired design with replicated landscapes.

    Location of the study area in southern Sweden and the eight pairs of landscapes (P01–P08) centred on oilseed rape fields sown with insecticide-coated (open circles) or untreated (control fields, filled circles) seeds. Pairing was based on land use within a 2-km radius surrounding the oilseed rape fields and geographical proximity between fields.

  2. Bee density and reproduction.
    Figure 2: Bee density and reproduction.

    a–d, Mean (± 95% confidence limits) number of wild bees (solitary bees and bumblebees) per 467 m2 oilseed rape field and adjacent border (generalized linear mixed model (GLMM)) (a), median number of tubes per field with O. bicornis brood cells (Wilcoxon test) (b), mean (± 95% confidence limits) number of B. terrestris queen (filled circles, GLMM) and worker/male (open circles, linear mixed model (LMM)) cocoons per colony (c), and mean (± 95% confidence limits) number of adult A. mellifera per colony (colony strength) after placement at the fields (LMM) (d) in relation to treatment (control or insecticide seed coating) in the oilseed rape fields. n = 8 fields per treatment. Means and confidence limits are based on back-transformed, model-estimated least square means. In panel b, horizontal line in the box, open diamond symbols, boxes and whiskers indicate median, mean, 25th–75th percentiles and minimum–maximum, respectively. NS, not significant (P > 0.05); *P < 0.05, **P < 0.01.

  3. Bumblebee colony development.
    Figure 3: Bumblebee colony development.

    Mean (± 95% confidence limits) bumblebee colony weight change (g) per field and survey day since day of placement at the fields (dashed horizontal reference line indicates initial colony weight) in relation to treatment (control (filled circles) or insecticide seed coating (open circles)). n = 8 fields per treatment. Dots are means of the six colonies at each field and weighing occasion. Two colonies at different fields (one control field and one treated field) were not weighed at one occasion, resulting in five colonies at those fields and weighing occasions. See Extended Data Table 6 for results from the colony growth model (linear mixed model).

  4. O. bicornis emergence and B. terrestris colonies.
    Extended Data Fig. 1: O. bicornis emergence and B. terrestris colonies.

    a, Mean (± 95% confidence limits) proportion emergence of O. bicornis from cocoons in relation to treatment (control or insecticide seed coating), with higher emergence for males than females (generalized linear mixed model, binomial error distribution, logit link; F1, 14 = 14.97, P = 0.0017), no difference between treatments (F1, 7 = 0.71, P = 0.43) and no interaction (F1, 14 = 0.01, P = 0.94). n = 8 fields per treatment, with 12 female and 15 male cocoons at each field. Photos (with permission; Morgan Boch): left, emerged O. bicornis cocoon; right, O. bicornis female at a trap nests filled with cardboard nest tubes. b, Mean (± 95% confidence limits) weight of B. terrestris colonies at placement at the fields in relation to treatment (linear mixed model, F1, 7 = 0.99, P = 0.35). n = 8 fields per treatment, with six colonies at each field. Photos (M.R.): left, B. terrestris worker foraging in the oilseed rape; right, house containing three B. terrestris colonies. Means and confidence limits in panels a and b are based on back-transformed, model-estimated least square means. c, B. terrestris silk cocoon width distribution of all cocoons in four colonies (two from two different control fields and two from two different fields with insecticide seed treatment) initially examined to separate between queen and worker/male cocoons. Dashed vertical line indicates selected cut-off width at 12 mm (the lowest value between the two peaks), with queens larger (or equal) and workers/males smaller. Photo (M.R.): B. terrestris colony under examination.

  5. Power curves for honeybee colony strength.
    Extended Data Fig. 2: Power curves for honeybee colony strength.

    a, b, Relationship between power and effect size estimated for the honeybee model (Extended Data Table 6), with effect size expressed as the difference in honeybee colony strength (number of bees per colony) (a) and the percentage change in colony strength (b) between colonies at control fields and at fields with insecticide seed coating after placement at the oilseed rape fields. Grey reference lines indicate a power of 0.8 and the corresponding effect size.

Tables

  1. 2013 field size and 2011 and 2013 land use in the landscapes surrounding (radius  =  2 km) the oilseed rape
    Extended Data Table 1: 2013 field size and 2011 and 2013 land use in the landscapes surrounding (radius = 2 km) the oilseed rape
  2. Phenology (date, BBCH and flower cover) in the oilseed rape fields and delivery, placement and survey* of bees
    Extended Data Table 2: Phenology (date, BBCH33 and flower cover) in the oilseed rape fields and delivery, placement and survey* of bees
  3. Use of plant protection products in the oilseed rape fields during the 2013 growing season
    Extended Data Table 3: Use of plant protection products in the oilseed rape fields during the 2013 growing season
  4. Wild bee density in oilseed rape fields and borders in relation to insecticide seed treatment and covariates
    Extended Data Table 4: Wild bee density in oilseed rape fields and borders in relation to insecticide seed treatment and covariates
  5. Statistical tests and mean values for bee-related variables in relation to the insecticide seed treatment in the oilseed rape fields
    Extended Data Table 5: Statistical tests and mean values for bee-related variables in relation to the insecticide seed treatment in the oilseed rape fields
  6. Bumblebee colony growth (net weight gain) and honeybee colony strength (adult bees per hive) in relation to insecticide seed treatment
    Extended Data Table 6: Bumblebee colony growth (net weight gain) and honeybee colony strength (adult bees per hive) in relation to insecticide seed treatment
  7. Number of individuals of wild bee species or groups at control (n  =  8) and insecticide-treated (n  =  8) oilseed rape fields
    Extended Data Table 7: Number of individuals of wild bee species or groups at control (n = 8) and insecticide-treated (n = 8) oilseed rape fields
  8. Residues of neonicotinoids (n) and a pyrethroid (p) in bee-collected pollen and nectar from control fields and fields sown with insecticide treated seeds
    Extended Data Table 8: Residues of neonicotinoids (n) and a pyrethroid (p) in bee-collected pollen and nectar from control fields and fields sown with insecticide treated seeds

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Author information

Affiliations

  1. Lund University, Department of Biology, 223 62 Lund, Sweden

    • Maj Rundlöf,
    • Georg K. S. Andersson,
    • Veronica Hederström,
    • Johanna Yourstone &
    • Henrik G. Smith
  2. Lund University, Centre for Environmental and Climate Research, 223 62 Lund, Sweden

    • Georg K. S. Andersson,
    • Lina Herbertsson,
    • Björn K. Klatt &
    • Henrik G. Smith
  3. Swedish University of Agricultural Sciences, Department of Ecology, 750 07 Uppsala, Sweden

    • Riccardo Bommarco &
    • Ingemar Fries
  4. Swedish University of Agricultural Sciences, Department of Aquatic Sciences and Assessment, 750 07 Uppsala, Sweden

    • Ove Jonsson
  5. Swedish University of Agricultural Sciences, Centre for Chemical Pesticides, 750 07 Uppsala, Sweden

    • Ove Jonsson
  6. Swedish Board of Agriculture, 551 82 Jönköping, Sweden

    • Thorsten R. Pedersen

Contributions

R.B., I.F., T.R.P. and H.G.S. conceived the project. M.R. designed the study, coordinated the work, analysed the data, and prepared the manuscript. G.K.S.A., V.H., L.H., B.K.K. and J.Y. collected the data. O.J. quantified the pesticide residues. All authors contributed to the interpretation of results and writing of the manuscript.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

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Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: O. bicornis emergence and B. terrestris colonies. (517 KB)

    a, Mean (± 95% confidence limits) proportion emergence of O. bicornis from cocoons in relation to treatment (control or insecticide seed coating), with higher emergence for males than females (generalized linear mixed model, binomial error distribution, logit link; F1, 14 = 14.97, P = 0.0017), no difference between treatments (F1, 7 = 0.71, P = 0.43) and no interaction (F1, 14 = 0.01, P = 0.94). n = 8 fields per treatment, with 12 female and 15 male cocoons at each field. Photos (with permission; Morgan Boch): left, emerged O. bicornis cocoon; right, O. bicornis female at a trap nests filled with cardboard nest tubes. b, Mean (± 95% confidence limits) weight of B. terrestris colonies at placement at the fields in relation to treatment (linear mixed model, F1, 7 = 0.99, P = 0.35). n = 8 fields per treatment, with six colonies at each field. Photos (M.R.): left, B. terrestris worker foraging in the oilseed rape; right, house containing three B. terrestris colonies. Means and confidence limits in panels a and b are based on back-transformed, model-estimated least square means. c, B. terrestris silk cocoon width distribution of all cocoons in four colonies (two from two different control fields and two from two different fields with insecticide seed treatment) initially examined to separate between queen and worker/male cocoons. Dashed vertical line indicates selected cut-off width at 12 mm (the lowest value between the two peaks), with queens larger (or equal) and workers/males smaller. Photo (M.R.): B. terrestris colony under examination.

  2. Extended Data Figure 2: Power curves for honeybee colony strength. (56 KB)

    a, b, Relationship between power and effect size estimated for the honeybee model (Extended Data Table 6), with effect size expressed as the difference in honeybee colony strength (number of bees per colony) (a) and the percentage change in colony strength (b) between colonies at control fields and at fields with insecticide seed coating after placement at the oilseed rape fields. Grey reference lines indicate a power of 0.8 and the corresponding effect size.

Extended Data Tables

  1. Extended Data Table 1: 2013 field size and 2011 and 2013 land use in the landscapes surrounding (radius = 2 km) the oilseed rape (190 KB)
  2. Extended Data Table 2: Phenology (date, BBCH33 and flower cover) in the oilseed rape fields and delivery, placement and survey* of bees (264 KB)
  3. Extended Data Table 3: Use of plant protection products in the oilseed rape fields during the 2013 growing season (167 KB)
  4. Extended Data Table 4: Wild bee density in oilseed rape fields and borders in relation to insecticide seed treatment and covariates (199 KB)
  5. Extended Data Table 5: Statistical tests and mean values for bee-related variables in relation to the insecticide seed treatment in the oilseed rape fields (389 KB)
  6. Extended Data Table 6: Bumblebee colony growth (net weight gain) and honeybee colony strength (adult bees per hive) in relation to insecticide seed treatment (201 KB)
  7. Extended Data Table 7: Number of individuals of wild bee species or groups at control (n = 8) and insecticide-treated (n = 8) oilseed rape fields (156 KB)
  8. Extended Data Table 8: Residues of neonicotinoids (n) and a pyrethroid (p) in bee-collected pollen and nectar from control fields and fields sown with insecticide treated seeds (114 KB)

Additional data