Pesticides and Honey Bees
Eric Mussen
Extension Apiculturist
Entomology and Nematology
UC Davis
Contributions Honey Bees to
California Commercial Agriculture
• Honey bees are rented to pollinate nearly 100
crops in California
▫ Fruit, vegetable, nut and forage seed crops
▫ The farm gate value exceeds $6 billion, directly
▫ Beekeepers generate about $150 million from
rentals
• Honey bee-pollinated crops make up about 1/3 of
the normal U.S. diet
Contributions Honey Bees to
California Commercial Agriculture
• California beekeepers produced around 12 million
pounds of honey in 2013, worth $23 million
▫ 240,000 pounds of beeswax, a byproduct, was worth
around $1 million
• California beekeepers produce nearly 1 million
queen bees, packaged bees, and nucs worth
around $25 million
• We are having a hard time keeping our colonies
alive
▫ No single cause, just too many sublethal stresses
Major Topics to be Covered
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Definition of “Pesticide”
Pesticide Modes of Action
Determining Toxicity of Pesticides to Honey Bees
Detoxification of Pesticides
Pesticide Residues in Beehives
Exposure of Honey Bees to Pesticides
Avoiding Pesticide Exposure
Definition of “Pesticide”
• According to the U.S. Environmental Protection
Agency (EPA): “A pesticide is any substance or
mixture of substances intended for preventing,
destroying, repelling or mitigating any pest.”
• According to the California Department of Pesticide
Regulation (DPR): “Any substance or product that
the user intends to be used for pesticidal poison
purposes.”
Definition of “Pesticide”
• California regulations also cover disinfectants,
repellents, wood preservatives, pheromones,
attractants, and plant growth regulators
• Any word ending in “-cide” means kill:
▫ Insecticide, herbicide, homicide, genocide
Modes of Action
(How Pesticides Kill)
• Pesticides are chosen or designed to interfere with
metabolism:
▫ The sum of the chemical reactions that take place
within each cell of a living organism and that provide
energy for vital processes and for synthesizing new
organic material
• Animals, plants, fungi, and bacteria rely on their
metabolism to live
Metabolic Pathways of Live Organisms
Metabolic Pathways of Live Organisms
Sites of Biochemical Interference
chemistrypictures.org
Sites of Biochemical Interference
en.wikpedia.org
Classifications of Pesticides
• By type (target pests)
▫ Algicides, antifouling agents, antimicrobials,
attractants, biopesticides, biocides, defoliants,
desiccants, disinfectants and sanitizers, fungicides,
fumigants, herbicides, insecticides, insect growth
regulators, miticides, microbial pesticides, molluscicides, nematicides, ovicides, pheromones, plant
growth regulators, repellents, and rodenticides
Classification of Insecticides
• By mode of action
▫ Group 1A – acetylcholine esterase inhibitors
 Carbamates: carbaryl (Sevin®), carbofuran (Furadan®)
(of 25) [atropine antidote]
▫ Group 1B – acetylcholine esterase inhibitors
 Organophosphates – chlorpyrifos (Lorsban®),
malathion, parathion (of 64)
▫ Group 2A – GABA-gated chloride channel
antagonists – chlordane, lindane, endosulfan
Classification of Insecticides
• By mode of action
▫ Group 2B – GABA-gated chloride channel
antagonists – fipronil (Maxforce® cockroach and ant
baits; Frontline Flea and Tick Control®)
▫ Group 3 – sodium channel modulators – DDT and
methoxychlor – Pyrethrins and pyrethroids: Pyganic®
(organic sprays), esfenvalerate (Asana®), fluvalinate
(Apistan®), permethrin (bug-repellent clothing)
Classification of Insecticides
• By mode of action
▫ Group 4A – nicotinic acetylcholine receptor
agonists/antagonists – imidacloprid, clothianidin,
thiamethoxam and dinotefuran are “nitro-substituted”
and much more toxic to honey bees than the “cyanosubstituted” acetamiprid and thiacloprid
 Muscarinic and nicotinic acetylcholine receptors
 Vertebrates and invertebrates
▫ Group 4B – nicotinic acetylcholine receptor
agonists/antagonists – nicotine
Other Classifications
• Fungicides and herbicides have similar sets of
information, including their resistance groups
• Fungicides and herbicides have similar modes of
action to insecticides, but targeting the biochemistries of fungi and plants
▫ The overlap in metabolic pathways is considerable
Measuring Toxicity to Honey Bees
• Adult worker LD50 (lethal dose 50 percent)
▫ Topical
▫ Oral
• Adult worker LC50 (lethal concentration)
▫ In environment
• LD50s and LC50s not usually determined for larval
or pupal honey bees
• Impacts of chronic sublethal doses on eventual
adult longevity not determined, either
Considering Synergisms
• Textbook definition of synergism
▫ The interaction of things resulting in the overall
effect that is greater than the sum of individual
effects of any of them.
• Example of good synergism: mixed pollen diets
better for honey bees than any pollen alone
Considering Synergisms
• Examples of synergisms harmful to honey bees:
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Fluvalinate and coumaphos (more toxic effects)
Fluvalinate and chlorothalonil (more toxic effects)
Coumaphos and chlorpyrifos (more toxic effects)
Chlorothalonil plus chlorpyrifos, then either fluvalinate
or coumaphos = no observable differences from
controls
▫ Imidacloprid and Nosema ceranae
 Intestinal parasite proliferates worse than normal
▫ Chlorothalonil and Nosema ceranae
 Intestinal parasite proliferates worse than normal
Considering Synergisms
• Fresno to Bakersfield – March 2014
▫ Beekeepers’ estimate = 80-87,000 colonies affected
▫ DPR’s estimate = “only 10,000 could be verified”
• Combination:
▫ Tilt fungicide – no known problems with honey bees
▫ Tourismo insecticide – supposed to be safe for bees
 EPA data sheet lists “Acceptable” where we expect to
see LD50s
▫ Adjuvant (?) – now, mostly “penetrants”
Considering Synergism
• Advertising claim of one penetrant manufacturer
▫ “Even moves chemicals through the waxy cuticular
layer of Eucalyptus leaves”
• What is the primary protection for an insect to
chemical poisoning?
▫ It’s waxy cuticular layer
Detoxification of Pesticides
• Basic systems to make pesticides water-soluble for
excretion
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Oxidation (loss of hydrogen)
Reduction (gain of hydrogen)
Hydrolysis (reaction with, or addition of water)
Hydration (decomposition reaction with water)
Dehalogenation (elimination of halides)
• Phase I requires cytochrome P450 enzymes
Cytochrome P450s in Honey Bees
• Fewer types of P450 enzymes in honey bee
genome than in mosquitoes or fruit flies
• Fewer replicate genes for each P450 enzyme
compared to mosquitoes and fruit flies
• Piperonyl butoxide (adjuvant) prevents production
of P450 enzymes
• Other, tank-mix agricultural adjuvants just
beginning to get serious attention
▫ Toxicity and ability to convey chemicals across
membranes are important considerations
Detoxification of Pesticides
• Phase II requires many functional enzymes to form
conjugates that can carry the toxins out of the
body:
▫ Sulfation; glucoronidation; glutathione conjugation;
acetylation; amino acid conjugation; or methylation
• Each of these processes also can be targeted to
disrupt an organism
Results of Residue Analyses
• Multi-year studies on residues (USDA/AMS)
▫ Two sources of beehive samples nearly pesticide-free
 Stored honey and immature bees
▫ Three types of samples very apt to have significant
residues associated with them
 Stored pollens
 Beeswax
 Adult bees
▫ So far, residues of about 150 of the 200 parental and
major breakdown products of our agricultural chemicals
have been found
Exposure of Honey Bees to
Pesticides
• Direct hit
▫ Foraging in treated area at time of application
▫ Drift over and into the hives
• Contact with toxic residues
▫ Entering a treated area before toxic residue dries, or
breaks down, on attractive bloom
▫ Foraging water over which pesticide has be applied
or into which pesticide has run (chemigation)
▫ Consuming contaminated pollen (or nectar) brought
back to the hive before the exposed foragers die
 neonics and other systemics
Avoiding Pesticide Exposure
• Try to choose apiary locations away from pesticide
use
▫ Hives sometimes can be covered for short periods
when applications are expected: mosquito
abatement, agricultural fields, orchards, etc.
▫ Encourage necessary applications be made when
pollen and pollen-collecting bees are not going to be
contaminated
 Best advice we can share!
Avoiding Pesticide Exposure
• GET THE WORD OUT!
▫ Right now the world is on the side of the bees
▫ Targeting neighbors, nursery store operators,
hardware store operators, retail store operators,
farmers’ market visitors, greens-keepers, PCA’s,
Farm Advisors, professional and public service
organizations that ALL PESTICIDES have demonstrable physiological effects on honey bees if the
bees come into contact with the materials
Latest Extension Publication on
Honey Bee Toxicity (2013)
• “How to Reduce Bee Poisoning From Pesticides”
▫ Pacific Northwest Extension Publication PNW591
▫ By L. Hooven, R. Sagili, and E. Johansen
▫ Chemicals cross-indexed by active ingredient and by
product name
▫ 34 pages
• May be purchased from Washington State or
Oregon State Universities for $5, plus shipping
▫ Available as free PDF on the Internet
 http://www.orsba.org/htdocs/home.php, then click on
the link to the publication
EPA Residual Times (RT25) Tables
• Time to 25 percent mortality of foragers following
application
▫ Sun exposure, temperature, and humidity all play big
roles
▫ Has to be a range, in hours or days
 over a year for Penncap-M in “bee bread” (stored
pollen)
• Free download on the Internet:
▫ Enter “Residual Time to 25% Bee Mortality (RT25)
Data” in your browser
▫ The direct URL runs on for miles
Speaker Contacts
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Eric Mussen
Extension Apiculturist Emeritus
UC Davis
Phone: 530-752-0472
Email: ecmussen@ucdavis.edu
URL: entomology.ucdavis.edu/Faculty/Eric_C_Mussen/