Modern pesticides damage the nervous system of honeybees

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The challenge to let people walk back and forth in a straight line isn’t just used by police to test if drivers are intoxicated: it’s also used by neurologists to diagnose neurological disorders like ataxia, where parts of the brain that coordinate movement are impaired.

Now, researchers use an insect version of this challenge to show for the first time that modern pesticides damage the nervous system of honeybees so that it becomes hard for them to walk in a straight line.

The results are published in Frontiers in Insect Science.

“Here we show that commonly used insecticides like sulfoxaflor and the neonicotinoid imidacloprid can profoundly impair the visually guided behavior of honeybees.

“Our results are reason for concern because the ability of bees to respond appropriately to visual information is crucial for their flight and navigation, and thus their survival,” said lead author Dr Rachel H Parkinson, currently a scientist at the University of Oxford.

The results add to what the Food and Agriculture Organization of the United Nations and the World Health Organization have called the “rapidly growing body of evidence [which] strongly suggests that the existing levels of environmental contamination [from neonicotinoid pesticides] are causing large-scale adverse effects on bees and other beneficial insects”.

Optomotor response keeps insects in line

Insects have an innate ‘optomotor response’, which lets them orient themselves back onto a straight trajectory when they threaten to steer off-course while walking or flying. Parkinson and colleagues challenged the optomotor response of walking honeybees to respond accurately and timely to videos of vertical bars that moved from left to right, or vice versa, across two screens in front of them.

This ‘tricks’ the bee into assuming that she has suddenly been blown off-course and needs to perform a corrective turn to return to a straight path. A healthy optomotor response will then instruct the bee’s motor system to orient back to an illusory straight line mid-way between the optic flow from right and left.

The researchers compared the efficiency of the optomotor response between four groups of wild-caught forager honeybees, with between 22 and 28 bees tested per group: each had been allowed to drink unlimited 1.5 molar sucrose solution over five days, either pure or contaminated with 50 ppb (parts per billion) imidacloprid, 50 ppb sulfoxaflor, or 25 ppb imidacloprid and 25 ppb sulfoxaflor simultaneously.

Optomotor response worse after exposure to pesticides

All bees were less good at responding to the simulated optic flow when the bars were narrow or moving slowly (ie, seemingly far away) than when they were wide or moving fast (ie, seemingly close by).

But for any width and speed, the bees who had ingested the pesticides performed poorly compared to control bees.

For example, they turned quickly in one direction only and didn’t respond to changes in the direction of movement of the bars, or showed a lack of turning responses.

The asymmetry between left and right turns was at least 2.4 times greater for pesticide-exposed bees than for control bees.

Minor brain damage

The researchers also show with molecular techniques that pesticide-exposed bees tended to have elevated proportion of dead cells in parts of the brain’s optic lobes, important for processing visual input.

Likewise, key genes for detoxification were dysregulated after exposure. But these changes were relatively weak and highly variable across bees, and unlikely to be the sole explanation for the observed strong impairment of the optomotor response.

“Neonicotinoid and sulfoximine insecticides activate neurons in the insect brain and are not always recycled fast enough to prevent toxicity.

“The effects we observed could be due to a type of rewiring in the brain: to prevent neural damage by reducing the sensitivity of neurons to these compounds,” said Parkinson.

Parkinson looked ahead: “To fully understand the risk of these insecticides to bees, we need to explore whether the effects we observed in walking bees occur in freely flying bees as well.

“The major concern is that – if bees are unable to overcome any impairment while flying – there could be profound negative effects on their ability to forage, navigate, and pollinate wildflowers and crops.”

Original Research: The findings will appear in Frontiers in Insect Science


The Significance of Bees to Humans as an Economically Important Species

Apiculture requires minimal investment, often occurs without land ownership, and generates various products for later sale [6]. Bees are therefore an economically important species. The long-term survival of farming and agriculture around the world depends on insect pollination. This is connected with huge amounts of money reaching hundreds of billions of dollars a year [7].

It is increasingly known that pollination also affects the nutritional value of food. The lack of macronutrients and numerous essential micronutrients cause specific conditions of nutrient deficiency, as well as greatly increase mortality from other diseases or weaken the immune system and the development of stunts [8].

Bees have a strong influence on ecological aspects, the preservation and stability of the ecosystem, biodiversity, and the genetic variation in the plant community. They play a significant role in most terrestrial ecosystems where the green vegetation lasts for at least 3 months a year. In tropical forests, savannah, and mangroves, many plants and animals would not survive without the existence of bees. This is as bees are the main pollinators, and have a significant influence on the production of seeds and fruits. In cultivated areas, bees are needed to pollinate many crops and to preserve biodiversity on non-cultivated areas. Other animals are associated with bees by eating honey, pollen, or wax, being parasitic for the bees, or living in the bees’ nest [9].

International transport of the honey bee by humans has led to its current cosmopolitan spread, which spans all continents except some oceanic islands and Antarctica. Having such an advanced level of knowledge about this species, it seems unforeseen that the role of bee as a pollinator in natural habitats is still poorly understood [10]. It was also found that the number of managed honey bees, A. mellifera, and wild bees is equally important in describing the results of open pollination [11].

Precise predictions of pollination performance require a thorough understanding of the interactions between plants and flower visitors [12]. It is known that at least 75% of the 115 leading crop species benefit from animal pollination [13]. A decrease in bee pollination service could potentially reduce yields by approximately 40% [6].

However, populations of wild and managed pollinators are declining. Research conducted in western Europe also showed unprecedented dismutation in both biomass and biodiversity of wild pollinators among many taxonomic groups. For this reason, many European countries have decided to develop pollinator maintenance strategies in the context of the European Initiative and Willing on Pollinators. The approach to pollinator maintenance differs between European countries, and the focus of the conservation strategy varies from country to country, e.g., in Belgium the initiative is dedicated exclusively to honey bees, and in France to all pollinators [14].

Products of Bee Origin—Effect on Human Health, Its Various Applications, and a Source of Chemical Contaminants
Honey is a sweet food product produced by honey bees by processing the flower nectar of plants, as well as some secretions found on tree leaves. Honey is used to treat throat infections, hiccups, dizziness, bronchial asthma, worm infection, tuberculosis, and as a nutritious supplement. It is also used for wounds in traditional medicine [15].

Raw honey can have a positive impact on oral well-being and dental health due to its antibacterial activities that work against both Gram positive and Gram negative bacteria [16]. Honey ingredients have anti-inflammatory [17] and antiproliferative properties [18]. Due to this, honey has the potential to treat many diseases and ailments such as diabetes [19].

Additionally, the two main biologically active ingredients of honey are flavonoids and polyphenols, which are known for their antioxidant abilities [20]. Hydrogen peroxide is produced enzymatically and is an important factor in honey’s antibacterial activity. This compound is produced due to the glucose oxidase, which occurs naturally in honey and is active only after dilution. Glucose oxidase is inactive at low pH of honey, which is caused by the presence of organic acids (e.g., glucuronic acid) [21]. Another property of honey is its antifungal activity associated with the presence of methylglyoxal, glucose oxidase, and high sugar content [22].

Bee pollen is a bee product that has a positive effect on human health [23]. It is a mixture of honey bee secretions, nectar and plant pollen pellets. Bees use bee pollen in order to make bee bread. It contains such nutritional components as proteins, minerals, vitamins, polyphenols, and carbohydrates [24]. Bee pollen contains phytosterols phospholipids and unsaturated fatty acids due to which it exhibits hypoglycemic activity [25]. Flavonoids, polyphenols, and phenolic acids contained in bee pollen play an important role in preventing toxication and protecting the liver from toxins.

The high content of omega fatty acids and essential amino acids strengthens the immune system, helps fight bacteria, and stimulates tissue repair [26]. Bee pollen also has anticancer activity due to the high content of biochemical components such as carotenoids and phenolics [27]. Bee pollen helps with malnutrition, which can often contribute to the deterioration of protein metabolism, digestive tract alterations, and immunological abnormalities [28]. It also has a positive effect on the skin by reducing water loss and influencing the lipid barrier. Bee pollen is also used to treat skin burns due to the high content of biologically active substances [29].

Propolis is a natural mixture produced by honey bees from substances collected from plants. Due to its mechanical properties and waxy nature, bees use propolis to build hives and provide thermal isolation by sealing cracks. In nature, it is hard and lipophilic, however, when heated, it becomes soft, sticky, and gummy [30]. Propolis has a positive effect on the immune system and exhibits many beneficial properties due to the content of bioactive constituents.

The content of compounds varies depending on where the propolis was produced. The molecules contained in propolis include, but are not limited to, esters, flavonoids, amino acids, aldehydes, phenolic acids, vitamins, fatty acids, and minerals [31]. Flavonoid content inhibits formation and attachment of biofilms and metabolism energy of bacteria [32]. These compounds are associated with antibacterial activity of propolis and thus have found their use in the treatment of oral diseases [33]. Flavonoids are also strong antioxidants, able to protect the cell membrane against lipid peroxidation and have a positive effect on oxidative stress [34].

Royal jelly is a mandibular and hypopharyngeal secretion secreted by worker bees. Bees use royal jelly to feed larvae and to help nature the brood. Royal jelly is also food for the queen, and it makes her live longer than the rest of the colony [35]. The composition of royal jelly includes vitamins, proteins, water, carbohydrates, mineral salts, and lipids [36]. It has the potential to treat human diseases due to its antioxidant, antiaging, antitumor, and anti-inflammatory activity [37,38,39].

Due to human activity, trace amounts of toxic molecules can be detected in bee products. Honey and royal jelly can often be contaminated with antibiotics that are used in agriculture to fight harmful pathogens (e.g., chloramphenicol chlortetracycline and doxycycline). Some antibiotics produce hypersensitivity and can also directly trigger toxic reactions and weaken the immune system of the bees and consumers [40].

Pesticides are chemical impurities that can be detected in bee products (especially propolis and pollen) and a lot of them are hazardous. The most common insecticides contaminating bee products include neonicotinoids, organochlorines (e.g., coumaphos and chlorpyrifos), organophosphates, and carbamates [41,42,43,44]. Honey products and bee colonies can be also contaminated by heavy metals contained in air and soil. Examples of such impurities are cadmium, zinc, and copper.

Heavy metals, absorbed above the levels of pollution standards, can also threaten bee and human health [45,46]. Other chemical contaminants, the residues of which may be present in bee products, are polychlorinated biphenyls and polycyclic aromatic hydrocarbons (congomers and mixtures) [47,48,49,50,51,52,53,54].

Knowing this, it can be concluded that bee products, through their chemical contamination, can negatively affect bee and human health, and this is an urgent problem of modern beekeeping. Due to the above, honey can be used as a bioindicator of environmental pollution.

Impact of Pesticides on Living Organisms and the Environment
Pesticides are biological agents or synthesized substances used for killing or restricting the development of organisms [74]. Pesticides include fungicides, herbicides, insecticides, and rodenticides. In animals and humans’ bodies, pesticides are metabolized, stored, excreted, and bioaccumulated in body fat. Pesticides can enter the body through various routes, e.g., inhalation, absorption through damaged skin, or ingestion [75]. Exposure to pesticides can be associated with numerous negative health effects such as dermatological, gastrointestinal, carcinogenic, respiratory, reproductive, and neurological effects. Long-term exposure to pesticides can cause chronic effects on health [76].

For a long time, pesticides have been suspected as one of the main reasons for the decline in bee colonies [77,78]. High-quality seed technologies have led to even greater development of pesticides to protect plants seasonally, which leads to contamination of nectar and pollen. By contact with contaminated plants, bees can be exposed to substances that are harmful to them [79]. The damage pesticides can do to bees includes, but is not limited to, delayed development, impairment of immunity system, and shortening the life span of adults [80]. The honey bee genome contains far less annotated genes than the genomes of other insects. The genome of A. mellifera contains only about 11,000 genes coding for proteins, when the malaria mosquito Anopheles gambia has about 14,000 of them. Honey bees have half as much glutathione-s-transferases (GSTs), carboxyl/cholinesterases (CCEs) and cytochrome P450 monooxygenases (P450s). These enzymes are associated with resistance to insecticides in other species and the shortfall of them may cause pesticides sensitivity in bees. This also affects their susceptibility to pesticide activity, and may weaken their ability to fight virus and bacteria in the future [81]. Immature bees are less likely to be exposed to pesticides as they do not leave the hive. Older bee individuals may come into contact with contaminated pollen or nectar and transfer the impurities to the hive, which is then associated with infecting other individuals. Referring to this, pesticides threaten bees regardless of their age [82]. Queens and other bees are exposed to pesticides by contact with contaminated food and wax. Exposure to pesticides through contaminated wax can negatively affect reproduction of bees, e.g., reduce the number of eggs laid, reduce ovarian weight in queens, or increase queen cell rejection. Pesticide residues can accumulate in the wax for years and may migrate through the brood comb wax, contaminating an even larger area of the hive. Developmental exposure of honey bees to brood combs contaminated with pesticides may appear subtle, but can result in sub-lethal effects that have severe consequences [83].

Honey bees dedicate a large amount of their resources to the production of drones, which help in mating with virgin queens from neighboring colonies during the reproductive season. There are significant differences in the production of viable sperm cells that can fertilize an ovule between sexually mature drones that are exposed to various environmental conditions during their development or as adults. Pesticide contamination of beeswax adversely affects the reproductive quality of drones, which can also affect the queens they mate with, and ultimately weaken the health of the colony [84]. Fungicides and insecticides can also alter insect mobility, navigation, orientation, overall development, and immune function in bees [85].

Exposure to pesticides (e.g., acaricides) may also result in susceptibility to some parasites that threaten the health of the colony [86]. This may be due to pesticide-induced changes in the pathways of the immune system. Exposure to parasites can cause not only the death of certain individuals but also lead to the extinction of the entire colony [87]. The use of pesticides can also affect the bee’s environment. The intensive use of conventional pesticides can reduce the harvest network for bee colonies. These effects are exacerbated by the loss of natural habitat, which can make farms more dependent on pesticide inputs as natural pest control is lost, ultimately reducing pollinator pools [88]. The exposure of bees to pesticides during pollination of flowering crops is associated with both the density of crops in the landscape and the collection of pollen from focal crop. A significant amount of pesticides that create a danger to bee health most likely come from the remains found in pollen from non-focal crops, e.g., wild flowers [89]. This review article focuses on insecticides and their effects on the viability and health of bees. Particular attention was paid to neonicotinoids, fipronil, coumaphos, and chlorpyrifos due to their effect on honey bee health. Additionally, spinosad was discussed as an example of a biopesticide used in agriculture.

Insecticides Present in the Honey Bee Environment and Their Effects

Neonicotinoids Neonicotinoids are a globally used acetylcholine-interfering neurotoxic class of insecticides [90]. Acetylcholine is an excitatory neurotransmitter and endogenous agonist of the cholinergic nervous system. Neonicotinoids act as agonists on the nicotine receptors of acetylcholine (nAChR). In insects, the AchR is predominantly distributed in the neuropil regions of the central nervous system, which is responsible for rapid neurotransmission [91]. Neonicotinoids include compounds such as imidacloprid, thiamethoxam, and clothianidin [92]. Neonicotinoids are used, among others, in urban landscaping, veterinary medicine and to protect crops in agriculture. Neonicotinoids target parasitic sucking insects, soil insects, and crop feeding parasites. In veterinary medicine, they are used to kill fleas on pets [93].

The application of neonicotinoids is varied, but the most common method is to use them as a soil or seed treatment [94]. Neonicotinoids are water-soluble, moderately small molecules. After absorption by the plant, neonicotinoids and their metabolites reach various plant tissues [95]. Neonicotinoids can be found in nectar and pollen collected by pollinators. Neonicotinoids increase the mortality rate of a bee colony and contribute to the reduction in its social immunity [96]. Bees show symptoms of pesticide poisoning including convulsions, uncoordinated movements, and tremors.

This negatively affects the condition of bees, weakening their health and the ability to learn, forage, and remember flower locations [97]. Neonicotinoids have synergistic and additive effects on honey bees, together with stressors such as nosemosis. In addition, some genes responsible for bees’ detoxification, immunity, behavior, and nutrition are up regulated by pollen or pesticide stress. The proper nutrition of bees is of great importance. The combination of exposure to pesticides, along with poor nutrition, can lead to unfavorable effects [98].

Exposing queens to neonicotinoids may result in a reduction in genetic diversity in bee colonies. The influence of neonicotinoids may affect mating of the queen before the formation of a new colony, which has a very negative effect on the health of the entire colony [99]. Bees are more likely to be exposed to neonicotinoids during planting season due to the high concentrations of these pesticides caused by the spread of these chemicals during and after planting [100].

Coumaphos Coumaphos is an organophosphate-based acaricide and a stable lipophilic compound. It is mainly used to control livestock pests and insects including lice, mosquitoes, fleas, ticks, and flies [101]. Coumaphos is an acetylcholinesterase inhibitor that targets cholinergic signaling and covers most excitatory neurotransmission in the nervous system of parasites. It occurs in the form of a crystal with a slightly brownish color and a slight sulfuric odor [102]. Coumaphos is also used to control varroosis in bee colonies in the form of liquid and strips. Coumaphos may negatively affect health of the bee colony.

The low toxicity of coumaphos at least partially depends on rapid detoxification mediated by the P450s. The synergism of coumaphos and, e.g., fluvalinate, causes antagonistic interactions as both compounds are metabolized by P450s. This increases the toxicity of each of these compounds to potentially harmful levels for bees [103]. Drones exposed to coumaphos have reduced body weight and higher mortality. Coumaphos also affects the expression of genes for the detoxification pathways and can lead to a decrease in the level of bee gene products associated with hormonal and cellular immunity. It affects immune responses, physiological and detoxification functions in bees, making them more susceptible to other pesticides and pathogens [104].

Continuous exposure to this pesticide may result in reduced foraging activity and affect the size of hypopharyngeal glands. Coumaphos spreads across the colony mostly by physical contact between the nest partners [105]. Trace concentrations of coumaphos may occur in beeswax, honey, and bee brood. Concentrations of this pesticide can be also determined in beeswax in beehives where coumaphos has not been used, which is probably due to the spread of this pesticide by bees. Coumaphos can accumulate in beeswax for up to 5 years and the larvae exposed to this pesticide are characterized by delayed larval development [106].

Chlorpyrifos Chlorpyrifos is a triphosphorous organophosphate insecticide of wide commercial use. It targets such pests as cockroaches, ticks, and fleas, and has found its application in horticulture, viticulture, forestry, and agriculture. Chlorpyrifos is found in a variety of formations such as wettable and granular powders, micro-encapsulated suspensions, gel-based products, and emulsifiable concentrates [107]. Chlorpyrifos, similar to other organophosphate insecticides upon bioactivation, inhibits acetylcholine in the brain and the peripheral nervous system, causing neurotoxic effects in pests and non-targeted organisms. Inhibition of acetylcholinesterase results in a reduction in acetylcholine degradation and, consequently, overstimulation of associated synapses [108].
Chlorpyrifos also has toxic effects on insects beneficial for the environment, including honey bees, by inhibiting acetylcholine in their nervous system. Under the influence of exposure to chlorpyrifos, adult bees suffer from memory and learning disorders. Chlorpyriphos induces both slowed acquisition and odor generalization in bees of foraging age. Honey bees have difficulty finding their way to the hive and the flowers, which is the reason they are less efficient in collecting food for the colony. Chlorpyrifos increases larval mortality of the colony and can be detected in bee products such as nectar, propolis, wax, and pollen [109]. In addition, sublethal levels of chlorpyrifos interfere with development of the queen, which negatively affects reproduction of bees in the colony [110].

Spinosad Spinosad is an insecticide obtained from actinomycete bacteria Saccharopolyspora spinosa. The fermentation of bacteria produces metabolites that are part of this pesticide. The major components of spinosad are spinosyn A and spinosyn D [111]. It is mainly sold as water-dispersible granules or as a water-based suspension concentrate. Spinosad activates the nicotinic acetylcholine receptor in insects, but at a different site from neonicotinoids. Spinosad also affects the γ-aminobutylic acid receptor, but its role in overall linkage activity is ambiguous.

Spinosad has a broad spectrum of activity on key pests, favoring the environmental profile and efficiency. It is used to kill insects such as leaf miners, thrips, and caterpillars, who destroy, for example, cabbage, spinach, and tomato crops [112]. Spinosad is environmentally friendly as it is degraded by the microbial action of the soil. It poses a minor threat to bee health and beehive activity. In laboratory conditions, the use of spinosad does not affect colony mortality. However, freshly sprayed, it may be intrinsically toxic to bees, and sprayed pollen and nectar may be harmful to brood development. To avoid this, spinosad should be allowed to dry on plant foil for about 3 h. Dry residues are not toxic and do not affect the honey bee’s viability [113].

Fipronil Fipronil is a phenylpyrazole insecticide often used to control insects including fleas, termites, cockroaches, and mosquitoes. Thanks to its wide application, it is used both on animals and plants. Fipronil is a chiral molecule due to the presence of the asymmetric sulfur atom and each enantiomer exhibits a different toxicity. In most cases, S-fipronil is less active against target organisms than R-fipronil. Fipronil interfere with the function of the ɣ-aminobutylic acid receptor chloride channels.

This insecticide disrupts the flow of chlorine ions causing ɣ-aminobutylic acid to build up in synaptic junctions. After application of appropriate doses, fipronil, due to its mode of action, leads to the hyper-expression of the insect nervous system, paralysis, and death [114]. As with neonicotinoids, chemical residues of fipronil can be found in pollen and nectar due to its systemic properties. The fipronil molecules can be taken up by the roots from the soil water and spread throughout the plant, reaching its various tissues [115].

Fipronil may also affect the health of non-target insects, including honey bees. Fipronil is an inhibitor in the mitochondrial bioenergetics of bees, which causes ATP depletion and activation of glycolysis [116]. Fipronil can also cause morphological alterations in larvae midgut, leading to the vacualisation of the cytoplasm, and promote defects in the respiratory process, thereby disrupting the neural activity of bees.

This neurotoxic phenylpyrazole insecticide, when ingested by bees, often causes agitation, convulsions, and paralysis. It also often interferes with motor activity, leading to a reduction in yields in crops pollinated by bees [117]. Fipronil also affects the number of hatched eggs, while reducing the number of new worker bees [118]. This insecticide is known to induce lethal and sub-lethal effects in bee colonies, thereby weakening their immune system and increasing bee mortality [117].

5.2.6. Possible Effects of Chosen Pesticides on A. mellifera Health Examples of possible effects of pesticides that are applied in agriculture and pose a threat to bee health have been collected in the table below (Table 1).

Table 1

Recognized possible effects of chosen pesticides on A. mellifera health (under laboratory conditions).

PesticideApplicationPossible Effect on BeesReferences
AbamectinControl of insect pests and mites destroying horticultural and agricultural crops.Negatively affects the viability and cytotoxic midgut cells which can lead to digestive diseases.[119,120]
AcephateControl a wide range of chewing and sucking insect pests threating agricultural crops.Suppresses esterase activity and reduces body weight.[121,122]
AmitrazControl of ticks, mites, and lice on domestic animals.Increases mortality, leads to behavioral changes in adult honey bees.[123,124]
BifenazateControl of spider mites.Affects the physiology and behavior.[125,126]
BifenthrinControl of insect pests, treatment of mosquito nets, suppression of malaria transmission.Increases mortality, affects central and peripheral nervous systems.[127,128]
ChlorfenapyrControl of insect pests threating agricultural crops and animals.Increases mortality, causes paralysis, affects nervous system.[129,130,131]
CoumaphosControl of insect pests threating agricultural crops and animals.Reduces foraging activity, affects colony mortality, and affects the size of hypopharyngeal glands, significantly affects oxidative status.[105,132,133]
CypermethrinControl of insect pests threating agricultural crops.Leads to a significant hypoglucosemia and hypotrehalosemia, causes minor expressional changes of genes.[134,135]
DeltamethrinControl of disease vectors and eradicating unwanted insects.Interferes with the nervous system such as memory-related characteristics and dance behavior.[136,137]
DiazinonControl of household insects and insect pests threating agricultural crops.Reduces activity of acetylcholineasterase (an enzyme essential to the transmission of nerve impulses), affects odor learning.[138,139]
DimethoateControl of insect pests threating agricultural crops.Leads to inhibition of the acetylcholinesterase, affects physiological traits.[140]
FenitrothionControl of insect pests threating agricultural crops.Leads to a significant hypoglucosemia and hypotrehalosemia, inhibits acetylcholinesterase activity.[134]
FipronilControl of insect pests threating agricultural crops (mostly sunflowers).Increases mortality, affects foraging intensity and homing success.[141]
NeonicotinoidsControl of insect pests threating agricultural crops and deterring pests on domesticated animals.Increases mortality, affects central nervous system, increases the levels of deformed wing virus, affects a large number of up and down-regulated differentially expressed genes, and reduces standard metabolic rate in queens.[142,143,144,145]
SpinosadControl of insect pests affecting agricultural crops.Absence of significant impact on honey bee colonies[146,147]

reference link: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8398688/

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