Conceived and designed the experiments: CAM MF JF Dv JSP. Performed the experiments: CAM MF SA RS. Analyzed the data: CAM. Contributed reagents/materials/analysis tools: CAM SA RS Dv JSP. Wrote the paper: CAM MF JF.
The authors have declared that no competing interests exist.
Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007–08 growing seasons.
We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm).
The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.
One third of honey bee colonies in the US were lost during each of the last three winters between ’06-’09
Pesticides have long been suspected as a potential cause of honey bee declines
Since 1999, beekeepers in France experiencing bee losses described as “mad bee disease” have blamed the systemic neonicotinoid pesticide, imidacloprid
The interactions between pesticides
During 2007 to 2008, we actively sampled beebread, trapped pollen, brood nest wax, beeswax foundation, and adult bees and brood for pesticide residues. These samples were drawn largely from commercial beekeepers from several states and one Canadian province, and included samples from apparently healthy colonies as well as from operations that were diagnosed as having CCD. Included in this survey were dead bees collected from local or community applications of insecticides. A comprehensive and sensitive analytical survey of 200 miticides, insecticides, fungicides and herbicides was conducted, including some no longer registered for use, to broadly assess known bee toxicants and other likely co-occurring pesticides. Here we document the plethora of pesticides that are currently present in US beehives and discuss their potential risks to honey bee health.
In 2007 and 2008 we analyzed pollen (total of 320 beebread, 28 trapped pollen, and 2 anther samples), 238 wax (derived mainly from the brood nest of colonies) and 21 foundation samples, and 34 immature (brood) and 106 adult bee samples for pesticide residues. These samples were collected as part of different studies and epidemiological surveys to investigate possible threats to colony health. The studies and surveys are described here. In January and February 2007, colonies resident in Florida and California distributed across 13 apiaries owned by 11 different beekeepers were selected to participate in multi-factorial study. Apiaries were classified as 1) having no colonies with CCD symptoms (‘control’) or 2) having colonies with CCD symptoms (‘CCD ’). Colonies were considered to have CCD symptoms when adult bee populations were in obvious decline leaving brood poorly attended, or were dead in an apiary having clear symptoms of CCD. In those CCD colonies where bees remained, there were insufficient number of bees to cover the brood, the remaining worker bees appeared young (i.e., adults bees that are unable to fly), and the queen was present. In a second study to investigate pesticides exposure to honey bee colonies engaged in apple pollination, samples of pollen, wax and bees were collected from 47 colonies in 2007 and 2008. These colonies were distributed in three Pennsylvania apple orchards with known pesticide application histories and a control location. In 2007, a longitudinal study was conducted which followed tagged colonies in three migratory operations as they moved from Florida up and down the east coast to pollinate a variety of crops (citrus, high bush blueberries, low bush blueberries, apples, cucumbers, squash, pumpkin). Samples of pollen, wax, and adult bees, and detailed colony measurements were taken each time these colonies were moved to a new crop. In this last survey
In some cases sampled colonies had a ∼15 cm by 10 cm section of brood comb removed and wrapped in aluminum foil and stored on dry ice until placed in a −80°C freezer. These sections of comb contained beeswax, beebread and brood. Beebread and brood were removed from the combs at room temperature and then stored along with the remaining beeswax at −20°C until processing. In other cases, samples of beebread collected in the field were removed from the brood nest of colonies using a spatula cleaned using Clorox® wipes and rinsed with 75% ethanol between collections. Beebread was placed in a 1.5 ml Eppendorf tube on dry ice until storage at −20°C. Samples of brood nest wax collected in the field were scraped with a sterilized standard hive tool into a 50 ml centrifuge tube and similarly stored. While care was taken to sample sections of the comb without honey, nectar, beebread or brood, small levels of cross-contamination were inevitable. Adult nurse bees were removed from the brood nest and placed into 50 ml centrifuge tubes on dry ice until they could be stored at −80°C.
In the apple orchard study, samples were field collected as described above but were placed on ice after collection and then stored in a standard freezer (−20°C). Beekeepers submitting samples were provided with a standardized protocol for collecting, storing and shipping samples. They were instructed to freeze all samples as soon as possible after collection and then ship samples overnight or second-day delivery in insulated containers with ice packs. Upon arrival these samples were stored in a standard freezer.
Foundation is processed beeswax pressed into sheets and used as templates for uniform comb construction. Wax samples from six different commercial and two private sources were analyzed. This included one sample of wax from wax-coated plastic foundation.
The majority of samples (749) we analyzed included brood nest wax and foundation, pollen and bees from colonies associated with the specific research projects described above. While the sampling was not completely random across time and space, it does include migratory or stationary colonies diagnosed as having “CCD” as well as those diagnosed as healthy, colonies placed in orchards with known pesticide application history as well as control colonies not placed in orchards, and samples submitted by beekeeper from colonies described as “unhealthy” as well as from those identified as “healthy.” The results and conclusion reported here are drawn mainly from these data. In addition, we analyzed 158 samples that included mixed matrices (pollen and wax),
Samples over the entire study were analyzed for 200 chemicals at an average of 171 pesticides and toxic metabolites per analysis. New compounds were added and others removed depending on lack of detection or negligible frequency of use where bees forage. Pesticide residue analysis was conducted by the USDA-AMS-NSL at Gastonia, NC. For multi-residue pesticide analysis, a modified QuEChERS method was used
For GC analyses, a dual layer solid-phase extraction (SPE) cartridge containing 250 mg of graphitized carbon black (GCB) and 500 mg of PSA is prepared with approximately 0.80 g of anhydrous MgSO4 added to the top of the cartridge. After conditioning the SPE cartridge by adding one cartridge volume (4.0 ml) of acetone/toluene (7∶3; v/v) using a positive pressure SPE manifold and eluting to waste, 2 ml of supernatant
Extracts of wax, beebread, and adult bees or brood were also analyzed for potentially toxic metabolites of primary miticide and insecticide detections. This included the respective oxon and the phenolic metabolite of coumaphos, chlorferone, the sulfoxide and sulfone metabolites of aldicarb, and the toxic olefin and 5-hydroxy metabolites of imidacloprid. Pesticides and metabolites were obtained in high-purity as standards from the EPA, Chem Service (West Chester, PA), or the manufacturer at the highest purity available.
Identity of parent pesticides and metabolites from extracts was based on co-chromatography with known standards by GC/MS and/or LC/MS-MS and consistent ratios of parent mass abundance to at least two fragment transitions. Standard parent mass and fragment ion transitions used
Honey bee LD50 values are averaged 24–72 h adult acute toxicities from the EPA-OPP Pesticide Ecotoxicity Database [
Mean, medians, percentiles, and standard errors of the means for individual pesticides and metabolites for all matrix-specific or paired pesticide analyses were calculated using 0 ppb for any non-detection (N.D.), unless otherwise noted. In-hive and between colony comparisons of pesticide detections were made by pairing 749 bee, pollen and wax sample analyses by colony/matrix, and then sorting colonies for concurrently-sampled matrices. This paired database of 519 analyses was further averaged according to matrix by colony identity if sampling dates were not identical. Significant trends were extracted by correlation followed by linear regression analysis of these data using Microsoft Excel Data Analysis package (ver. 11.5) or SAS JMP ver. 9.0. A two sample one way ANOVA was used to determine significant differences between compounds or treatments at the P<0.05 level.
Brood nest wax and foundations, beebread and trapped pollen, and adult bees and brood comprising 749 samples contained 118 different pesticides and metabolites, 4894 total residues of which 748 were systemics, and averaged 6.5 detections per sample. In the 259 wax samples (
Wax Pesticide |
Class |
Detects | Samples | % | Detections (ppb) | |||||||
Analyzed | High | Low | Median | 90%tile | 95%tile | Mean |
SEM |
LOD |
||||
Fluvalinate | PYR | 254 | 259 | 98.1 | 204000.0 | 2.0 | 3595.0 | 15080.0 | 28710.5 | 7473.8 | 973.6 | 1.0 |
Coumaphos | OP | 254 | 259 | 98.1 | 91900.0 | 1.0 | 1240.0 | 6875.0 | 11340.0 | 3300.4 | 499.8 | 1.0 |
Coumaphos oxon | OP | 187 | 208 | 89.9 | 1300.0 | 1.3 | 56.1 | 184.2 | 269.8 | 102.7 | 12.5 | 5.0 |
Chlorpyrifos | OP | 163 | 258 | 63.2 | 890.0 | 1.0 | 4.3 | 28.5 | 55.7 | 24.5 | 7.5 | 0.1 |
Chlorothalonil | FUNG | 127 | 258 | 49.2 | 53700.0 | 1.0 | 91.4 | 1552.0 | 2623.0 | 1066.6 | 453.4 | 1.0 |
DMPF (amitraz) | FORM | 107 | 177 | 60.5 | 43000.0 | 9.2 | 228.0 | 4718.0 | 8093.0 | 2199.8 | 574.2 | 4.0 |
Endosulfan I | CYC | 97 | 258 | 37.6 | 95.0 | 1.2 | 4.1 | 13.0 | 31.0 | 8.7 | 1.5 | 0.1 |
Endosulfan II | CYC | 65 | 258 | 25.2 | 39.0 | 1.1 | 3.8 | 10.9 | 21.2 | 6.2 | 0.8 | 0.1 |
DMA (amitraz) | FORM | 60 | 177 | 33.9 | 3820.0 | 120.0 | 437.0 | 1664.0 | 2433.0 | 742.1 | 104.6 | 50.0 |
Pendimethalin | HERB | 49 | 176 | 27.8 | 84.0 | 2.5 | 6.1 | 18.7 | 36.0 | 10.9 | 2.1 | 1.0 |
Fenpropathrin | PYR | 44 | 258 | 17.1 | 200.0 | 1.3 | 14.3 | 51.3 | 61.3 | 24.8 | 5.0 | 0.4 |
Esfenvalerate | PYR | 43 | 258 | 16.7 | 56.1 | 1.0 | 4.5 | 17.0 | 19.9 | 8.9 | 1.5 | 0.5 |
Azoxystrobin | S FUNG | 40 | 258 | 15.5 | 278.0 | 1.0 | 5.7 | 22.4 | 40.4 | 15.4 | 6.9 | 1.0 |
Methoxyfenozide | IGR | 39 | 208 | 18.8 | 495.0 | 3.5 | 42.3 | 171.0 | 271.4 | 81.5 | 17.2 | 0.4 |
Bifenthrin | PYR | 33 | 258 | 12.8 | 56.1 | 1.5 | 5.3 | 18.5 | 39.5 | 9.8 | 2.3 | 0.4 |
Endosulfan sulfate | CYC | 29 | 258 | 11.2 | 33.0 | 1.3 | 3.0 | 12.1 | 18.4 | 6.3 | 1.3 | 0.1 |
Atrazine | S HERB | 29 | 208 | 13.9 | 31.0 | 1.0 | 5.5 | 16.5 | 18.4 | 8.2 | 1.3 | 1.0 |
Dicofol | OC | 26 | 258 | 10.1 | 21.0 | 1.5 | 5.1 | 15.1 | 17.5 | 6.8 | 1.1 | 0.4 |
Aldicarb sulfoxide | S CARB | 22 | 208 | 10.6 | 649.0 | 13.4 | 298.5 | 609.2 | 638.8 | 306.6 | 48.0 | 20.0 |
Trifluralin | HERB | 22 | 176 | 12.5 | 36.0 | 1.0 | 1.4 | 2.2 | 21.0 | 3.9 | 1.8 | 1.0 |
Boscalid | S FUNG | 21 | 208 | 10.1 | 388.0 | 16.9 | 84.0 | 261.0 | 265.0 | 109.8 | 20.6 | 1.0 |
Carbendazim | S FUNG | 21 | 208 | 10.1 | 133.0 | 2.1 | 12.0 | 48.7 | 87.0 | 23.2 | 7.0 | 1.0 |
Oxyfluorfen | HERB | 16 | 258 | 6.2 | 34.0 | 2.1 | 6.1 | 26.5 | 29.1 | 11.1 | 2.6 | 0.5 |
Methidathion | OP | 15 | 258 | 5.8 | 78.7 | 2.9 | 10.0 | 23.0 | 40.5 | 15.3 | 4.8 | 1.0 |
Aldicarb sulfone | S CARB | 15 | 208 | 7.2 | 49.6 | 18.0 | 27.5 | 45.8 | 48.1 | 31.0 | 2.8 | 10.0 |
Iprodione | FUNG | 14 | 208 | 6.7 | 636.0 | 32.6 | 164.5 | 555.2 | 586.6 | 269.7 | 52.4 | 10.0 |
Pyrethrins | PYR | 13 | 208 | 6.3 | 222.0 | 19.0 | 78.7 | 151.4 | 181.2 | 84.5 | 16.9 | 20.0 |
Cypermethrin | PYR | 13 | 258 | 5.0 | 131.0 | 4.5 | 13.2 | 95.3 | 114.8 | 31.2 | 11.4 | 1.0 |
Norflurazon | S HERB | 13 | 208 | 6.3 | 38.1 | 1.1 | 2.9 | 5.6 | 18.7 | 5.8 | 2.7 | 1.0 |
Vinclozolin | FUNG | 13 | 258 | 5.0 | 27.0 | 1.2 | 4.6 | 21.7 | 24.6 | 8.8 | 2.4 | 1.0 |
Cyhalothrin | PYR | 13 | 258 | 5.0 | 16.9 | 1.0 | 5.7 | 13.2 | 15.3 | 6.5 | 1.3 | 0.1 |
Chlorferone (coumaphos) | OP | 11 | 176 | 6.3 | 4390.0 | 299.0 | 932.0 | 2830.0 | 3610.0 | 1236.7 | 381.6 | 25.0 |
Cyprodinil | S FUNG | 11 | 208 | 5.3 | 106.0 | 6.2 | 17.0 | 85.4 | 95.7 | 34.7 | 10.3 | 5.0 |
Cyfluthrin | PYR | 11 | 258 | 4.3 | 44.7 | 3.2 | 7.8 | 17.0 | 30.9 | 12.6 | 3.5 | 1.0 |
Pyraclostrobin | FUNG | 10 | 208 | 4.8 | 438.0 | 1.8 | 27.3 | 193.2 | 315.6 | 84.2 | 42.4 | 1.0 |
Fenbuconazole | S FUNG | 10 | 176 | 5.7 | 183.0 | 7.4 | 46.1 | 86.0 | 134.5 | 54.2 | 15.7 | 6.0 |
Tebufenozide | IGR | 10 | 208 | 4.8 | 27.7 | 2.0 | 5.3 | 18.3 | 23.0 | 8.0 | 2.6 | 2.0 |
Pronamide | S HERB | 10 | 208 | 4.8 | 22.8 | 1.7 | 3.0 | 12.5 | 17.6 | 6.1 | 2.1 | 1.0 |
Deltamethrin | PYR | 8 | 258 | 3.1 | 613.0 | 107.0 | 129.5 | 368.0 | 490.5 | 209.9 | 60.6 | 20.0 |
Allethrin | PYR | 8 | 208 | 3.8 | 139.0 | 1.7 | 9.2 | 62.1 | 100.5 | 28.0 | 16.1 | 1.0 |
Trifloxystrobin | PS FUNG | 8 | 258 | 3.1 | 22.4 | 2.6 | 4.2 | 12.0 | 17.2 | 6.7 | 2.3 | 0.5 |
Azinphos methyl | OP | 6 | 258 | 2.3 | 121.0 | 10.9 | 18.8 | 75.0 | 98.0 | 35.2 | 17.4 | 3.0 |
Tribufos = DEF | SYN | 6 | 208 | 2.9 | 59.0 | 7.6 | 19.3 | 44.1 | 51.5 | 25.1 | 7.4 | 2.0 |
Malathion | OP | 6 | 258 | 2.3 | 35.1 | 4.0 | 5.2 | 26.6 | 30.8 | 12.1 | 5.1 | 1.0 |
OC | 5 | 130 | 3.8 | 1050.0 | 6.9 | 30.9 | 642.7 | 846.3 | 228.0 | 205.5 | 6.0 | |
Permethrin | PYR | 5 | 258 | 1.9 | 372.0 | 31.0 | 227.8 | 333.6 | 352.8 | 209.6 | 58.2 | 10.0 |
Phosmet | OP | 5 | 258 | 1.9 | 209.0 | 2.9 | 28.3 | 157.8 | 183.4 | 69.0 | 37.3 | 2.0 |
DDE p,p' | OC | 5 | 208 | 2.4 | 31.0 | 5.5 | 11.3 | 30.9 | 31.0 | 17.2 | 5.7 | 3.0 |
Flutolanil | S FUNG | 4 | 208 | 1.9 | 105.0 | 7.2 | 54.2 | 102.1 | 103.5 | 55.2 | 26.1 | 4.0 |
Thiacloprid | S NEO | 4 | 208 | 1.9 | 7.8 | 1.9 | 5.9 | 7.5 | 7.7 | 5.4 | 1.3 | 1.0 |
Diazinon | OP | 4 | 208 | 1.9 | 4.3 | 1.4 | 1.6 | 3.5 | 3.9 | 2.2 | 0.7 | 1.0 |
Thiabendazole | S FUNG | 3 | 208 | 1.4 | 76.0 | 7.4 | 19.0 | 64.6 | 70.3 | 34.1 | 21.2 | 1.0 |
Fipronil | INS | 3 | 208 | 1.4 | 35.9 | 1.1 | 1.3 | 29.0 | 32.4 | 12.8 | 11.6 | 1.0 |
Dieldrin | CYC | 3 | 258 | 1.2 | 35.4 | 6.9 | 12.1 | 30.7 | 33.1 | 18.1 | 8.8 | 4.0 |
Pyrimethanil | FUNG | 3 | 208 | 1.4 | 27.8 | 3.4 | 11.7 | 24.6 | 26.2 | 14.3 | 7.2 | 2.0 |
Tebuthiuron | S HERB | 3 | 208 | 1.4 | 22.4 | 4.9 | 5.8 | 19.1 | 20.7 | 11.0 | 5.7 | 1.0 |
Chlorfenapyr | PS MITI | 3 | 176 | 1.7 | 11.9 | 1.3 | 3.6 | 10.2 | 11.1 | 5.6 | 3.2 | 1.0 |
Parathion methyl | OP | 3 | 208 | 1.4 | 6.1 | 3.8 | 4.0 | 5.7 | 5.9 | 4.6 | 0.7 | 1.0 |
Quintozene = PCNB | FUNG | 3 | 208 | 1.4 | 2.5 | 1.0 | 1.3 | 2.3 | 2.4 | 1.6 | 0.5 | 1.0 |
Ethofumesate | S HERB | 2 | 208 | 1.0 | 560.0 | 224.0 | 392.0 | 526.4 | 543.2 | 392.0 | 168.0 | 5.0 |
Propiconazole | S FUNG | 2 | 208 | 1.0 | 227.0 | 166.0 | 196.5 | 220.9 | 224.0 | 196.5 | 30.5 | 3.0 |
Piperonyl butoxide | SYN | 2 | 208 | 1.0 | 208.0 | 31.1 | 119.6 | 190.3 | 199.2 | 119.6 | 88.5 | 6.0 |
Dimethomorph | S FUNG | 2 | 176 | 1.1 | 133.0 | 58.0 | 95.5 | 125.5 | 129.3 | 95.5 | 37.5 | 15.0 |
Ethion | OP | 2 | 208 | 1.0 | 131.0 | 83.6 | 107.3 | 126.3 | 128.6 | 107.3 | 23.7 | 2.0 |
Captan | FUNG | 2 | 258 | 0.8 | 69.1 | 25.0 | 47.1 | 64.7 | 66.9 | 47.1 | 22.1 | 10.0 |
Fluoxastrobin | S FUNG | 2 | 208 | 1.0 | 44.5 | 23.1 | 33.8 | 42.4 | 43.4 | 33.8 | 10.7 | 4.0 |
Bendiocarb | S CARB | 2 | 257 | 0.8 | 22.0 | 5.5 | 13.8 | 20.4 | 21.2 | 13.8 | 8.3 | 2.0 |
Carbofuran, 3-hydroxy | S CARB | 2 | 208 | 1.0 | 21.1 | 12.4 | 16.8 | 20.2 | 20.7 | 16.8 | 4.4 | 3.0 |
Carfentrazone ethyl | PS HERB | 2 | 208 | 1.0 | 17.0 | 4.9 | 11.0 | 15.8 | 16.4 | 11.0 | 6.1 | 1.0 |
Imidacloprid | S NEO | 2 | 208 | 1.0 | 13.6 | 2.4 | 8.0 | 12.5 | 13.0 | 8.0 | 5.6 | 2.0 |
Tetradifon | MITI | 2 | 208 | 1.0 | 11.1 | 4.7 | 7.9 | 10.5 | 10.8 | 7.9 | 3.2 | 1.0 |
Metribuzin | S HERB | 2 | 208 | 1.0 | 8.0 | 1.0 | 4.5 | 7.3 | 7.7 | 4.5 | 3.5 | 1.0 |
Pyriproxyfen | IGR | 2 | 208 | 1.0 | 7.6 | 2.2 | 4.9 | 7.1 | 7.3 | 4.9 | 2.7 | 1.0 |
Prallethrin | PYR | 2 | 208 | 1.0 | 6.8 | 4.3 | 5.6 | 6.6 | 6.7 | 5.6 | 1.3 | 4.0 |
Fluridone | S HERB | 2 | 208 | 1.0 | 6.6 | 5.7 | 6.2 | 6.5 | 6.6 | 6.2 | 0.4 | 5.0 |
Fenamidone | FUNG | 1 | 208 | 0.5 | 138.0 | 138.0 | 138.0 | 138.0 | 138.0 | 138.0 | --- | 10.0 |
Heptachlor | CYC | 1 | 208 | 0.5 | 31.0 | 31.0 | 31.0 | 31.0 | 31.0 | 31.0 | --- | 4.0 |
Spirodiclofen | MITI | 1 | 208 | 0.5 | 28.5 | 28.5 | 28.5 | 28.5 | 28.5 | 28.5 | --- | 1.0 |
Heptachlor epoxide | CYC | 1 | 208 | 0.5 | 13.3 | 13.3 | 13.3 | 13.3 | 13.3 | 13.3 | --- | 1.0 |
Fenhexamid | FUNG | 1 | 176 | 0.6 | 9.3 | 9.3 | 9.3 | 9.3 | 9.3 | 9.3 | --- | 5.0 |
Carbofuran | S CARB | 1 | 208 | 0.5 | 5.8 | 5.8 | 5.8 | 5.8 | 5.8 | 5.8 | --- | 5.0 |
Pyridaben | MITI | 1 | 208 | 0.5 | 5.4 | 5.4 | 5.4 | 5.4 | 5.4 | 5.4 | --- | 1.0 |
Carbaryl | PS CARB | 1 | 208 | 0.5 | 4.5 | 4.5 | 4.5 | 4.5 | 4.5 | 4.5 | --- | 5.0 |
Tefluthrin | PYR | 1 | 208 | 0.5 | 3.3 | 3.3 | 3.3 | 3.3 | 3.3 | 3.3 | --- | 1.0 |
Triadimefon | S FUNG | 1 | 208 | 0.5 | 2.4 | 2.4 | 2.4 | 2.4 | 2.4 | 2.4 | --- | 2.0 |
Metalaxyl | S FUNG | 1 | 208 | 0.5 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | --- | 1.0 |
Hexachlorobenzene | FUNG | 1 | 258 | 0.4 | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 | --- | 0.1 |
*Carbendazim is also a degradate of benomyl; Thiabendazole is a degradate of thiophanate methyl.
Class: CAR = carbamate, CYC = cyclodiene, FORM = formamidine, FUNG = fungicide, HERB = herbicide, IGR = insect growth regulator, INS = misc. insecticide, MITI = miticide, NEO = neonicotinoid, OC = organochlorine, OP = organophosphate, PS = partial systemic, PYR = pyrethroid, S = systemic.
Mean and SEM for detections > LOD.
LOD = limit of detection (ppb).
Pollen Pesticide |
Class |
Detects | Samples | % | Detections (ppb) | |||||||
High | Low | Median | 90%tile | 95%tile | Mean |
SEM |
LOD† | |||||
Fluvalinate | PYR | 309 | 350 | 88.3 | 2670.0 | 1.6 | 40.2 | 186.8 | 323.0 | 95.1 | 12.6 | 1.0 |
Coumaphos | OP | 263 | 350 | 75.1 | 5828.0 | 1.0 | 13.1 | 518.4 | 892.0 | 180.4 | 33.0 | 1.0 |
Chlorpyrifos | OP | 153 | 350 | 43.7 | 830.0 | 0.1 | 4.4 | 140.4 | 226.5 | 53.3 | 10.6 | 0.1 |
Chlorothalonil | FUNG | 148 | 280 | 52.9 | 98900.0 | 1.1 | 35.0 | 9939.0 | 18765.0 | 3014.8 | 880.9 | 1.0 |
Pendimethalin | HERB | 113 | 247 | 45.7 | 1730.0 | 1.1 | 13.4 | 72.9 | 129.8 | 44.6 | 15.7 | 1.0 |
Endosulfan I | CYC | 98 | 350 | 28.0 | 76.7 | 0.4 | 4.2 | 33.9 | 47.2 | 10.9 | 1.5 | 0.1 |
Endosulfan sulfate | CYC | 92 | 350 | 26.3 | 35.0 | 0.2 | 2.2 | 9.2 | 11.3 | 4.3 | 0.6 | 0.1 |
DMPF (amitraz) | FORM | 77 | 247 | 31.2 | 1117.0 | 6.1 | 75.0 | 360.2 | 615.0 | 147.9 | 23.5 | 4.0 |
Atrazine | S HERB | 71 | 350 | 20.3 | 49.0 | 4.2 | 8.9 | 27.0 | 35.2 | 13.6 | 1.1 | 1.0 |
Endosulfan II | CYC | 70 | 350 | 20.0 | 67.7 | 0.1 | 3.8 | 24.7 | 39.6 | 9.1 | 1.6 | 0.1 |
Fenpropathrin | PYR | 63 | 350 | 18.0 | 170.0 | 0.4 | 7.0 | 24.6 | 60.8 | 15.1 | 3.3 | 0.4 |
Azoxystrobin | S FUNG | 53 | 350 | 15.1 | 107.0 | 1.0 | 10.2 | 58.9 | 68.1 | 21.0 | 3.3 | 1.0 |
Metolachlor | PS HERB | 52 | 350 | 14.9 | 103.0 | 2.6 | 8.1 | 19.4 | 44.6 | 13.4 | 2.5 | 2.0 |
Captan | FUNG | 45 | 350 | 12.9 | 10000.0 | 16.0 | 103.0 | 571.8 | 663.2 | 433.5 | 219.9 | 10.0 |
Esfenvalerate | PYR | 41 | 350 | 11.7 | 59.6 | 1.0 | 3.3 | 10.0 | 47.5 | 7.8 | 2.2 | 0.5 |
Carbaryl | PS CARB | 38 | 350 | 10.9 | 1010.0 | 13.6 | 36.7 | 269.5 | 602.9 | 117.1 | 36.5 | 5.0 |
Cyhalothrin | PYR | 38 | 350 | 10.9 | 28.0 | 0.1 | 1.7 | 4.3 | 18.2 | 3.4 | 0.9 | 0.1 |
THPI (captan) | PS FUNG | 35 | 247 | 14.2 | 363.0 | 60.1 | 227.0 | 312.0 | 342.0 | 205.8 | 15.1 | 30.0 |
Methoxyfenozide | IGR | 29 | 350 | 8.3 | 128.0 | 0.4 | 22.3 | 96.4 | 111.2 | 35.0 | 7.1 | 0.4 |
Dicofol | OC | 28 | 350 | 8.0 | 143.0 | 0.4 | 8.1 | 60.3 | 85.7 | 23.2 | 6.4 | 0.4 |
Trifloxystrobin | PS FUNG | 27 | 350 | 7.7 | 264.0 | 0.6 | 10.3 | 96.2 | 168.4 | 34.1 | 11.9 | 0.5 |
Tebufenozide | IGR | 27 | 350 | 7.7 | 58.4 | 2.0 | 12.5 | 28.9 | 30.0 | 14.8 | 2.4 | 2.0 |
Diazinon | OP | 27 | 350 | 7.7 | 29.0 | 1.0 | 4.6 | 25.6 | 27.7 | 9.2 | 1.8 | 1.0 |
Cypermethrin | PYR | 25 | 350 | 7.1 | 49.0 | 1.6 | 4.6 | 27.8 | 44.7 | 10.8 | 2.6 | 1.0 |
Cyfluthrin | PYR | 24 | 350 | 6.9 | 33.6 | 1.1 | 5.1 | 9.9 | 9.9 | 6.7 | 1.3 | 1.0 |
Azinphos methyl | OP | 23 | 350 | 6.6 | 643.0 | 3.9 | 22.0 | 104.7 | 615.3 | 86.2 | 37.1 | 3.0 |
Aldicarb sulfoxide | S CARB | 21 | 350 | 6.0 | 1245.0 | 22.0 | 327.0 | 1039.0 | 1146.0 | 493.7 | 85.7 | 20.0 |
Phosmet | OP | 20 | 350 | 5.7 | 418.0 | 3.7 | 38.0 | 284.2 | 351.7 | 110.0 | 28.3 | 2.0 |
Thiacloprid | S NEO | 19 | 350 | 5.4 | 115.0 | 1.7 | 14.0 | 42.9 | 108.7 | 23.8 | 7.2 | 1.0 |
Pyrimethanil | FUNG | 19 | 350 | 5.4 | 83.0 | 2.0 | 8.3 | 67.6 | 82.2 | 18.5 | 6.0 | 2.0 |
Norflurazon | S HERB | 18 | 350 | 5.1 | 108.0 | 2.8 | 23.5 | 54.3 | 66.9 | 29.7 | 6.0 | 1.0 |
1-Naphthol (carbaryl) | S CARB | 18 | 350 | 5.1 | 85.5 | 3.6 | 9.7 | 45.6 | 58.7 | 20.9 | 5.2 | 2.0 |
Metribuzin | S HERB | 18 | 350 | 5.1 | 44.0 | 1.0 | 3.3 | 10.1 | 15.6 | 6.3 | 2.3 | 1.0 |
Bifenthrin | PYR | 18 | 350 | 5.1 | 12.6 | 0.7 | 3.0 | 7.1 | 7.6 | 3.9 | 0.7 | 0.4 |
Carbendazim | S FUNG | 16 | 350 | 4.6 | 149.0 | 1.5 | 4.5 | 46.0 | 89.0 | 18.8 | 9.7 | 1.0 |
Cyprodinil | S FUNG | 15 | 350 | 4.3 | 344.0 | 5.3 | 18.7 | 246.8 | 286.6 | 90.2 | 29.1 | 5.0 |
Myclobutanil | S FUNG | 14 | 350 | 4.0 | 981.0 | 4.4 | 72.8 | 565.6 | 798.4 | 192.3 | 78.3 | 2.0 |
Propiconazole | S FUNG | 14 | 350 | 4.0 | 361.0 | 3.1 | 68.0 | 203.2 | 259.6 | 110.3 | 27.3 | 3.0 |
Fenbuconazole | S FUNG | 14 | 247 | 5.7 | 264.0 | 11.0 | 55.4 | 174.9 | 217.8 | 80.6 | 19.9 | 6.0 |
Coumaphos oxon | OP | 14 | 280 | 5.0 | 89.0 | 5.4 | 13.5 | 38.2 | 52.2 | 21.2 | 5.9 | 5.0 |
Methidathion | OP | 14 | 350 | 4.0 | 32.7 | 7.8 | 21.0 | 31.7 | 32.3 | 21.6 | 2.1 | 1.0 |
Malathion | OP | 13 | 350 | 3.7 | 61.0 | 0.9 | 5.9 | 16.2 | 35.2 | 10.4 | 4.4 | 1.0 |
Aldicarb sulfone | S CARB | 12 | 350 | 3.4 | 97.2 | 17.0 | 43.8 | 87.7 | 93.2 | 46.8 | 7.8 | 10.0 |
Simazine | S HERB | 12 | 350 | 3.4 | 54.0 | 5.2 | 22.0 | 36.9 | 44.7 | 22.4 | 4.3 | 5.0 |
Pronamide | S HERB | 11 | 350 | 3.1 | 378.0 | 17.7 | 71.0 | 355.0 | 366.5 | 122.9 | 38.7 | 1.0 |
Indoxacarb | INS | 11 | 350 | 3.1 | 330.0 | 10.0 | 102.0 | 175.0 | 252.5 | 118.2 | 24.7 | 10.0 |
Acetamiprid | S NEO | 11 | 350 | 3.1 | 134.0 | 14.0 | 57.0 | 101.0 | 117.5 | 59.3 | 11.8 | 5.0 |
Deltamethrin | PYR | 11 | 350 | 3.1 | 91.0 | 28.0 | 66.0 | 88.5 | 88.4 | 66.6 | 6.2 | 20.0 |
Imidacloprid | S NEO | 10 | 350 | 2.9 | 206.0 | 6.2 | 20.5 | 63.0 | 41.3 | 39.0 | 19.0 | 2.0 |
Fenhexamid | FUNG | 9 | 247 | 3.6 | 129.0 | 5.8 | 28.0 | 53.8 | 96.1 | 34.4 | 12.3 | 5.0 |
Permethrin | PYR | 9 | 350 | 2.6 | 92.0 | 9.6 | 28.7 | 89.6 | 73.8 | 40.1 | 10.7 | 10.0 |
Trifluralin | HERB | 9 | 247 | 3.6 | 14.4 | 1.0 | 1.9 | 10.9 | 12.6 | 3.9 | 1.6 | 1.0 |
Tebuthiuron | S HERB | 8 | 350 | 2.3 | 48.0 | 1.6 | 16.2 | 34.7 | 40.4 | 17.9 | 5.8 | 1.0 |
Thiabendazole | S FUNG | 8 | 350 | 2.3 | 5.6 | 1.4 | 2.4 | 4.8 | 5.2 | 3.0 | 0.5 | 1.0 |
Dimethomorph | S FUNG | 7 | 247 | 2.8 | 166.0 | 17.2 | 25.2 | 95.1 | 142.4 | 46.9 | 20.2 | 15.0 |
Oxyfluorfen | HERB | 7 | 350 | 2.0 | 4.5 | 0.5 | 1.8 | 3.1 | 3.8 | 2.0 | 0.5 | 0.5 |
Difenoconazole | S FUNG | 6 | 350 | 1.7 | 214.1 | 48.3 | 122.4 | 184.8 | 199.4 | 129.8 | 22.2 | 10.0 |
Famoxadone | FUNG | 6 | 350 | 1.7 | 141.0 | 73.5 | 95.7 | 125.5 | 133.3 | 98.3 | 10.9 | 20.0 |
Diphenylamine | FUNG | 6 | 103 | 5.8 | 32.0 | 3.6 | 10.5 | 24.5 | 28.3 | 13.2 | 4.3 | 2.0 |
Hexachlorobenzene | FUNG | 6 | 350 | 1.7 | 0.4 | 0.1 | 0.2 | 0.4 | 0.4 | 0.2 | 0.1 | 0.1 |
Pyridaben | MITI | 5 | 350 | 1.4 | 26.6 | 10.9 | 19.0 | 25.6 | 26.1 | 18.8 | 3.0 | 1.0 |
Diflubenzuron | IGR | 4 | 350 | 1.1 | 128.0 | 15.0 | 78.5 | 122.0 | 125.0 | 75.0 | 26.1 | 10.0 |
Oxamyl | S CARB | 4 | 350 | 1.1 | 43.0 | 20.0 | 32.5 | 40.3 | 41.7 | 32.0 | 4.7 | 5.0 |
Allethrin | PYR | 4 | 350 | 1.1 | 11.0 | 6.6 | 7.9 | 10.2 | 10.6 | 8.3 | 0.9 | 1.0 |
Vinclozolin | FUNG | 4 | 350 | 1.1 | 4.1 | 1.0 | 1.0 | 3.2 | 3.6 | 1.8 | 0.8 | 1.0 |
Boscalid | S FUNG | 3 | 350 | 0.9 | 962.0 | 1.4 | 12.0 | 772.0 | 11.5 | 325.1 | 318.4 | 1.0 |
Potasan (coumaphos) | OP | 3 | 247 | 1.2 | 160.0 | 61.5 | 138.0 | 155.6 | 157.8 | 119.8 | 29.9 | 10.0 |
Pyrethrins | PYR | 3 | 350 | 0.9 | 61.5 | 27.0 | 35.0 | 56.2 | 61.5 | 41.2 | 10.4 | 20.0 |
Tebuconazole | S FUNG | 3 | 350 | 0.9 | 34.0 | 6.4 | 18.0 | 30.8 | 32.4 | 19.5 | 8.0 | 3.0 |
Prallethrin | PYR | 3 | 350 | 0.9 | 7.6 | 4.7 | 7.3 | 7.5 | 7.6 | 6.5 | 0.9 | 4.0 |
Carfentrazone ethyl | PS HERB | 3 | 350 | 0.9 | 2.5 | 1.5 | 2.4 | 2.5 | 2.5 | 2.1 | 0.3 | 1.0 |
Propanil | HERB | 2 | 350 | 0.6 | 358.0 | 265.0 | 311.5 | 348.7 | 353.4 | 311.5 | 46.5 | 10.0 |
Pyraclostrobin | FUNG | 2 | 350 | 0.6 | 265.0 | 26.6 | 145.8 | 241.2 | 26.6 | 145.8 | 119.2 | 1.0 |
DDT p,p' | OC | 2 | 350 | 0.6 | 35.6 | 6.0 | 20.8 | 32.6 | 34.1 | 20.8 | 14.8 | 2.0 |
Fluridone | S HERB | 2 | 350 | 0.6 | 24.0 | 5.8 | 14.9 | 22.2 | 22.2 | 14.9 | 9.1 | 5.0 |
DDD p,p' | OC | 2 | 350 | 0.6 | 13.4 | 11.8 | 12.6 | 13.2 | 13.3 | 12.6 | 0.8 | 4.0 |
4,4-dibromobenzophenone | MITI | 2 | 247 | 0.8 | 10.8 | 2.2 | 6.5 | 9.9 | 10.4 | 6.5 | 4.3 | 2.0 |
Carbofuran, 3-hydroxy | S CARB | 2 | 350 | 0.6 | 4.6 | 3.6 | 4.1 | 4.5 | 4.6 | 4.1 | 0.5 | 3.0 |
DDE p,p' | OC | 2 | 350 | 0.6 | 4.3 | 3.3 | 3.8 | 4.2 | 4.3 | 3.8 | 0.5 | 3.0 |
Chlorfenapyr | PS MITI | 2 | 247 | 0.8 | 1.4 | 1.2 | 1.3 | 1.4 | 1.4 | 1.3 | 0.1 | 1.0 |
Diphenamid | S FUNG | 2 | 350 | 0.6 | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 | 0.0 | 1.0 |
Imidacloprid olefin | S NEO | 1 | 350 | 0.3 | 554.0 | 554.0 | 554.0 | 554.0 | 554.0 | 554.0 | --- | 25.0 |
Sethoxydim | S HERB | 1 | 350 | 0.3 | 173.0 | 173.0 | 173.0 | 173.0 | 173.0 | 173.0 | --- | 1.0 |
Acephate | S OP | 1 | 350 | 0.3 | 163.0 | 163.0 | 163.0 | 163.0 | 163.0 | 163.0 | --- | 35.0 |
Imidacloprid, 5-hydroxy | S NEO | 1 | 350 | 0.3 | 152.0 | 152.0 | 152.0 | 152.0 | 152.0 | 152.0 | --- | 25.0 |
Amicarbazone | HERB | 1 | 350 | 0.3 | 98.0 | 98.0 | 98.0 | 98.0 | 98.0 | 98.0 | --- | 30.0 |
Phenothrin | PYR | 1 | 350 | 0.3 | 83.9 | 83.9 | 83.9 | 83.9 | 83.9 | 83.9 | --- | 10.0 |
Fenamidone | FUNG | 1 | 350 | 0.3 | 73.9 | 73.9 | 73.9 | 73.9 | 73.9 | 73.9 | --- | 10.0 |
Thiamethoxam | S NEO | 1 | 350 | 0.3 | 53.3 | 53.3 | 53.3 | 53.3 | 53.3 | 53.3 | --- | 5.0 |
Phosalone | OP | 1 | 247 | 0.4 | 31.3 | 31.3 | 31.3 | 31.3 | 31.3 | 31.3 | --- | 10.0 |
Fipronil | INS | 1 | 350 | 0.3 | 28.5 | 28.5 | 28.5 | 28.5 | 28.5 | 28.5 | --- | 1.0 |
Chlorfenvinphos | OP | 1 | 247 | 0.4 | 10.7 | 10.7 | 10.7 | 10.7 | 10.7 | 10.7 | --- | 6.0 |
Iprodione | FUNG | 1 | 350 | 0.3 | 10.3 | 10.3 | 10.3 | 10.3 | 10.3 | 10.3 | --- | 10.0 |
Spiromesifen | S INS | 1 | 350 | 0.3 | 10.0 | 10.0 | 10.0 | 10.0 | 10.0 | 10.0 | --- | 10.0 |
Tetramethrin | PYR | 1 | 350 | 0.3 | 6.1 | 6.1 | 6.1 | 6.1 | 6.1 | 6.1 | --- | 6.0 |
Tribufos = DEF | SYN | 1 | 350 | 0.3 | 3.5 | 3.5 | 3.5 | 3.5 | 3.5 | 3.5 | --- | 2.0 |
Spirodiclofen | MITI | 1 | 350 | 0.3 | 1.9 | 1.9 | 1.9 | 1.9 | 1.9 | 1.9 | --- | 1.0 |
Heptachlor epoxide | CYC | 1 | 350 | 0.3 | 1.7 | 1.7 | 1.7 | 1.7 | 1.7 | 1.7 | --- | 1.0 |
*Carbendazim is also a degradate of benomyl; Thiabendazole is a degradate of thiophanate methyl.
Class: CAR = carbamate, CYC = cyclodiene, FORM = formamidine, FUNG = fungicide, HERB = herbicide, IGR = insect growth regulator, INS = misc. insecticide, MITI = miticide, NEO = neonicotinoid, OC = organochlorine, OP = organophosphate, PS = partial systemic, PYR = pyrethroid, S = systemic.
Mean and SEM for detections > LOD.
Bee Pesticide |
Class |
Detects | Samples | % | Detections (ppb) | |||||||
Analyzed | High | Low | Median | 90%tile | 95%tile | Mean |
SEM |
LOD |
||||
Fluvalinate | PYR | 117 | 140 | 83.6 | 5860.0 | 1.1 | 53.0 | 610.8 | 1710.0 | 357.7 | 94.5 | 1.0 |
Coumaphos | OP | 84 | 140 | 60.0 | 762.0 | 1.0 | 8.0 | 118.7 | 156.2 | 50.4 | 13.5 | 1.0 |
Chlorpyrifos | OP | 12 | 140 | 8.6 | 10.7 | 1.0 | 2.2 | 8.5 | 9.7 | 3.4 | 0.9 | 0.1 |
Chlorothalonil | FUNG | 10 | 140 | 7.1 | 878.0 | 1.5 | 7.2 | 121.1 | 499.5 | 100.2 | 86.5 | 1.0 |
Cypermethrin | PYR | 9 | 140 | 6.4 | 25.8 | 2.0 | 3.5 | 22.0 | 23.9 | 10.1 | 3.2 | 1.0 |
Permethrin | PYR | 8 | 140 | 5.7 | 19600.0 | 12.0 | 35.8 | 5919.2 | 12759.6 | 2478.1 | 2446.0 | 10.0 |
DMPF (amitraz) | FORM | 8 | 125 | 6.4 | 9040.0 | 6.0 | 117.5 | 3015.8 | 6027.9 | 1249.1 | 1114.1 | 4.0 |
Esfenvalerate | PYR | 8 | 140 | 5.7 | 9.3 | 1.0 | 3.5 | 8.5 | 8.9 | 4.3 | 1.2 | 0.5 |
Methidathion | OP | 7 | 140 | 5.0 | 32.0 | 6.5 | 12.0 | 28.4 | 30.2 | 16.2 | 3.6 | 1.0 |
Deltamethrin | PYR | 6 | 140 | 4.3 | 39.0 | 23.0 | 26.5 | 38.5 | 38.8 | 29.3 | 3.0 | 20.0 |
Pendimethalin | HERB | 6 | 140 | 4.3 | 27.6 | 6.5 | 14.0 | 26.4 | 27.0 | 15.9 | 3.8 | 1.0 |
Cyfluthrin | PYR | 5 | 140 | 3.6 | 14.0 | 2.0 | 10.0 | 13.2 | 13.6 | 8.2 | 2.4 | 1.0 |
Dicofol | OC | 5 | 140 | 3.6 | 3.8 | 1.0 | 1.4 | 3.6 | 3.7 | 2.1 | 0.6 | 0.4 |
Fenpropathrin | PYR | 4 | 140 | 2.9 | 37.0 | 2.8 | 14.2 | 32.8 | 34.9 | 17.1 | 8.0 | 0.4 |
Azinphos methyl | OP | 4 | 140 | 2.9 | 22.0 | 4.8 | 13.1 | 20.5 | 21.3 | 13.3 | 3.9 | 3.0 |
Cyprodinil | S FUNG | 4 | 140 | 2.9 | 19.0 | 9.2 | 11.0 | 16.6 | 17.8 | 12.6 | 2.2 | 5.0 |
THPI (captan) | PS FUNG | 3 | 125 | 2.4 | 43.4 | 37.7 | 39.5 | 42.6 | 43.0 | 40.2 | 1.7 | 30.0 |
Allethrin | PYR | 3 | 140 | 2.1 | 24.0 | 6.7 | 19.0 | 23.0 | 23.5 | 16.6 | 5.1 | 1.0 |
Tetramethrin | PYR | 3 | 140 | 2.1 | 23.0 | 18.0 | 23.0 | 23.0 | 23.0 | 21.3 | 1.7 | 6.0 |
Methoxyfenozide | IGR | 3 | 140 | 2.1 | 21.0 | 1.5 | 3.4 | 17.5 | 19.2 | 8.6 | 6.2 | 0.4 |
Endosulfan I | CYC | 3 | 140 | 2.1 | 6.1 | 1.3 | 1.6 | 5.2 | 5.7 | 3.0 | 1.6 | 0.1 |
Endosulfan sulfate | CYC | 3 | 140 | 2.1 | 3.0 | 1.6 | 2.7 | 2.9 | 3.0 | 2.4 | 0.4 | 0.1 |
Endosulfan II | CYC | 3 | 140 | 2.1 | 2.4 | 1.4 | 1.9 | 2.3 | 2.4 | 1.9 | 0.3 | 0.1 |
Parathion methyl | OP | 3 | 140 | 2.1 | 2.0 | 1.5 | 1.8 | 2.0 | 2.0 | 1.8 | 0.1 | 1.0 |
Cyhalothrin | PYR | 3 | 140 | 2.1 | 1.8 | 1.1 | 1.7 | 1.8 | 1.8 | 1.5 | 0.2 | 0.1 |
DMA (amitraz) | FORM | 2 | 125 | 1.6 | 4740.0 | 275.0 | 2507.5 | 4293.5 | 4516.8 | 2507.5 | 2232.5 | 50.0 |
Fipronil | INS | 2 | 140 | 1.4 | 3060.0 | 9.9 | 1535.0 | 2755.0 | 2907.5 | 1535.0 | 1525.1 | 1.0 |
Bifenthrin | PYR | 2 | 140 | 1.4 | 12.3 | 2.9 | 7.6 | 11.4 | 11.8 | 7.6 | 4.7 | 0.4 |
Dieldrin | CYC | 2 | 140 | 1.4 | 12.0 | 10.0 | 11.0 | 11.8 | 11.9 | 11.0 | 1.0 | 4.0 |
Prallethrin | PYR | 2 | 140 | 1.4 | 8.6 | 6.2 | 7.4 | 8.4 | 8.5 | 7.4 | 1.2 | 4.0 |
Coumaphos oxon | OP | 2 | 140 | 1.4 | 6.8 | 2.1 | 4.5 | 6.3 | 6.6 | 4.5 | 2.4 | 5.0 |
Oxyfluorfen | HERB | 2 | 140 | 1.4 | 4.8 | 3.8 | 4.3 | 4.7 | 4.8 | 4.3 | 0.5 | 0.5 |
Chlorfenapyr | PS MITI | 2 | 140 | 1.4 | 2.7 | 1.8 | 2.3 | 2.6 | 2.7 | 2.3 | 0.5 | 1.0 |
Carbaryl | PS CARB | 1 | 140 | 0.7 | 588.0 | 588.0 | 588.0 | 588.0 | 588.0 | 588.0 | --- | 5.0 |
1-Naphthol (carbaryl) | S CARB | 1 | 140 | 0.7 | 238.0 | 238.0 | 238.0 | 238.0 | 238.0 | 238.0 | --- | 2.0 |
Dimethomorph | S FUNG | 1 | 125 | 0.8 | 56.0 | 56.0 | 56.0 | 56.0 | 56.0 | 56.0 | --- | 15.0 |
Tebuconazole | S FUNG | 1 | 140 | 0.7 | 34.0 | 34.0 | 34.0 | 34.0 | 34.0 | 34.0 | --- | 3.0 |
Chlorferone (coumaphos) | OP | 1 | 125 | 0.8 | 25.0 | 25.0 | 25.0 | 25.0 | 25.0 | 25.0 | --- | 25.0 |
Tebufenozide | IGR | 1 | 140 | 0.7 | 23.0 | 23.0 | 23.0 | 23.0 | 23.0 | 23.0 | --- | 2.0 |
Fenoxaprop-ethyl | S HERB | 1 | 140 | 0.7 | 15.4 | 15.4 | 15.4 | 15.4 | 15.4 | 15.4 | --- | 6.0 |
Atrazine | S HERB | 1 | 140 | 0.7 | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | --- | 1.0 |
Carbendazim | S FUNG | 1 | 140 | 0.7 | 14.3 | 14.3 | 14.3 | 14.3 | 14.3 | 14.3 | --- | 1.0 |
Pyraclostrobin | FUNG | 1 | 140 | 0.7 | 8.6 | 8.6 | 8.6 | 8.6 | 8.6 | 8.6 | --- | 1.0 |
DDE p,p' | OC | 1 | 140 | 0.7 | 6.6 | 6.6 | 6.6 | 6.6 | 6.6 | 6.6 | --- | 3.0 |
Fluridone | S HERB | 1 | 140 | 0.7 | 6.5 | 6.5 | 6.5 | 6.5 | 6.5 | 6.5 | --- | 5.0 |
Pronamide | S HERB | 1 | 140 | 0.7 | 2.2 | 2.2 | 2.2 | 2.2 | 2.2 | 2.2 | --- | 1.0 |
*Carbendazim is also a degradate of benomyl; Thiabendazole is a degradate of thiophanate methyl.
Class: CAR = carbamate, CYC = cyclodiene, FORM = formamidine, FUNG = fungicide, HERB = herbicide, IGR = insect growth regulator, INS = misc. insecticide, MITI = miticide, NEO = neonicotinoid, OC = organochlorine, OP = organophosphate, PS = partial systemic, PYR = pyrethroid, S = systemic.
Mean and SEM for detections > LOD.
LOD = limit of detection (ppb).
Multiple residues prevailed in the bee, pollen and wax samples, with 2 or more pesticides detected in 92.3% of 749 analyzed (
Total Pesticide |
CLASS |
Samples Analyzed | LD50 |
Max Detection (ppb) | Wax (ppb) |
Bee (ppb) |
||||||||||||||
Wax | Pollen | Bee | Wax | Pollen | Bee | (ppb) | Wax | Pollen | Bee | Wax | Pollen | Bee | Mean | SEM | Mean | SEM | Mean | SEM | ||
Fluvalinate | PYR | 259 | 350 | 140 | 98.1 | 88.3 | 83.6 | 15860 | 204000 | 2670 | 5860 | 28703 | 294 | 1623 | 7329.5 | 956.9 | 83.9 | 11.2 | 299.0 | 79.7 |
Coumaphos | OP | 259 | 350 | 140 | 98.1 | 75.4 | 60.0 | 46300 | 94131 | 5828 | 762 | 11555 | 730 | 135 | 3363.4 | 511.8 | 137.4 | 25.4 | 30.5 | 8.4 |
Chlorpyrifos | OP | 258 | 350 | 140 | 63.2 | 43.7 | 8.6 | 1220 | 890 | 830 | 11 | 33 | 127 | 1 | 15.5 | 4.8 | 23.3 | 4.8 | 0.3 | 0.1 |
Chlorothalonil | FUNG | 258 | 280 | 140 | 49.2 | 52.9 | 7.1 | 1110000 | 53700 | 98900 | 878 | 1545 | 10380 | 3 | 525.0 | 225.2 | 1593.5 | 473.5 | 7.2 | 6.3 |
Amitraz | FORM | 177 | 247 | 125 | 61.6 | 31.2 | 6.4 | 750000 | 46060 | 1117 | 13780 | 4700 | 181 | 6 | 1080.7 | 327.1 | 32.5 | 7.3 | 107.2 | 104.2 |
Pendimethalin | HERB | 176 | 247 | 140 | 27.8 | 45.7 | 4.3 | 665000 | 84 | 1730 | 28 | 11 | 71 | 0 | 3.0 | 0.7 | 20.4 | 7.3 | 0.7 | 0.3 |
Endosulfan | CYC | 258 | 350 | 140 | 39.1 | 36.6 | 3.6 | 78700 | 132 | 157 | 9 | 22 | 33 | 0 | 5.5 | 1.0 | 6.0 | 1.0 | 0.2 | 0.1 |
Fenpropathrin | PYR | 258 | 350 | 140 | 17.1 | 18.0 | 2.9 | 500 | 200 | 170 | 37 | 30 | 12 | 0 | 4.2 | 1.0 | 2.7 | 0.7 | 0.5 | 0.3 |
Esfenvalerate | PYR | 258 | 350 | 140 | 16.7 | 11.7 | 5.7 | 2240 | 56 | 60 | 9 | 11 | 3 | 1 | 1.5 | 0.3 | 0.9 | 0.3 | 0.2 | 0.1 |
Atrazine | S HERB | 208 | 350 | 140 | 13.9 | 20.3 | 0.7 | 980000 | 31 | 49 | 15 | 8 | 17 | 0 | 1.1 | 0.3 | 2.8 | 0.4 | 0.1 | 0.1 |
Methoxyfenozide | IGR | 208 | 350 | 140 | 18.8 | 8.3 | 2.1 | 1000000 | 495 | 128 | 21 | 89 | 11 | 0 | 15.3 | 3.9 | 2.9 | 0.8 | 0.2 | 0.2 |
Azoxystrobin | S FUNG | 258 | 350 | 140 | 15.5 | 15.1 | 0.0 | 1120000 | 278 | 107 | 0 | 7 | 17 | 0 | 2.4 | 1.1 | 3.2 | 0.6 | 0.0 | 0.0 |
Bifenthrin | PYR | 258 | 350 | 140 | 12.8 | 5.1 | 1.4 | 150 | 56 | 13 | 12 | 6 | 0 | 0 | 1.3 | 0.4 | 0.2 | 0.1 | 0.1 | 0.1 |
Trifluralin | HERB | 176 | 247 | 125 | 12.5 | 3.6 | 0.0 | 685000 | 36 | 14 | 0 | 1 | 0 | 0 | 0.5 | 0.2 | 0.1 | 0.1 | 0.0 | 0.0 |
Aldicarb | S CARB | 208 | 350 | 140 | 10.6 | 6.0 | 0.0 | 3730 | 693 | 1342 | 0 | 217 | 92 | 0 | 27.8 | 7.9 | 31.2 | 8.4 | 0.0 | 0.0 |
Carbendazim | S FUNG | 208 | 350 | 140 | 10.1 | 4.6 | 0.7 | 500000 | 133 | 149 | 14 | 11 | 0 | 0 | 2.3 | 0.8 | 0.9 | 0.5 | 0.1 | 0.1 |
Boscalid | S FUNG | 208 | 350 | 140 | 10.1 | 0.9 | 0.0 | 1550000 | 388 | 962 | 0 | 80 | 0 | 0 | 11.1 | 3.1 | 2.8 | 2.7 | 0.0 | 0.0 |
Dicofol | OC | 258 | 350 | 140 | 10.1 | 8.0 | 3.6 | 370000 | 21 | 143 | 4 | 5 | 3 | 0 | 0.7 | 0.2 | 1.9 | 0.6 | 0.1 | 0.0 |
Iprodione | FUNG | 208 | 350 | 140 | 6.7 | 0.3 | 0.0 | 1020000 | 636 | 10 | 0 | 136 | 0 | 0 | 18.2 | 5.8 | 0.0 | 0.0 | 0.0 | 0.0 |
Norflurazon | S HERB | 208 | 350 | 140 | 6.3 | 5.1 | 0.0 | 1630000 | 38 | 108 | 0 | 2 | 2 | 0 | 0.4 | 0.2 | 1.5 | 0.5 | 0.0 | 0.0 |
Pyrethrins | PYR | 208 | 350 | 140 | 6.3 | 0.9 | 0.0 | 1480 | 222 | 62 | 0 | 22 | 0 | 0 | 5.3 | 1.7 | 0.4 | 0.2 | 0.0 | 0.0 |
Oxyfluorfen | HERB | 258 | 350 | 140 | 6.2 | 2.0 | 1.4 | 1000000 | 34 | 5 | 5 | 3 | 0 | 0 | 0.7 | 0.2 | 0.0 | 0.0 | 0.1 | 0.0 |
Methidathion | OP | 258 | 350 | 140 | 5.8 | 4.0 | 5.0 | 2010 | 79 | 33 | 32 | 4 | 0 | 0 | 0.9 | 0.3 | 0.9 | 0.2 | 0.8 | 0.3 |
Fenbuconazole | S FUNG | 176 | 247 | 125 | 5.7 | 5.7 | 0.0 | 1490000 | 183 | 264 | 0 | 11 | 0 | 0 | 3.1 | 1.3 | 4.6 | 1.6 | 0.0 | 0.0 |
Cyprodinil | S FUNG | 208 | 350 | 140 | 5.3 | 4.3 | 2.9 | 3320000 | 106 | 344 | 19 | 4 | 0 | 0 | 1.8 | 0.8 | 3.9 | 1.6 | 0.4 | 0.2 |
Cyhalothrin | PYR | 258 | 350 | 140 | 5.0 | 10.9 | 2.1 | 790 | 17 | 28 | 2 | 0 | 2 | 0 | 0.3 | 0.1 | 0.4 | 0.1 | 0.0 | 0.0 |
Cypermethrin | PYR | 258 | 350 | 140 | 5.0 | 7.1 | 6.4 | 1350 | 131 | 49 | 26 | 1 | 3 | 2 | 1.6 | 0.7 | 0.8 | 0.2 | 0.6 | 0.3 |
Vinclozolin | FUNG | 258 | 350 | 140 | 5.0 | 1.1 | 0.0 | 1000000 | 27 | 4 | 0 | 0 | 0 | 0 | 0.4 | 0.2 | 0.0 | 0.0 | 0.0 | 0.0 |
Tebufenozide | IGR | 208 | 350 | 140 | 4.8 | 7.7 | 0.7 | 2340000 | 28 | 58 | 23 | 0 | 8 | 0 | 0.4 | 0.2 | 1.1 | 0.3 | 0.2 | 0.2 |
Pronamide | S HERB | 208 | 350 | 140 | 4.8 | 3.1 | 0.7 | 1580000 | 23 | 378 | 2 | 0 | 0 | 0 | 0.3 | 0.1 | 3.9 | 1.6 | 0.0 | 0.0 |
Pyraclostrobin | FUNG | 208 | 350 | 140 | 4.8 | 0.6 | 0.7 | 870000 | 438 | 265 | 9 | 0 | 0 | 0 | 4.0 | 2.3 | 0.8 | 0.8 | 0.1 | 0.1 |
Cyfluthrin | PYR | 258 | 350 | 140 | 4.3 | 6.9 | 3.6 | 220 | 45 | 34 | 14 | 0 | 2 | 0 | 0.5 | 0.2 | 0.5 | 0.1 | 0.3 | 0.2 |
Allethrin | PYR | 208 | 350 | 140 | 3.8 | 1.1 | 2.1 | 48800 | 139 | 11 | 24 | 0 | 0 | 0 | 1.1 | 0.7 | 0.1 | 0.0 | 0.4 | 0.2 |
Trifloxystrobin | PS FUNG | 258 | 350 | 140 | 3.1 | 7.7 | 0.0 | 1750000 | 22 | 264 | 0 | 0 | 5 | 0 | 0.2 | 0.1 | 2.6 | 1.0 | 0.0 | 0.0 |
Deltamethrin | PYR | 258 | 350 | 140 | 3.1 | 3.1 | 4.3 | 500 | 613 | 91 | 39 | 0 | 0 | 0 | 6.5 | 2.9 | 2.1 | 0.6 | 1.3 | 0.5 |
Azinphos methyl | OP | 258 | 350 | 140 | 2.3 | 6.6 | 2.9 | 2420 | 121 | 643 | 22 | 0 | 10 | 0 | 0.8 | 0.5 | 5.7 | 2.6 | 0.4 | 0.2 |
Malathion | OP | 258 | 350 | 140 | 2.3 | 3.7 | 0.0 | 3950 | 35 | 61 | 0 | 0 | 0 | 0 | 0.3 | 0.2 | 0.4 | 0.2 | 0.0 | 0.0 |
Phosmet | OP | 258 | 350 | 140 | 1.9 | 5.7 | 0.0 | 8030 | 209 | 418 | 0 | 0 | 2 | 0 | 1.3 | 0.9 | 6.3 | 2.1 | 0.0 | 0.0 |
Permethrin | PYR | 258 | 350 | 140 | 1.9 | 2.6 | 5.7 | 1120 | 372 | 92 | 19600 | 0 | 0 | 12 | 4.1 | 2.1 | 1.0 | 0.4 | 141.6 | 140.0 |
Diazinon | OP | 208 | 350 | 140 | 1.9 | 7.7 | 0.0 | 2220 | 4 | 29 | 0 | 0 | 3 | 0 | 0.0 | 0.0 | 0.7 | 0.2 | 0.0 | 0.0 |
Thiacloprid | S NEO | 208 | 350 | 140 | 1.9 | 5.4 | 0.0 | 252000 | 8 | 115 | 0 | 0 | 5 | 0 | 0.1 | 0.1 | 1.3 | 0.5 | 0.0 | 0.0 |
Pyrimethanil | FUNG | 208 | 350 | 140 | 1.4 | 5.4 | 0.0 | 1000000 | 28 | 83 | 0 | 0 | 1 | 0 | 0.2 | 0.1 | 1.0 | 0.4 | 0.0 | 0.0 |
Tebuthiuron | S HERB | 208 | 350 | 140 | 1.4 | 2.3 | 0.0 | 650000 | 22 | 48 | 0 | 0 | 0 | 0 | 0.2 | 0.1 | 0.4 | 0.2 | 0.0 | 0.0 |
Thiabendazole | S FUNG | 208 | 350 | 140 | 1.4 | 2.3 | 0.0 | 500000 | 76 | 6 | 0 | 0 | 0 | 0 | 0.5 | 0.4 | 0.1 | 0.0 | 0.0 | 0.0 |
Fipronil | INS | 208 | 350 | 140 | 1.4 | 0.3 | 1.4 | 50 | 36 | 29 | 3060 | 0 | 0 | 0 | 0.2 | 0.2 | 0.1 | 0.1 | 21.9 | 21.9 |
Dimethomorph | S FUNG | 176 | 247 | 125 | 1.1 | 2.8 | 0.8 | 308000 | 133 | 166 | 56 | 0 | 0 | 0 | 1.1 | 0.8 | 1.3 | 0.7 | 0.4 | 0.4 |
Metribuzin | S HERB | 208 | 350 | 140 | 1.0 | 5.1 | 0.0 | 567000 | 8 | 44 | 0 | 0 | 1 | 0 | 0.0 | 0.0 | 0.3 | 0.1 | 0.0 | 0.0 |
Propiconazole | S FUNG | 208 | 350 | 140 | 1.0 | 4.0 | 0.0 | 625000 | 227 | 361 | 0 | 0 | 0 | 0 | 1.9 | 1.3 | 4.4 | 1.6 | 0.0 | 0.0 |
Imidacloprid | S NEO | 208 | 350 | 140 | 1.0 | 2.9 | 0.0 | 280 | 14 | 912 | 0 | 0 | 0 | 0 | 0.1 | 0.1 | 3.1 | 1.0 | 0.0 | 0.0 |
Captan | PS FUNG | 258 | 350 | 140 | 0.8 | 17.7 | 2.1 | 1080000 | 69 | 10000 | 43 | 0 | 326 | 0 | 0.4 | 0.3 | 76.3 | 29.6 | 0.9 | 0.5 |
Fenhexamid | FUNG | 176 | 247 | 125 | 0.6 | 3.6 | 0.0 | 1580000 | 9 | 129 | 0 | 0 | 0 | 0 | 0.1 | 0.1 | 1.3 | 0.6 | 0.0 | 0.0 |
Carbaryl | PS CARB | 208 | 350 | 140 | 0.5 | 11.4 | 0.7 | 10500 | 5 | 1050 | 826 | 0 | 45 | 0 | 0.0 | 0.0 | 13.8 | 4.7 | 5.9 | 5.9 |
Metolachlor | PS HERB | 208 | 350 | 140 | 0.0 | 14.9 | 0.0 | 1260000 | 0 | 103 | 0 | 0 | 10 | 0 | 0.0 | 0.0 | 2.0 | 0.4 | 0.0 | 0.0 |
Myclobutanil | S FUNG | 208 | 350 | 140 | 0.0 | 4.0 | 0.0 | 1870000 | 0 | 981 | 0 | 0 | 0 | 0 | 0.0 | 0.0 | 7.7 | 3.6 | 0.0 | 0.0 |
Simazine | S HERB | 208 | 350 | 140 | 0.0 | 3.4 | 0.0 | 967000 | 0 | 54 | 0 | 0 | 0 | 0 | 0.0 | 0.0 | 0.8 | 0.3 | 0.0 | 0.0 |
Acetamiprid | S NEO | 208 | 350 | 140 | 0.0 | 3.1 | 0.0 | 99000 | 0 | 134 | 0 | 0 | 0 | 0 | 0.0 | 0.0 | 1.9 | 0.7 | 0.0 | 0.0 |
Indoxacarb | INS | 208 | 350 | 140 | 0.0 | 3.1 | 0.0 | 600000 | 0 | 330 | 0 | 0 | 0 | 0 | 0.0 | 0.0 | 3.7 | 1.3 | 0.0 | 0.0 |
Pyrethroids | PYR | 259 | 350 | 140 | 98.8 | 92.6 | 86.4 | ---- | 204000 | 2670 | 19626 | 28706 | 307 | 1680 | 7354.5 | 956.6 | 93.2 | 11.3 | 444.6 | 159.3 |
Organophosphates | OP | 259 | 350 | 140 | 99.6 | 92.6 | 62.9 | ---- | 94131 | 5828 | 762 | 11584 | 823 | 137 | 3383.1 | 511.7 | 175.2 | 25.7 | 32.0 | 8.4 |
Carbamates | CARB | 208 | 350 | 140 | 13.0 | 18.0 | 0.7 | ---- | 693 | 1342 | 826 | 217 | 308 | 0 | 28.1 | 7.9 | 45.4 | 9.5 | 5.9 | 5.9 |
Insecticides | Total | 259 | 350 | 140 | 99.6 | 98.9 | 91.4 | ---- | 213597 | 5832 | 19630 | 43006 | 1306 | 3190 | 11872.4 | 1131.2 | 370.0 | 30.7 | 612.4 | 187.1 |
Fungicides | FUNG | 258 | 350 | 140 | 63.2 | 60.6 | 12.9 | ---- | 53705 | 98905 | 897 | 1578 | 3930 | 36 | 563.1 | 224.8 | 1388.1 | 381.2 | 9.2 | 6.4 |
Herbicides | HERB | 208 | 350 | 140 | 41.8 | 50.3 | 6.4 | ---- | 560 | 1750 | 28 | 29 | 102 | 7 | 7.8 | 2.7 | 28.8 | 5.7 | 1.0 | 0.4 |
Systemics | S | 208 | 350 | 140 | 57.7 | 60.9 | 10.7 | ---- | 723 | 1436 | 845 | 364 | 609 | 15 | 53.8 | 9.4 | 117.2 | 12.7 | 8.2 | 6.1 |
Pesticides | Total | 259 | 350 | 140 | 99.6 | 99.1 | 91.4 | ---- | 213597 | 99936 | 19630 | 43492 | 7740 | 3219 | 12443.3 | 1145.5 | 1786.9 | 385.3 | 622.6 | 187.4 |
*Aldicarb based on sulfoxide and sulfone metabolites; Amitraz based on total DMA and DMPF metabolites; Captan includes THPI; Carbaryl includes 1-naphthol; Carbendazim is also a degradate of benomyl; Coumaphos includes oxon, chlorferone and potasan; Endosulfan includes isomers and sulfate; Imidacloprid includes 5-hydroxy and olefin metabolites; Thiabendazole is a degradate of thiophanate methyl.
Class: CAR = carbamate, CYC = cyclodiene, FORM = formamidine, FUNG = fungicide, HERB = herbicide, IGR = insect growth regulator.
INS = misc. insecticide, NEO = neonicotinoid, OC = organochlorine, OP = organophosphate, PS = partial systemic, PYR = pyrethroid, S = systemic.
LD50 is ave. honey bee acute toxicity from literature in ppb = 10,000× µg/bee; bold nos. < LD50.
Mean and SEM for all analyzed samples; non detects = 0 ppb.
Focused analysis of detections from only the pollen and wax further indicates the high potential of bee exposure to hive pesticide residues. Two or more pesticides were found in 98.4%, three or more in 91%, and four or more in 80% of the 609 samples analyzed. Almost 60% of these pollen and wax samples, in contrast to 10.7% of bee samples, contained at least one systemic pesticide, 57% in combination with a pyrethroid. The most frequent binary combination was fluvalinate and coumaphos (83.1% of samples), followed by fluvalinate with chlorothalonil (50.0%), coumaphos with chlorothalonil (47.8%), and fluvalinate with chlorpyrifos (46.7%). All 375 pollen or wax samples with a fungicide residue (61.7%) had at least one other insecticide or miticide present, and except for 6 or 8 of these samples, respectively, contained a pyrethroid or organophosphate. The most prevalent triple detections were fluvalinate and coumaphos combined with chlorothalonil (47.2%), chlorpyrifos (41.0%), degradates of amitraz (41.0%), or with one of 43 systemic pesticides (47.9%). At least one each of an insecticide/acaricide, fungicide or herbicide were found in 34.8% of samples, with the fluvalinate, chlorothalonil and pendimethalin combination most frequent (20.6%). The highest frequency of quaternary detections were fluvalinate, coumaphos and amitraz combined with chlorothalonil (30.7%) or chlorpyrifos (20.3%), or fluvalinate, coumaphos and chlorothalonil combined with a systemic (31.4%) or chlorpyrifos (26.2%).
The most frequently found residues were from fluvalinate and coumaphos, followed in order by chlorpyrifos, chlorothalonil, amitraz, pendimethalin, endosulfan, fenpropathrin, esfenvalerate and atrazine. These top ten comprise three in-hive miticides and five insecticidal, one fungicidal and one herbicidal crop protection agents (
Lower residues of pesticides prevailed in bees except for occasional samples associated with high mortality (see below) or with notable miticide (up to 14 ppm), and near ppm carbaryl and chlorothalonil detections (
Pesticide residues ranged over six orders of magnitude (1 million-fold), and wide-differences in mean, and 90%- and 95%-tile values (levels at which only 10% or 5% of detections, respectively, are higher) per matrix were found (
The highly-lipophilic fluvalinate and amitraz degradates (DMPF and DMA) bioaccumulate in bees to a much greater extent than does coumaphos, as indicated by the respective 3.6- and 3.3-times greater bee to pollen ratios of mean residue values relative to a 4.5-fold lower ratio for coumaphos (
Comparison of ppb residue levels across matrices with known LD50 values for honey bees in ppb relative to body weight provided only a few detections at or well above the lethal dose (
Pairing by colony/matrix for concurrently-sampled matrices, reduced our database to 519 analyses that averaged 6.5 detections per sample representing 102 different pesticides and metabolites. Colony analyses were then averaged according to matrix if sampling dates were not identical. The following significant trends were extracted by correlation followed by linear regression analysis of these data. Fluvalinate accounts for most of the miticide content of bees (bee miticide = 1.016 • bee fluvalinate +27.5 ppb; r2 = 0.9967,
Regressions of bee fluvalinate with total miticides (A), wax fluvalinate with total miticides (B), bee fluvalinate with total pesticides (C), and of wax miticides with total pesticides (D).
Noteworthy trends uncovered here for pollen pesticide residues resulted from their high fungicide content. Most fungicide contents in bee-collected pollen were due to chlorothalonil (pollen fungicides = 0.9975 • pollen chlorothalonil +8.2 ppb; r2 = 0.9991,
Regressions of pollen chlorothalonil (A) and wax chlorothalonil (B) with total fungicides.
Slopes from linear regression analyses, although with high variance, are consistent with pollen being the probable source of wax chlorothalonil (wax chlorothalonil = 0.502 • pollen chlorothalonil +79 ppb; r2 = 0.385,
Twenty-one wax samples from six different commercial and two private foundation sources were uniformly contaminated with up to 10.1 ppm fluvalinate (mean of 2±0.6 ppm) and up to 14.3 ppm coumaphos (mean of 3.3±1.0 ppm,
Pesticide |
Class |
Detects | Samples | % | Detections (ppb) | ||||||
Analyzed | High | Low | Median | 90%tile | 95%tile | Mean |
SEM |
||||
Fluvalinate | PYR | 21 | 21 | 100.0 | 10120.0 | 2.0 | 455.0 | 6020.0 | 9810.0 | 2006.1 | 661.4 |
Coumaphos | OP | 20 | 21 | 95.2 | 14300.0 | 1.0 | 1350.0 | 8867.0 | 12875.0 | 3315.1 | 962.7 |
Chlorpyrifos | OP | 17 | 21 | 81.0 | 110.0 | 1.4 | 10.0 | 51.8 | 76.4 | 22.2 | 7.1 |
Endosulfan I | CYC | 8 | 21 | 38.1 | 11.0 | 1.2 | 2.4 | 5.8 | 8.4 | 3.3 | 1.1 |
Coumaphos oxon | OP | 7 | 13 | 53.8 | 102.0 | 6.5 | 27.3 | 62.4 | 82.2 | 36.0 | 11.6 |
Chlorothalonil | FUNG | 6 | 21 | 28.6 | 60.0 | 1.3 | 11.4 | 39.1 | 49.6 | 18.2 | 8.7 |
Cypermethrin | PYR | 5 | 21 | 23.8 | 131.0 | 6.5 | 8.3 | 120.2 | 125.6 | 51.6 | 27.3 |
Endosulfan II | CYC | 5 | 21 | 23.8 | 4.7 | 1.1 | 1.9 | 3.6 | 4.1 | 2.1 | 0.7 |
Cyfluthrin | PYR | 4 | 21 | 19.0 | 14.0 | 6.9 | 7.4 | 12.1 | 13.1 | 8.9 | 1.7 |
Esfenvalerate | PYR | 4 | 21 | 19.0 | 19.0 | 1.1 | 2.8 | 14.2 | 16.6 | 6.4 | 4.2 |
Pendimethalin | HERB | 2 | 11 | 18.2 | 7.2 | 7.1 | 7.2 | 7.2 | 7.2 | 7.2 | 0.0 |
Trifluralin | HERB | 2 | 11 | 18.2 | 36.0 | 2.2 | 19.1 | 32.6 | 34.3 | 19.1 | 16.9 |
Allethrin | PYR | 2 | 13 | 15.4 | 139.0 | 9.5 | 74.3 | 126.1 | 132.5 | 74.3 | 64.8 |
Fluridone | S HERB | 2 | 13 | 15.4 | 6.6 | 5.7 | 6.2 | 6.5 | 6.6 | 6.2 | 0.4 |
Vinclozolin | FUNG | 2 | 21 | 9.5 | 1.7 | 1.2 | 1.5 | 1.7 | 1.7 | 1.5 | 0.3 |
OC | 1 | 3 | 33.3 | 6.9 | 6.9 | 6.9 | 6.9 | 6.9 | 6.9 | --- | |
Atrazine | S HERB | 1 | 13 | 7.7 | 31.0 | 31.0 | 31.0 | 31.0 | 31.0 | 31.0 | --- |
Norflurazon | S HERB | 1 | 13 | 7.7 | 38.1 | 38.1 | 38.1 | 38.1 | 38.1 | 38.1 | --- |
Parathion methyl | OP | 1 | 13 | 7.7 | 3.8 | 3.8 | 3.8 | 3.8 | 3.8 | 3.8 | --- |
Tebuthiuron | S HERB | 1 | 13 | 7.7 | 5.8 | 5.8 | 5.8 | 5.8 | 5.8 | 5.8 | --- |
Thiabendazole | S FUNG | 1 | 13 | 7.7 | 76.0 | 76.0 | 76.0 | 76.0 | 76.0 | 76.0 | --- |
Dicofol | OC | 1 | 21 | 4.8 | 2.3 | 2.3 | 2.3 | 2.3 | 2.3 | 2.3 | --- |
Endosulfan sulfate | CYC | 1 | 21 | 4.8 | 1.6 | 1.6 | 1.6 | 1.6 | 1.6 | 1.6 | --- |
Fenpropathrin | PYR | 1 | 21 | 4.8 | 25.0 | 25.0 | 25.0 | 25.0 | 25.0 | 25.0 | --- |
Methidathion | OP | 1 | 21 | 4.8 | 14.0 | 14.0 | 14.0 | 14.0 | 14.0 | 14.0 | --- |
Phosmet | OP | 1 | 21 | 4.8 | 2.9 | 2.9 | 2.9 | 2.9 | 2.9 | 2.9 | --- |
Trifloxystrobin | PS FUNG | 1 | 21 | 4.8 | 3.5 | 3.5 | 3.5 | 3.5 | 3.5 | 3.5 | --- |
*Thiabendazole is a degradate of thiophanate methyl.
Class: CAR = carbamate, CYC = cyclodiene, FORM = formamidine, FUNG = fungicide, HERB = herbicide, IGR = insect growth regulator, INS = misc. insecticide, MITI = miticide, NEO = neonicotinoid, OC = organochlorine, OP = organophosphate, PS = partial systemic, PYR = pyrethroid, S = systemic.
Mean and SEM for detections > LOD.
LOD = limit of detection (ppb).
Substantial levels of coumaphos oxon, the toxiPlos finished live paper--pone.0009730 oxidative metabolite of coumaphos, and the related degradate, chlorferone were frequently detected in comb wax (
We found 121 different pesticides and metabolites comprising 5519 total residues within 887 wax, pollen, bee and associated hive samples (average of 6.2 detections per sample) from 23 states and one Canadian province (
We have found unprecedented levels of miticides and agricultural pesticides in honey bee colonies from across the US and one Canadian province. While these samples were not part of a full-scale landscape or grower-level survey, the data contained here is the largest sampling of pesticide residues in N. American bee colonies or worldwide to date, and represents a cost of nearly $175,000 for the analyses alone. We attempt here to draw trends from these data to indicate both potential risks for bee health as well as justifying the need for greater investments in monitoring pesticide residues in the future.
While a slightly larger number of pesticides are found by including materials associated with beekeeping such as corn syrup, pollen substitute, royal jelly, honey and floral nectars, the trends are well represented by the hive contents of pollen, wax, and bees. A comparison of
High levels of fluvalinate and coumaphos are co-occuring with lower but significant levels of 98 other insecticides, fungicides and herbicides in pollen. Most noteworthy were the very high levels of the fungicide chlorothalonil in pollen and wax (
As pollen is the main protein source for developing brood and is intimately involved in development of the hypopharyngeal glands of nurse bees
It is well documented that neonicotinoid pesticides occur in pollen at levels that affect the learning ability of bees fed such pollen
Growers of many bee-pollinated crops routinely apply fungicides during bloom, while pollinators are present
Beeswax remains the ultimate sink from the long-term use of the miticides fluvalinate, coumaphos, amitraz (
Almost all wax and pollen samples (98.4%) contained two or more pesticide residues, of which greater than 83% were fluvalinate and coumaphos (
Almost 60% of our pollen and wax samples, in contrast to 11% of bee samples, contained at least one of 43 systemic pesticides, 57% in combination with a pyrethroid. Substantial amounts of potentially synergistic fungicides such as cyprodinil, fenbuconazole, myclobutanil and propiconazole were also found. Fungicides generally have low bee toxicity by themselves, but exceptions with captan and the ergosterol biosynthesis inhibitor (EBI) propiconazole have been reported
Bees generally have lower pesticide residues than pollen [
Externally-derived, highly-toxic pyrethroids, up to 9 in addition to fluvalinate per sample, were the most frequent and dominant class of insecticides in our samples. Pyrethroids are frequently associated with bee kills
Pyrethroids other than fluvalinate have been reported to impact the foraging capabilities of honey bees. After topical application with 0.009 µg permethrin/bee (approx. 90 ppb body weight), none of the foraging workers returned to the hive at days end
Other classes of pesticides have been associated with bee kills including 3.1 ppm of the phenylpyrazole fipronil (
Pesticide metabolites (enzymatically-produced) and degradates (chemically-produced or of unknown origin) can be as toxic and are often more systemic than their respective parent compounds. Systemic movement can enhance their levels in floral pollens and nectars, but their increased water solubility can also facilitate excretion from bees. Much higher amounts of the more bee-toxic aldicarb sulfoxide than its sulfone
The affects of chronic exposure to pyrethroids, organophosphates, neonicotinoids, fungicides and other pesticides can range from lethal and/or sub-lethal effects in brood and workers to reproductive effects on the queen
Systemic neonicotinoid use has greatly increased recently for treating seeds of many major crops, particularly those genetically-engineered
The high frequency of multiple pesticides in bee collected pollen and wax indicates that pesticide interactions need thorough investigation before their roles in decreasing bee health can be either supported or refuted. The large number of studies to date, are limited by being done on mostly one compound at a time, as well as using whole colonies where the timing of contaminated pollen intake and its utilization by the colony are difficult to interpret as a causal relationship. Laboratory studies have clearly indicated sublethal impacts on honey bee learning
Fluvalinate has been considered a relatively “safe” material for honey bees by the beekeeping industry; however its history is unclear with potentially significant implications for honey bee health. The original formulation of fluvalinate had an established lethal dose that killed 50% of the tested population (LD50) of 65.85 µg/bee for honey bees, which is considered relatively non-toxic
Widely-occurring
The widespread occurrence of multiple residues, some at toxic levels for single compounds, and the lack of any scientific literature on the biological consequences of combinations of pesticides, argues strongly for urgent changes in regulatory policies regarding pesticide registration and monitoring procedures as they relate to pollinator safety. This further calls for emergency funding to address the myriad holes in our scientific understanding of pesticide consequences for pollinators. The relegation of bee toxicity for registered compounds to impact only label warnings, and the underestimation of systemic pesticide hazards to bees in the registration process may well have contributed to widespread pesticide contamination of pollen, the primary food source of our major pollinator. Is risking the $14 billion contribution of pollinators to our food system really worth lack of action?
Summary of pesticide detections in 887 North American beehive and related samples.
(0.37 MB DOC)
Summary of pesticides and their metabolites not detected in 887 North American beehive and related samples.
(0.20 MB DOC)
We are grateful to the significant input from other CCD workgroup members, especially David Biddinger, Diana Cox-Foster and Jerry Hayes.