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TOXICITY TO HONEY BEES
By:
WAHAB ALI WAZIR
MPhil Scholar
2nd Semester
Department of Zoology
Course Instructor:
DR. ISHTIAQ ANJUM
Assistant Professor
Department of Zoology
Department Of Zoology
Kohat University Of Science &Technology,Kohat-26000
Khyber Pakhtunkhwa, Pakistan
TOXICITY TO HONEY BEE:-
There are several ways that honey bee poisoning can occur, such as
a chemical was used on crops that are flowering, and foraging bees
are exposed to contaminated foliage, nectar or pollen.
Honey bees contribute more than 90% of the global pollination of
more than approximately 85% of the total cross-pollinated plant
species in the world, the blessing of being able to hover around and
pollinate this much diverse array of floral plant species comes with
a curse to these bees, of being in unremitting contact with a wide
array of stresses like, parasites, predators, diseases, chemical, etc.
present in the environment.
 As being the most successful and commercially exploited
pollinators in agro-ecosystems not just for their pollination
duties but for commercially valuable by-products such as,
honey, wax, propolis, etc. as well, honey bees faces more
diverse stresses in nature.
 Honeybees (Apis mellifera) are exposed to an ever changing
array of xenobiotics from both natural and synthetic sources.
 Thousands of older foraging worker honey bees travel as far as
10 km from the hive in the course of collecting the nectar,
pollen, water, and propolis needed to sustain a colony of tens of
thousands of young adult workers, immature bees, and male
reproductive or drones
 Nectar and pollen may contain environmental pollutants or
systemic pesticides drawn from the soil, or they can be
contaminated from topical pesticide applications or drift from such
applications.
 Different agro-chemicals like, herbicides, fungicides and most
importantly the insecticides, alone and in combination with other
factors such as elevated temperature, production of hybrid varieties
with lesser quantity of pollen and nectar in their flowers, have
caused a devastating effect on honey bees at a global level.
 Bee foragers may bring such contaminated floral rewards back to
the colony for feeding and storing as a resource for future
generations
 While foraging over this large area for collecting pollen and nectar to satisfy the
carbohydrate needs of the colony, bees forage in various flowering plants with
different nature, but these food sources are not always entirely pure every time,
 having either different plant derived chemicals or the widely used toxic agro-
chemicals mixed with them. With the ever increasing use of synthetic chemical
pesticides in agriculture honey bees and other wild pollinators have faced a serious
threat to their global biodiversity in recent decades
 Pesticides which are being used in agriculture crops are highly toxic to
bees as they kill the bees through many ways such as, direct killing of
foraging workers with their acute toxicity, drifting out from agricultural
land to nearby apiaries,
 thus, making the whole colony more susceptible to different pathogens
and to some point reduce their possibility to thrive in the nature by getting
accumulated in the pollen inside the colony.
 Nectars produced by some flowering plant species also contain plant-
synthesized chemicals which are toxic to different pollinators.
 The farmers discriminately use these agro-chemicals with a
purpose to manage the pests; instead, they end up with killing their
own beneficial insects, i.e., the pollinators.
 Honey bees and other pollinators get exposed to different toxic
agro-chemicals in nature through different paths and these different
pesticides affect honey bee colonies to different levels thus;
 to minimize the losses to pollinators from the adverse effect of
pesticide poisoning is a burning topic of interest for human to
protect the pollinators.
Routes of exposures to different pesticides:-
 The different types of pesticidal formulations travel across the plant
through different ways in order to protect the plant or part of it from
different factors such as weeds, pathogen, insect pests or rodents, etc.
 According to the nature of the different pesticides, three principal
application methods that are often used to treat crops are: direct spray,
which is often used around homes and gardens; soil applications and
seed applications, typically used in larger treatment systems.
 These different methods of application play a crucial role in the
exposure of these chemicals to the insect pollinators, visiting a crop
 Thus, on the basis of different application methods and the persistence of
different pesticides in nature, bees get exposed to different pesticides
through these major routes:
 Direct contact with chemical during foraging on a treated plant
 Pesticide particles of dust formulations sticking to the foraging bees or to
whole colony via drift through wind
 Pesticidal runoff from the treated fields to nearby water reservoirs
 Pesticidal drift to non-treated foraging plants growing nearby to the treated
crop
 Pesticidal residues in pollen through seed treatment

 These different routes for exposure of various pesticides to honey
bees facilitate their entry into a honey bee colony system, but still
the mode by which, these chemicals are pulled out by the forager
bees from the fields are quite different being either by oral,
respiratory or dermal intake.
 These different modes of intake of such chemicals are described
here.[Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K.
Multiple routes of pesticide exposure for honey bees living near
agricultural fields.[PLoS One. 2012;7(1):e29268. DOI:
10.1371/journal.pone.0029268]
Mode of intake of toxicants:-
1. ORAL INTAKE
 Oral intake of chemical pesticides from fields is facilitated through the foraging
worker bees. Plants treated with different systemic insecticides, produce nectar and
pollen containing these insecticides and thus, worker bees collecting this floral
resource carries to the colonies to store it into the colony and further use to feed
the young developing brood.
 Several reports of an extremely high concentration of different pesticidal
compounds, including insecticides, fungicides, miticides and herbicides have been
reported from pollen samples of several crops .
 These events, from collecting the pollen in the field to feeding to the developing
brood results in to a chain of catastrophic events as: foragers are killed during
collecting and transporting such contaminated pollen, nurse bees are killed while
storing and feeding pollen and the brood are killed by consuming the toxic pollen,
thus, leading to a total collapse of the colony.
2. RESPIRATORY INTAKE
 Respiration of pure oxygen plays a vital role in an organism’s growth
and development since it ensures proper functioning of various
organs in the organism.
 But respiration of air admixture with toxicants causes various
abnormalities such as abrupt behavioral changes and degradation of
learning ability.
 Pesticide formulations like, dust and fumigants travels through the air
called ‘drift’ can either be carried out onto the body surface of
foraging bees or can be absorbed through trachea (respiratory organs)
in sufficient concentrations to be toxic to the bees[Karise R, Mänd M.
Recent insights into sublethal effects of pesticides on insect
respiratory physiology. Insect Physiology. 2015;5:31-39].
DERMAL INTAKE
 This is the major mode of intake of toxicants by the bees since
they are exposed to direct contact of pesticides in the fields while
foraging on the crops.
 Honey bee foragers come in direct contact with several pesticides
while foraging and such chemicals can be lethal even in small
quantities.
 Dermal toxicity through topical spray has been reported for
various insecticides and thorax has widely been regarded as a
major route of dermal exposure of pesticides to the honey bees
.Other than thorax, insect wings have been reported as a more
lethal route of exposure to the bees
Some of the majorly important and frequent ways of dermal intakes are
following:
 Majority of bee poisoning is due to application of insecticides to crops
during blooming period.
 Bees coming in contact of treated areas.
 Bees coming in contact with insecticides residues on plants and collect
insecticide dust with pollen.
 Bees drinking or touching contaminated water or honeydew on the
ground or foliage or from nearby water bodies.
 Contamination through treated nectar sources. Dimethaote is the only
systemic insecticide known to be excreted in hazardous amount in nectar
under field conditions.
Symptoms of bee poisoning
 One of the obvious signs of pesticide poisoning is the presence of a
large number of dead or dying bees at the hive entrance.
 These bees are foragers who have been exposed to pesticides sprayed
in the fields.
 Another common symptom includes the presence of a moist and
sticky mass of dead bees at the hive entrance.
 This results from poisoning by some fast-acting pesticides, e.g.,
organophosphorus pesticides.
 Dying bees extend their tongues through which nectar is regurgitated
resulting in sticky and moist dead bees.
 Bees that have been exposed to a pesticide may regurgitate a thick and
dark fluid.
Classification of toxicants
 Classification of different toxicants to honey bees can be done
either on the basis of levels of toxicity or on the basis of sources
in the nature.
 Different toxicants have variable toxicity levels, according to
their mode of action on bees and this toxicity level is measured as
LD50, which is the dose at which 50% of the bee population dies
due to the intoxication.
 On the basis of their LD50 levels, toxicants have been classified
into four different categories[Apis mellifera. Environmental
Entomology. 1980;9(1):144-150. DOI: 10.1093/ee/9.1.144].
 Honey bee populations, however, have been affected
by a combination of environmental factors in recent
years [CCD Steering Committee. Available online
https://www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf
(accessed on 20 June 2017)].
 Studies suggest that bee declines, generally, are caused
by the interaction of many stress factors, including
pathogens, parasitic mites, pesticides, lack of forage
and nesting habitat due to intensive monocultures, and
stress from poor nutrition and the transport of hives for
commercial pollination .
 Pesticide exposure has received a disproportionate amount of media
attention due to the presence of agricultural chemicals detected in
honey bee wax and pollen.
 One class of pesticides, known as neonicotinoids, has been implicated
in increased mortality of honey bee colonies and has become the
subject of much debate and regulatory restrictions on its use.
 Neonicotinoids are systemic pesticides that, once applied by foliar
sprays, trunk injection, or root drenching, are transported throughout
the plant vascular tissue and protect against sap-feeding insects.
 Neonicotinoids act as nicotinic acetylcholine receptors, blocking the
transmission of nerve impulses in the central nervous system of insects.
 Bees can encounter systemic insecticides, such as neonicotinoids,
in many ways, including direct contact with foliar sprays or
particles released during treated seed planting, contacting residues
on treated plants or nesting substrate, or consuming contaminated
pollen, nectar, and water.
 Neonicotinoids may also have indirect effects on honey bees by
altering the community structure of the bee gut microbiome.
 However, because of their lower mammalian toxicity,
neonicotinoids are sometimes considered lower risk relative to
other pesticides.
.
References
 Ollerton, J.; Winfree, R.; Tarrant, S. How Many Flowering Plants Are
Pollinated by Animals? Oikos 2011, 120, 321–326. [Google Scholar]
[CrossRef]
 Klein, A.-M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.;
Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of Pollinators in
Changing Landscapes for World Crops. Proc. R. Soc. B Biol. Sci. 2007,
274, 303–313. [Google Scholar] [CrossRef] [PubMed][Green Version]
 Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.;
Kunin, W.E. Global Pollinator Declines: Trends, Impacts and Drivers.
Trends Ecol. Evol. 2010, 25, 345–353. [Google Scholar] [CrossRef]
 Calderone, N.W. Insect Pollinated Crops, Insect Pollinators and
US Agriculture: Trend Analysis of Aggregate Data for the Period
1992–2009. PLoS ONE 2012, 7, e37235. [Google Scholar]
[CrossRef][Green Version]
 CCD Steering Committee. Available online:
https://www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf (accessed
on 20 June 2017).
 Van Engelsdorp, D.; Evans, J.D.; Saegerman, C.; Mullin, C.;
Haubruge, E.; Nguyen, B.K.; Frazier, M.T.; Frazier, J.L.; Cox-
Foster, D.; Chen, Y.; et al. Colony Collapse Disorder: A
Descriptive Study. PLoS ONE 2009, 4, e6481. [Google Scholar]
[CrossRef]
Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E.L. Bee
Declines Driven by Combined Stress from Parasites,
Pesticides, and Lack of Flowers. Science 2015, 347,
1255957. [Google Scholar] [CrossRef]
Belsky, J.E.; Joshi, N.K. Effects of Fungicide and
Herbicide Chemical Exposure on Apis and Non-Apis Bees
in Agricultural Landscape. Front. Environ. Sci. 2020, 8, 81.
[Google Scholar] [CrossRef]
Siviter, H.; Bailes, E.J.; Martin, C.D.; Oliver, T.R.;
Koricheva, J.; Leadbeater, E.; Brown, M.J.F.
Agrochemicals Interact Synergistically to Increase Bee
Mortality. Nature 2021, 596, 389–392. [Google Scholar]
[CrossRef]
 Ostiguy N, Drummond FA, Aronstein K, Eitzer B, Ellis JD, Spivak
M, et al. Honey bee exposure to pesticides: A four-year nationwide
study. Insects. 2019;10(1):13. DOI: 10.3390/insects10010013
 Wright SI, Kalisz S, Slotte T. Evolutionary consequences of self-
fertilization in plants. Proceedings of the Royal Society B:
Biological Sciences. 2013;280(1760):20130133. DOI:
10.1098/rspb.2013.0133
 Beekman M, Ratnieks FL. Long-range foraging by the honey-bee,
Apis mellifera L. Functional Ecology. 2000;14(4):490-496. DOI:
10.1046/j.1365-2435.2000.00443.x
 Decourtye A, Mader E, Desneux N. Landscape enhancement of
floral resources for honey bees in agro-ecosystems. Apidologie.
2010;41(3):264-277. DOI: 10.1051/apido/2010024

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Wahab Wazir.pptx

  • 1. TOXICITY TO HONEY BEES By: WAHAB ALI WAZIR MPhil Scholar 2nd Semester Department of Zoology Course Instructor: DR. ISHTIAQ ANJUM Assistant Professor Department of Zoology Department Of Zoology Kohat University Of Science &Technology,Kohat-26000 Khyber Pakhtunkhwa, Pakistan
  • 2. TOXICITY TO HONEY BEE:- There are several ways that honey bee poisoning can occur, such as a chemical was used on crops that are flowering, and foraging bees are exposed to contaminated foliage, nectar or pollen. Honey bees contribute more than 90% of the global pollination of more than approximately 85% of the total cross-pollinated plant species in the world, the blessing of being able to hover around and pollinate this much diverse array of floral plant species comes with a curse to these bees, of being in unremitting contact with a wide array of stresses like, parasites, predators, diseases, chemical, etc. present in the environment.
  • 3.  As being the most successful and commercially exploited pollinators in agro-ecosystems not just for their pollination duties but for commercially valuable by-products such as, honey, wax, propolis, etc. as well, honey bees faces more diverse stresses in nature.  Honeybees (Apis mellifera) are exposed to an ever changing array of xenobiotics from both natural and synthetic sources.  Thousands of older foraging worker honey bees travel as far as 10 km from the hive in the course of collecting the nectar, pollen, water, and propolis needed to sustain a colony of tens of thousands of young adult workers, immature bees, and male reproductive or drones
  • 4.  Nectar and pollen may contain environmental pollutants or systemic pesticides drawn from the soil, or they can be contaminated from topical pesticide applications or drift from such applications.  Different agro-chemicals like, herbicides, fungicides and most importantly the insecticides, alone and in combination with other factors such as elevated temperature, production of hybrid varieties with lesser quantity of pollen and nectar in their flowers, have caused a devastating effect on honey bees at a global level.  Bee foragers may bring such contaminated floral rewards back to the colony for feeding and storing as a resource for future generations
  • 5.  While foraging over this large area for collecting pollen and nectar to satisfy the carbohydrate needs of the colony, bees forage in various flowering plants with different nature, but these food sources are not always entirely pure every time,  having either different plant derived chemicals or the widely used toxic agro- chemicals mixed with them. With the ever increasing use of synthetic chemical pesticides in agriculture honey bees and other wild pollinators have faced a serious threat to their global biodiversity in recent decades
  • 6.  Pesticides which are being used in agriculture crops are highly toxic to bees as they kill the bees through many ways such as, direct killing of foraging workers with their acute toxicity, drifting out from agricultural land to nearby apiaries,  thus, making the whole colony more susceptible to different pathogens and to some point reduce their possibility to thrive in the nature by getting accumulated in the pollen inside the colony.  Nectars produced by some flowering plant species also contain plant- synthesized chemicals which are toxic to different pollinators.
  • 7.
  • 8.  The farmers discriminately use these agro-chemicals with a purpose to manage the pests; instead, they end up with killing their own beneficial insects, i.e., the pollinators.  Honey bees and other pollinators get exposed to different toxic agro-chemicals in nature through different paths and these different pesticides affect honey bee colonies to different levels thus;  to minimize the losses to pollinators from the adverse effect of pesticide poisoning is a burning topic of interest for human to protect the pollinators.
  • 9. Routes of exposures to different pesticides:-  The different types of pesticidal formulations travel across the plant through different ways in order to protect the plant or part of it from different factors such as weeds, pathogen, insect pests or rodents, etc.  According to the nature of the different pesticides, three principal application methods that are often used to treat crops are: direct spray, which is often used around homes and gardens; soil applications and seed applications, typically used in larger treatment systems.  These different methods of application play a crucial role in the exposure of these chemicals to the insect pollinators, visiting a crop
  • 10.  Thus, on the basis of different application methods and the persistence of different pesticides in nature, bees get exposed to different pesticides through these major routes:  Direct contact with chemical during foraging on a treated plant  Pesticide particles of dust formulations sticking to the foraging bees or to whole colony via drift through wind  Pesticidal runoff from the treated fields to nearby water reservoirs  Pesticidal drift to non-treated foraging plants growing nearby to the treated crop  Pesticidal residues in pollen through seed treatment
  • 11.
  • 12.  These different routes for exposure of various pesticides to honey bees facilitate their entry into a honey bee colony system, but still the mode by which, these chemicals are pulled out by the forager bees from the fields are quite different being either by oral, respiratory or dermal intake.  These different modes of intake of such chemicals are described here.[Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. Multiple routes of pesticide exposure for honey bees living near agricultural fields.[PLoS One. 2012;7(1):e29268. DOI: 10.1371/journal.pone.0029268]
  • 13. Mode of intake of toxicants:- 1. ORAL INTAKE  Oral intake of chemical pesticides from fields is facilitated through the foraging worker bees. Plants treated with different systemic insecticides, produce nectar and pollen containing these insecticides and thus, worker bees collecting this floral resource carries to the colonies to store it into the colony and further use to feed the young developing brood.  Several reports of an extremely high concentration of different pesticidal compounds, including insecticides, fungicides, miticides and herbicides have been reported from pollen samples of several crops .  These events, from collecting the pollen in the field to feeding to the developing brood results in to a chain of catastrophic events as: foragers are killed during collecting and transporting such contaminated pollen, nurse bees are killed while storing and feeding pollen and the brood are killed by consuming the toxic pollen, thus, leading to a total collapse of the colony.
  • 14.
  • 15. 2. RESPIRATORY INTAKE  Respiration of pure oxygen plays a vital role in an organism’s growth and development since it ensures proper functioning of various organs in the organism.  But respiration of air admixture with toxicants causes various abnormalities such as abrupt behavioral changes and degradation of learning ability.  Pesticide formulations like, dust and fumigants travels through the air called ‘drift’ can either be carried out onto the body surface of foraging bees or can be absorbed through trachea (respiratory organs) in sufficient concentrations to be toxic to the bees[Karise R, Mänd M. Recent insights into sublethal effects of pesticides on insect respiratory physiology. Insect Physiology. 2015;5:31-39].
  • 16. DERMAL INTAKE  This is the major mode of intake of toxicants by the bees since they are exposed to direct contact of pesticides in the fields while foraging on the crops.  Honey bee foragers come in direct contact with several pesticides while foraging and such chemicals can be lethal even in small quantities.  Dermal toxicity through topical spray has been reported for various insecticides and thorax has widely been regarded as a major route of dermal exposure of pesticides to the honey bees .Other than thorax, insect wings have been reported as a more lethal route of exposure to the bees
  • 17. Some of the majorly important and frequent ways of dermal intakes are following:  Majority of bee poisoning is due to application of insecticides to crops during blooming period.  Bees coming in contact of treated areas.  Bees coming in contact with insecticides residues on plants and collect insecticide dust with pollen.  Bees drinking or touching contaminated water or honeydew on the ground or foliage or from nearby water bodies.  Contamination through treated nectar sources. Dimethaote is the only systemic insecticide known to be excreted in hazardous amount in nectar under field conditions.
  • 18.
  • 19. Symptoms of bee poisoning  One of the obvious signs of pesticide poisoning is the presence of a large number of dead or dying bees at the hive entrance.  These bees are foragers who have been exposed to pesticides sprayed in the fields.  Another common symptom includes the presence of a moist and sticky mass of dead bees at the hive entrance.  This results from poisoning by some fast-acting pesticides, e.g., organophosphorus pesticides.  Dying bees extend their tongues through which nectar is regurgitated resulting in sticky and moist dead bees.  Bees that have been exposed to a pesticide may regurgitate a thick and dark fluid.
  • 20. Classification of toxicants  Classification of different toxicants to honey bees can be done either on the basis of levels of toxicity or on the basis of sources in the nature.  Different toxicants have variable toxicity levels, according to their mode of action on bees and this toxicity level is measured as LD50, which is the dose at which 50% of the bee population dies due to the intoxication.  On the basis of their LD50 levels, toxicants have been classified into four different categories[Apis mellifera. Environmental Entomology. 1980;9(1):144-150. DOI: 10.1093/ee/9.1.144].
  • 21.  Honey bee populations, however, have been affected by a combination of environmental factors in recent years [CCD Steering Committee. Available online https://www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf (accessed on 20 June 2017)].  Studies suggest that bee declines, generally, are caused by the interaction of many stress factors, including pathogens, parasitic mites, pesticides, lack of forage and nesting habitat due to intensive monocultures, and stress from poor nutrition and the transport of hives for commercial pollination .
  • 22.
  • 23.  Pesticide exposure has received a disproportionate amount of media attention due to the presence of agricultural chemicals detected in honey bee wax and pollen.  One class of pesticides, known as neonicotinoids, has been implicated in increased mortality of honey bee colonies and has become the subject of much debate and regulatory restrictions on its use.  Neonicotinoids are systemic pesticides that, once applied by foliar sprays, trunk injection, or root drenching, are transported throughout the plant vascular tissue and protect against sap-feeding insects.  Neonicotinoids act as nicotinic acetylcholine receptors, blocking the transmission of nerve impulses in the central nervous system of insects.
  • 24.  Bees can encounter systemic insecticides, such as neonicotinoids, in many ways, including direct contact with foliar sprays or particles released during treated seed planting, contacting residues on treated plants or nesting substrate, or consuming contaminated pollen, nectar, and water.  Neonicotinoids may also have indirect effects on honey bees by altering the community structure of the bee gut microbiome.  However, because of their lower mammalian toxicity, neonicotinoids are sometimes considered lower risk relative to other pesticides. .
  • 25.
  • 26. References  Ollerton, J.; Winfree, R.; Tarrant, S. How Many Flowering Plants Are Pollinated by Animals? Oikos 2011, 120, 321–326. [Google Scholar] [CrossRef]  Klein, A.-M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of Pollinators in Changing Landscapes for World Crops. Proc. R. Soc. B Biol. Sci. 2007, 274, 303–313. [Google Scholar] [CrossRef] [PubMed][Green Version]  Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W.E. Global Pollinator Declines: Trends, Impacts and Drivers. Trends Ecol. Evol. 2010, 25, 345–353. [Google Scholar] [CrossRef]
  • 27.  Calderone, N.W. Insect Pollinated Crops, Insect Pollinators and US Agriculture: Trend Analysis of Aggregate Data for the Period 1992–2009. PLoS ONE 2012, 7, e37235. [Google Scholar] [CrossRef][Green Version]  CCD Steering Committee. Available online: https://www.ars.usda.gov/is/br/ccd/ccd_actionplan.pdf (accessed on 20 June 2017).  Van Engelsdorp, D.; Evans, J.D.; Saegerman, C.; Mullin, C.; Haubruge, E.; Nguyen, B.K.; Frazier, M.T.; Frazier, J.L.; Cox- Foster, D.; Chen, Y.; et al. Colony Collapse Disorder: A Descriptive Study. PLoS ONE 2009, 4, e6481. [Google Scholar] [CrossRef]
  • 28. Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E.L. Bee Declines Driven by Combined Stress from Parasites, Pesticides, and Lack of Flowers. Science 2015, 347, 1255957. [Google Scholar] [CrossRef] Belsky, J.E.; Joshi, N.K. Effects of Fungicide and Herbicide Chemical Exposure on Apis and Non-Apis Bees in Agricultural Landscape. Front. Environ. Sci. 2020, 8, 81. [Google Scholar] [CrossRef] Siviter, H.; Bailes, E.J.; Martin, C.D.; Oliver, T.R.; Koricheva, J.; Leadbeater, E.; Brown, M.J.F. Agrochemicals Interact Synergistically to Increase Bee Mortality. Nature 2021, 596, 389–392. [Google Scholar] [CrossRef]
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