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

skegley@pesticideresearch.com

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