A (Technical) Overview of Pesticides and their Exposure Effects
Pesticides (insecticides, herbicides and fungicides) are chemicals used for pest control in residential and commercial environments. Not all pesticides kill bees instantly, and many have delayed sub-lethal effects that appear when a critical threshold is reached. Broadly, the effects of pesticides are based on their impact on brood, adult bees, or both life stages. These chemicals may be deliberately introduced into the hive in the form of miticides, but most are accidental environmental exposures.
This article outlines the types of pesticides encountered by bees in a commercial setting, and examines the fipronil baiting operations for control of Varroa mites in Australia. The article concludes with a technical analysis on the current insecticide chemical classes available for pest control.
There’s a shirt that goes with this article, designed & printed by yours truly:
Bees and Pesticides in Commercial Pollination Settings
The Effects of Pesticides on Honey Bee Mortality
Pesticide toxicity is not created equal. Bees exposed to multiple chemicals often result in multiplicative, systemic effects as a result of this chronic exposure. Some pesticides do not harm the foraging adult bee. However as the bee returns her collected pollen and nectar to the hive, the chemical residues can spread to the queen and nurse bees, who then pass onto the brood.
If enough honey bees forage on affected crops, the entire colony can show signs of pesticide poisoning, depending on the chemical used. This rapid dispersal is a consequence of natural social insect behaviours. Bees engage in trophallaxis (feeding other bees and larvae by regurgitating liquids) and allogrooming (grooming one another) – this direct contact leads to an exponential dispersal of the pesticide at the colony level.
Studies have shown that pesticide exposure has been linked to honey bee mortality. Poisoning manifests through the appearance of dead bees at the hive entrance. Different formulations and application methods influence the duration of colony survival, with the general trend showing that many commercial products are indeed pesticides that kill bees. Other types of harm can come indirectly from the indiscriminate application of herbicides and fungicides on bees during flowering periods.
What the figures don’t always show is that sub-lethal effects like impaired navigation and reduced foraging capabilities (which are not as oblivious as “dead bees”) impair colony performance and could collapse one when an additional stressor (e.g. disease) is introduced.
Pesticide Exposure and Solitary Bees
Ongoing research demonstrates that honey bee colony survival is critical to preserving world food production. Another issue is off-target effects from pesticide exposure, which impact many species of beneficial insects. Unfortunately, the vast majority of cases go unnoticed or underrepresented due to the difficulty in identifying and tracking solitary species year on year (O’Connor et al., 2019).
Like honey bees, solitary bees collect pollen and nectar for their nests. As the larvae hatch and begin to feed, they develop pesticide poisoning symptoms that could lead to death or impaired growth. Research on the impacts of pesticide exposure on solitary bee species is limited due the difficulties in replicating natural nesting conditions, and ability to obtain a suitable number of individual bees for study (Sgolastra et al., 2018).
Multiple Pesticide Exposure and the Risk of Synergy
Synergism occurs when the combined effects of two pesticides is greater than the sum of their individual effects. Assessing synergistic risk is complex and depends on factors like application methods, timing and concentrations. While two pesticides may be marked safe for standalone use, their combination could lead to unknown, harmful effects. Multi-exposure scenarios occur when bees forage on crops treated with different pesticides, irrespective of the application method.
How Pesticide Application Methods Affect Different Bee Species
A 2016 study by Sgolastra et al., showed that co-application of an ergosterol biosynthesis inhibitor fungicide (propiconazole) with a neonicotinoid (clothianidin) lead to lethal outcomes in three bee species. In commercial pollination settings, these pesticides are applied on sunflowers, canola and various fruit trees. As bees were exposed to contaminated pollen and nectar, they were found to be more susceptible to the neonicotinoid1. Other studies have also confirmed that honey bees exposed to pyrethroid insecticides mixed with ergosterol biosynthesis inhibitors were significantly more toxic to bees (Schmuck et al., 2003).
The degree of pesticide toxicity depends on the lifestyle of the bee species. The individual bees in social species like Apis mellifera and Bombus terrestris are not as vulnerable to chemical exposure as they buffer their effects at the colony level, termed “superorganism resilience”2 (Straub et al., 2015). An analysis of bees foraging on clothianidin-coated canola, showed negative effects on wild bee nesting and B. terrestris colony growth, but no significant effects on the development of A. mellifera colonies (Rundlöf et al., 2015).
Fipronil Baiting for Varroa Mite Control
Australia is currently the only continent free from (widespread) Varroa mites. In June 2022, Varroa destructor was detected in surveillance hives within the state of New South Wales, and a taskforce was established by government and honey bee industry bodies to prevent its spread within the country.
One feature of the biosecurity order is the complete removal of wild honey bee colonies within affected areas. The euthanasia program uses fipronil bait stations the at identified “red zones”, a 10 kilometer radius around each premises where Varroa was detected.
How Fipronil Bait Stations Prevent the Spread of Varroa
Fipronoil belongs to the family of insecticides that target the central nervous system, leading to death as a result of nerve over-stimulation (technical aspects covered below). In the open environment, the chemical half-life is 12 hours in water and 3.7 days in clay soil. The pesticide baiting stations are designed to minimise off-target exposure, and prevent contamination of soil and water.
Sugar syrup feeding station are setup a certain distance away from one another within the red zones. These stations are monitored by a trained operator, who upon observing a sufficient number of honey bees foraging from the syrup, add fipronil to the solution. The fipronil concentrations within this bait syrup are low dose, enabling the worker bees to return their forage back to hive. The fipronil is then mixed into larval diets and shared with other bees via trophallaxis, rapidly spreading the pesticide within the colony and killing it completely.
Drawbacks of this method include the fipronil residues remaining inside dead honey bee hives for up to three years. Feral colonies typically nest in trees, and as a result there is a high probability that native bee species, reptiles, birds and mammals may visit these empty nests and collect contaminated honey. These off-target effects lead to an accumulation and spread of fipronil into the ecosystem, as shown during the eradication attempts of the invasive Asian honey bee colonies in Queensland (Koetz 2013).
How Fipronil Baiting of Feral European Honey Bee Colonies Works
As of February 2024, the NSW government has transitioned to management rather than eradication. Living with Varroa from here on!
Feeder stations consists of various concentrations of sugar syrup depending on the weather and the bees’ needs. To further its appeal as foraging source, propolis, irradiated honey and wax comb are added . The box is then heated to disperse the aroma and encourage scout bee recruitment.
Once the operator counts over 300 honey bees visiting the feeding station, a fipronil spike is added to make a final solution of 0.01 g/L. Over 600 feeder stations have been deployed in the red zones, of which there were 550 fipronil administrations (i.e. there was sufficient bee recruitment in over 550 stations to warrant fipronil application). The dosage used for honey bee control is far lower than what is used in home and garden products; 0.01 g/L, compared to 100 g/L in pet flea treatments.
The social native bee species, Tetragonula carbonaria, has not been detected at feeding stations. This stingless bee species shows no interest in collecting honey from dead honey bee colonies. As wild A. mellifera bees are eradicated more forage becomes for T. carbonaria & other native insects.
Which Pesticides are Commonly Used in Domestic & Agricultural Settings?
Non-technical readers are welcome to skip this section.
There are hundreds of pesticides avaliable on the market, used according to the need and intended target. Broadly, they are split into four major classes:
Pesticides that target the central nervous system
Pesticides that target the muscular system
Growth & development inhibitors
Non-specific disruptions of normal function (e.g. energy generation, exoskeleton)
Pesticides Targeting Insect Nervous Systems
This is the most common class of pesticides, aimed at manipulating acetylcholine (ACh) concentrations or disrupting the interaction between sodium and chloride channels. They achieve lethality by stimulating, inhibiting prolonging or removing the drug target from the insects’ nerve cells.
Pesticides Targeting Sodium Ion Channels
Pyrethrins and Pyrethroids have been used for over a hundred years as compounds derived from pyrethrum, a chrysanthemum flower extract. As a result, they have been approved for use in organic farming methods, with example compounds including allethrin, resmethrin, and tetramethrin, however these organic pesticides can still affect bees.
Pyrethrins and Pyrethroids bind to the voltage-gated sodium channels on nerve axons, preventing them from closing. As a result, the insect experiences rapid tremors and convulsions, leading to death. This class is indiscriminate, and pyrethrin pesticide use has been shown to harm pollinators and other beneficial insects.
Another sodium channel-targeting class is oxadizine, which works by blocking the sodium ion flow into nerve cells. Oxadizines contain the prodrug (or pro-insectiside) indoxacarb, whichis activated by the hydrolysis of its ester bonds by the insect’s carboxyelsterase enzymes. The resulting compound has a high affinity for sodium ion channels, which causes the blockage that leads to paralysis and eventual death.
Semicarbazones act in a similar manner to to indoxacarb, as the active ingredient metaflumizone binds to sodium channels and thus prevents ion movement into the nerve cells.
Pesticides Targeting the Acetylcholine System
Once a widely used class of pesticide, they have heavily regulated due to the human health concerns and relatively high degree of mammalian toxicity. Two such chemical classes are carbamates and organophosphates, which inhibit acetylcholinesterase (AChE) enzyme function. The result is insect death via overstimulation, due to the prolonged presence of ACh in the post-synaptic nerve terminal. The similarities of ACh systems between insects and mammals makes carbamates and organophosphates non-selective in their actions, leading to significant off-target effects in humans, leading to their eventual withdrawal.
Although no longer commonly used, examples of organophosphates include Malathion, Chlorphyrifos (once widely used on corn and soybeans), and Diazinon (previously used on turf and home gardens). Likewise, Carbamates like Carbaryl, Adldicarb & Carbofuran are rarely used to due extreme off-target toxicity.
Organophosphates bind to AChE through phosphorylation of the AChE active site, altering its configuration and inhibiting ACh binding. Carbamates act in a similar matter by conudcitng cabamylation that inhibts ACh binding. The key difference in these two processes is that the effects of cabamylation can be reversed over time by removing the carbamate.
Neonicotinoids are synthetic materials modelled after the natural plant-based pesticide nicotine, neonicotinoids (eg thiamethoxam, clothianidin & acetamiprid) also prolong the presence of ACh in the post synaptic nerve terminal by binding to the ACh molecules themselves, resulting in insect death from nerve hyperstimulation. This class of pesticides has been implicated in colony collapse disorder & the “disappearing bees” phenomenon.
Spinosyns are produced by the fermentation of Saccharopolyspora spinosa, a soil bacterium. These pesticides work in a similar manner to neonictinoids by binding to the ACh receptor and prolonging ACh excitation. Other mechanisms have also been detected, such as blockage of the gamma amino butyric acid (GABA) receptor.
Pesticides Targeting Chloride Ion Channels
The chemical class phenylpyrazole includes the active ingredient fipronil, which has been covered above as part of the feral honey bee hive baiting operations for Varroa mite control. Fipronil exhibits non-competitive inhibition of the GABA receptor, altering the GABA neurotransmitter binding site, and preventing GABA from binding and opening the neuronal chloride channel. The lack of chloride ions leads to death by hyperexcitation in a similar manner to pyrethrin-treated targets.
Another chemical class is the Avermectins, including abamectin and ivermectin. These bind to glutamate-gated chloride channels, stimulating them to release an unimpeded chloride flow into cells, leading to nerve cell inactivation and disabiling neurological function. They are predominately used in internal human and veterinary medicines.
Pesticides Targeting Calcium Channels
Diamides contain active ingredients like flubendiamide and chlorantraniliprole. They act on the calcium ion channels and stimulate muscular contractions. Diamaides bind to to the ryanodine receptors (RyRs) in the endoplasmic reticulum, causing them to remain open and flush the muscle cells with calcium, leading to contractile paralysis and death.
What Makes Insect Growth Regulators Effective?
Insect growth regulators (IGR) prevent the normal, adult development of their target species. The specific modes of actions makes them popular in integrated pest management approaches, as they have less harmful off-target effects.
IGRs are one of the most common pesticides encountered by honey bees. Some regions apply them to almond trees during blooms as they exhibit low lethality to the adult bees. However, these foraging bees exposed to pesticides, can carry contaminated pollen and nectar back to the hive. The resulting hive-wide exposure spreads to the hive occupants, potentially contaminating larvae and placing pesticides in honey combs (Mullin et al., 2016)
Juvenile Hormone Analogs & Ecdysone Agonists
These molecules alter the hormone levels inside insects. Juvenile hormone analogs (JHAs) like methoprene and fenoxycarb extend the juvenile stage, preventing their maturation into adults by binding to hormonal receptors and mimicking the natural juvenile hormone. This tricks the insect’s body into maintaining the juvenile stage, even when it is time for it to metamorphose into an adult. As a result insect development and reproductive physiology is altered, resulting in death or sterilization.
Ecdysone agonists such as tebufenozide and methoxyfenozide mimic the actions of the molting hormone ecdysone, resulting in premature molting. The emerging adult insects are premature, which result in a reduced lifespan and reproductive capacity.
Chitin Synthesis Inhibitors
Arthropods have exoskeletons constructed from chitin. Chitin Synthesis Inhibitors (CSIs) work by disrupting the actions of chitin synthase, the enzyme responsible for chitin synthesis. A lack of chitin has fatal outcomes, and chemicals such as noviflumuron and lufenuron have been specifically developed for termite and flea control respectively.
Like JHAs, CSIs are often applied to blooming crops, but this action is discouraged where insect pollinators are involved due as the foraging bees return this contaminated pollen and nectar back to the hive, leading to toxic effects on the developing larvae.
Pesticides with Non-Specific Cellular Disruption
Certain chemicals are design to disrupt mitochondrial functions, causing cell death from energy imbalances. These chemical classes include Pyrroles, Amidinohydrazone, Borates and Fumigiants. Pyrroles can be used to protect stored grains against weeviles, while amidinohydrazones are not commonly used in agricultural settings. Borates are not commonly used in agriculture due to the fact that boron, while necessary for the plants’ growth, can be toxic to plants in high concentrations, and can harm the crops themselves.
Fumigants are volatile gases used in greenhouses and soil to control a wide variety of pests including insects, nematodes, fungi, and rodents. The gaseous nature of these chemicals make them a last-resort pest control technique, as exposure carries a large risk of toxicity to humans and non-target organisms.
Desiccating Chemicals for Pest Control
The last group of pesticides are compounds that absorb the thin wax layers on insect exoskeletons, increasing permeability and water loss to cause death by dehydration. Synthetic desiccating chemicals include silica gels, whereas diatomaceous earth3 is a natural alternative. Both compounds contain silicon dioxide, and their direct contact is effective against crawling insects.
The Pros and Cons of Pesticide Use
Unwanted pests greatly impair crop production. There is a need to balance between pest control and the preservation of wildlife species. This article covered the insecticides that honey bees may encounter in the field during commercial pollination operations. Their mechanisms of action, chemical classes and biological effects were examined, using the ongoing fipronil baiting operations in Australia as an example.
In the real world, chemical synergy as a result of multiple pesticide exposure poses an unknown risk to honey bee health. Emerging evidence shows that while two chemicals are deemed safe individually, the risk of harmful effects increases following combination exposure, as seen in field tests. Also in the real world are interactions with weather, pests, disease and nutrition, which may exacerbate an otherwise-manageable exposure.
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Footnotes
- This increased susceptibility to clothianidin is thought to be due to the fungicide’s inhibition of bee detoxification enzymes (P450 family). Further reading on neonicotinoids is available on the effects of Neonicotinoids on Bees.. ↩︎
- Superorganism resilience the ability of the colony as a whole to withstand and recover from stressors or disturbances. Individual honey bee colonies operate as a unified entity; individual bees cannot survival or reproduce on their own, and the success of the colony depend on the cooperation and coordination of all its members.
For example, if a large number of forager bees die due to pesticide exposure, the colony can adjust by promoting younger bees to start foraging earlier than they normally would. The colony adjusts its behaviour to deal with the loss and continue maintaining essential functions. Further reading can be found here ↩︎ - Diatomaceous earth refers to the fossilised remains of diatoms (microscopic algae) and is used in controlling small hive beetles within honey bee hives. Hive bottom boards or inter-frame beetle traps can be filled with the substance, with the beetles killed upon contact. The application method selected by beekeepers matters, in order to protect bees from being impacted by diatomaceous earth. ↩︎