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Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees

Mickaël Henry, Nicolas Cerrutti, Pierrick Aupinel, Axel Decourtye, Mélanie Gayrard, Jean-François Odoux, Aurélien Pissard, Charlotte Rüger, Vincent Bretagnolle
Published 18 November 2015.DOI: 10.1098/rspb.2015.2110
Mickaël Henry
INRA, UR406 Abeilles et Environnement, 84914 Avignon, FranceUMT Protection des Abeilles dans l'Environnement, Site Agroparc, 84914 Avignon, France
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Nicolas Cerrutti
UMT Protection des Abeilles dans l'Environnement, Site Agroparc, 84914 Avignon, FranceTerres Inovia, Centre de Grignon, Avenue Lucien Brétignières, 78850 Thiverval Grignon, France
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Pierrick Aupinel
INRA, UE1255, UE Entomologie, 17700 Surgères, France
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Axel Decourtye
UMT Protection des Abeilles dans l'Environnement, Site Agroparc, 84914 Avignon, FranceAssociation de Coordination Technique Agricole, Site Agroparc, 84914 Avignon, FranceITSAP–Institut de l'Abeille, Site Agroparc, 84914 Avignon, France
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Mélanie Gayrard
Terres Inovia, Centre de Grignon, Avenue Lucien Brétignières, 78850 Thiverval Grignon, France
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Jean-François Odoux
INRA, UE1255, UE Entomologie, 17700 Surgères, France
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Aurélien Pissard
Association de Coordination Technique Agricole, Site Agroparc, 84914 Avignon, France
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Charlotte Rüger
Terres Inovia, Centre de Grignon, Avenue Lucien Brétignières, 78850 Thiverval Grignon, France
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Vincent Bretagnolle
Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS and Université de La Rochelle, 79360 Beauvoir-sur-Niort, FranceLTER ‘Zone Atelier Plaine and Val de Sèvre’, Centre d'Etudes Biologiques de Chizé, CNRS, 79360 Villiers-en-Bois, France
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  • Data Supplement

    • Papier_Gradient_151015_SupMat.pdf
    • Supplementary data table S1 - Day-by-day excess mortality rate per 15 field exposure units in foragers and just-emerged honeybees, and corresponding Cox PH survival statistics.
    • Supplementary data table S2 - Raw data for mean cumulative disappearance of monitored individuals after cohort introduction in high and low field exposure environments.
    • Supplementary data table S3 - Raw data for differential reproductive investment of colonies into female (worker) and drone (disperser) brood.

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    Figure 1.

    Field exposure experimental design. The maps show the location of the experimental fields with oilseed rape grown from thiamethoxam-treated seeds (23 fields (total 153 ha) in 2013 and 18 fields (135 ha) in 2014). Dots show the positions of beehives fitted with RFID readers, spatially allocated in a way that covers a broad range of field exposure levels. Thiamethoxam field exposure was computed as the sum of all treated surfaces in the territory, with individual field surfaces moderated by an ordinary IDW interpolation. Surfaces of treated fields located farther away than the average honeybee foraging range (1 km) were down-weighted by a 1/d2 multiplicative coefficient, where d is the distance (km) of the field to the colony. The resulting field exposure values ranged from 1 to 63 (mean = 15.7 ± 16.8 (s.d.)). The most exposed colony (exposure value = 82) showed dramatically high mortality rates compared to the other colonies, but concomitantly developed foulbrood syndromes. It was therefore discarded from the analyses to avoid overstating the excess mortality due to field exposure.

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    Figure 2.

    Non-stationary excess mortality due to field exposure during oilseed rape flowering. The honeybee excess mortality level due to field exposure is not stationary, but steadily increases in time. (a) Non-stationary excess mortality due to field exposure in 1638 bees tagged at the foraging stage with RFID microchips. (b) Non-stationary excess mortality due to field exposure in 5209 bees tagged after emergence with RFID microchips. Shaded areas show the 95% confidence envelope of the Cox PH estimate of excess mortality, expressed in per cent of the baseline mortality, and indicating a significant field exposure effect whenever it is above zero. Excess mortality was sequentially reassessed along the temporal axis using a left-censoring procedure, i.e. discarding newly disappeared individuals at each time step. For the sake of comparison, dashed lines show the field exposure effect that would be found on the assumption of stationary excess mortality.

  • Figure 3.
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    Figure 3.

    Mean cumulative disappearance of monitored individuals under high versus low field exposure. Mean proportion of (a) undetected foragers and (b) undetected just-emerged bees over time with high (8–63 units, black dots) and low (less than eight units, white dots) field exposure values. The high non-detection levels during the first week correspond to the in-hive life stage before first exits in young bees. (c) A posteriori power analysis showing the ability (%) of the Cox PH survival analysis to detect the significant excess mortality due to field exposure out of random subsets of the 17 experimental colonies (n = 100 subsets for dots up to 14 colonies, and n = 50 and 16 subsets for 15 and 16 colonies, respectively). Dashed line shows the recommended 80% statistical power threshold.

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22 November 2015
Volume 282, issue 1819
Proceedings of the Royal Society B: Biological Sciences: 282 (1819)
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Keywords

Apis mellifera
imidacloprid
oilseed rape
pesticides
thiamethoxam
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Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees
Mickaël Henry, Nicolas Cerrutti, Pierrick Aupinel, Axel Decourtye, Mélanie Gayrard, Jean-François Odoux, Aurélien Pissard, Charlotte Rüger, Vincent Bretagnolle
Proc. R. Soc. B 2015 282 20152110; DOI: 10.1098/rspb.2015.2110. Published 18 November 2015
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Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees

Mickaël Henry, Nicolas Cerrutti, Pierrick Aupinel, Axel Decourtye, Mélanie Gayrard, Jean-François Odoux, Aurélien Pissard, Charlotte Rüger, Vincent Bretagnolle
Proc. R. Soc. B 2015 282 20152110; DOI: 10.1098/rspb.2015.2110. Published 18 November 2015

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