Pesticide Impacts on Bees: Using the PUR data to provide clues to
the role of pesticides in Colony Collapse Disorder
Susan E. Kegley, PhD, Joshua R. Pepper Pesticide Research Institute
Overview
• The role of bees in our food system • Colony Collapse Disorder (CCD) • Pesticides toxic to bees • Trends in pesticide use over time • Recent research on CCD and pesticides
Not Just Honey
Globally, pollination services estimated at $216 billion dollars in 2008. In U.S., $15B.
Insect Pollinators Are Responsible for Every Third Bite of Food—$15B Worth in U.S.
Not Just Honeybees: 4,000 species of Native Bees
Leafcutter bee Halictid bee Bumblebee
Orchard Mason bee
How the Hive Works: Social Structure
• Queen bee (1) • Worker bees (female,
5–60,000) • Drones (male, ~15%)
How the Hive Works: Life Cycle
Colony Collapse Disorder
• Rapid loss of adult bees, but brood (and sometimes queen) still present
• No dead bees near the hive • Food stores untouched by “robber” bees or other scavengers • Major overwintering losses in 2006-2007, and continuing • Shortened queen lifespan
Possible Causes of CCD Under Consideration
• Hive pathogens: Viruses, bacteria, microsporidia
• Hive parasites: Varroa mites, tracheal mites, small hive beetle, wax moth
• Pesticides • Habitat degradation • GMO crops • Some combination of the above
Possible Causes of CCD Under Consideration
• Hive pathogens: Viruses, bacteria, microsporidia
• Hive parasites: Varroa mites, tracheal mites, small hive beetle, wax moth
• Pesticides • Habitat degradation • GMO crops • Some combination of the above
Pesticides Toxic to Bees
Organophosphorus compounds
N-Methyl Carbamates
Spinosyns
Neonicotinoids
Thiacloprid LD50 = 14.6 µg/bee
Nicotine
Imidacloprid LD50 = 0.0179 µg/bee Clothianidin
LD50 = 0.0218 µg/bee
Neonicotinoids
Thiamethoxam LD50 = 0.0299 µg/bee
Acetamiprid LD50 = 7.07 µg/bee
Nitenpyram LD50 = 0.138 µg/bee
Dinotefuran LD50 = 0.075 µg/bee
Chlorothalonil
Fungicides Too?
• Some neonictinoids in combination with certain fungicides synergized to increase the toxicity of the neonicotinoid to honey bees by over 1,000 fold (Iwasa et al., 2004).
Boscalid
Triflumizole
Neonicotinoids: Effects on Bees
• Highly acutely toxic: LD50 < 0.01 µg/bee • Sublethal effects
– Impairment of immune function – Impairment of learning and memory – Hive dwindling and loss
Neonicotinoids: Exposure
• Water soluble • Persistent in the environment,
t1/2 ~ 1–3 yrs • Many opportunities for exposure
Direct Sprays Kill Bees
Dust from Seed Drilling Exhaust
Christian Krupke et al. “Multiple routes of pesticide exposure for honey bees near agricultural fields,” PLoS One, 7(1):e29268 (January 2012)
Pesticides in Nectar and Pollen
• From seed treatments Nectar: 3.6-11.4 ppm; Pollen: 2–3 ppb
Water Contamination
Contaminated guttation water: 10–200 mg/L
Contaminated surface waters in CA: 89% detects, 19% > Aquatic Life Benchmark
Starner and Goh, 2012. “Detections of the Neonicotinoid Insecticide Imidacloprid in Surface Waters of Three Agricultural Regions of California, USA, 2010–2011,” Bull Envi Contam Toxicol 88:316-321.
Bee-to-Bee Transmission of Contaminated Food and Water
• Trophallaxis: Mouth-to-mouth food exchange between bees
• Larvae exposed through royal jelly
In-Hive Miticides
• Varroa mite control
Amitraz
Coumaphos
Fenvalerate
Insecticide Use in California by Chemical Class
OP Insecticide Use in California
Carbamate Insecticide Use in California
Systemic Insecticide Use in California
Pyrethroid Insecticide Use in California
PRI’s Bee Resource Center www.pesticideresearch.com
Herbicides?
Consumer Use Contributes
Sales vs. Use for Imidacloprid
How Pesticide Use Reporting Could Be Improved to Help Pollinators
• Require reporting of plantings of treated seeds – Acres planted – Seed brand used that DPR could back-calculate
application rate per acre
Thiamethoxam Impairs Homing Ability
• Bees dosed with low levels of thiamethoxam in food via syringe
• Control bees not dosed
• Exposed bees were 2-3 times more likely to not return from foraging than unexposed bees
Mickael Henry, et al. “A Common Pesticide Decreases Foraging Success and Survival in Honey Bees,” Science Express, March 29, 2012 (UR406 Abeilles et Environnement, Avingnon, France)
Ability to Navigate to the Hive Impaired by Thiamethoxam
A: Bees released in areas they had foraged in before. B: Bees released in unfamiliar areas.
Harvard Imidacloprid Study (Released 4/5/12)
• Hypothesis: Imidacloprid is causing CCD • Experiment: 16 hives dosed with varying levels of
imidacloprid in 16 hives, with 4 control hives – After 12 weeks, all hives still alive – After 23 weeks, 15/16 dosed hives had died, with
symptoms of CCD – Those exposed to the highest concentrations of
imidacloprid died first – Doses used were lower than those resulting from typical
pesticide use that still caused CCD • Exposure source in managed bees: High-fructose
corn syrup? Beekeepers beg to differ.
Chensheng Lu, et al., “In Situ Replication of Honey Bee Colony Collapse Disorder,” Bulletin of Insectology, June 2012. (Harvard School of Public Health)
Analysis of Hive Components
• Varroa mite load • Viruses, bacteria • Pesticides
Pesticides in Pollen: M. Frazier, 2007 108 samples
Detection limits too high to see most neonicotinoids
Pesticides in Pollen: M. Frazier, 2007 108 samples
Pesticides in Pollen: J. Frazier, 2011 503 samples
Evaluation of Multiple Risk Factors
• Analysis of pollen, wax, parasites, pathogens, pesticide residues, protein content, genetic lineage, morphological measurements
• Statistical analysis of 61 variables – No single factor could account for CCD – Classification and Regression Tree Analysis (CART)
indicated that six of the 19 variables having the greatest discriminatory value were pesticide levels in different hive matrices
• Coumaphos had highest discriminatory value and was highest in healthy colonies
• Varroa control? • Bees selected for resistance?
Van Englesdorp, et al. 2009. “Colony Collapse Disorder: A Descriptive Study,” PLoS One, 4(8):1–17. (Penn State, Entomology, Agriculture, Veterinary School)
Colony Collapse Disorder
• Higher virus loads in CCD colonies • Higher incidence of co-infected
microsporidian/virus in CCD hives • Premature foraging behavior because of loss of
adult bees
Honeybee Pathogens
• Viruses – Israeli acute paralysis virus – Chronic paralysis virus – Deformed wing virus
• Microsporidia – Nosema sp.
• Bacteria – Foulbrood, chalkbrood
Varroa Mite: Arrived in U.S. in 1987