Fungicide Safety

Fungicides during bloom – the pollination paradox

Practices that maximize productivity can undermine the pollination process, reducing profitability.                                                      Updated March 2017

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Fungicides are useful tools for growers to protect against many serious plant pathogens.  The use of fungicides, however, can have serious health effects for honey bees and other pollinators.  These health effects can lead to weaker colonies, or even colony loss.  Weaker and lost colonies mean an increase in rental fees, as well as less efficient pollination services, increasing costs, and reducing benefits.  This document reviews the known effects that fungicide products can have on honey bee health, and provides some guidelines to reduce honey bee fungicide exposure, and protect your investment in pollination services.

Honey bee on apple blossom Zachary Huang

Exposure

Honey bees can come into contact with fungicides through direct spray, contact with treated crops, drift onto nearby floral resources, and water contamination through runoff. Foraging bees will carry resources and pesticides back to the hive, which means that bees who are not coming into immediate contact with pesticides can still be exposed through stored hive products. Stored pesticides can remain in bee hives for a long period, resulting in chronic exposure. Fungicides are commonly found in honey bee hives – fungicide residues found in both hive pollen stores and in wax comb are significantly higher than residues of herbicides or insecticides. Fungicides are a significant contaminant of bee bread, the main food source for developing bees, and have also been detected in honey.

The danger of chemical mixtures

Honey bees are exposed to many agrochemicals at once. When mixed with other chemicals, fungicides can increase in toxicity, and they can increase the toxicity of other chemicals - a phenomenon called “synergism.” Fungicides can cause synergistic effects with many commonly used chemicals. Synergistic effects include increased risk of disease, an inability to detoxify other chemicals, a reduction in energy within flight muscles, an increase in hypothermia, and an inability to digest important compounds in their diet. Some pyrethroid insecticides repel pollinating bees, so they are considered “safe for pollinators.”  Fungicides can reduce this repellency effect and therefore increase the insecticide’s toxicity. Many fungicide products that are deemed “safe for bees” can become very hazardous when they are combined with other chemicals.

Knowledge gaps

Pesticide regulations and labels do not reflect true risks to bees. Label restrictions focus only on death after acute exposure and are not found on chemicals like fungicides that cause sub-lethal effects - they do not immediately cause death but still severely disrupt the bee’s health and ability to function properly. Each bee fills a distinct role within the colony, and fungicides can disrupt a bee’s ability to perform their role, causing a ripple effect within the colony, and eventually leading to colony collapse.

Just because fungicides are not labeled as “toxic to pollinators” does not mean the product is safe for bees!

Other risks are highly understudied, including effects in developing bees, and the increased toxicity caused by combined exposures. Recent studies have begun to examine fungicide ingredients that are supposedly “inert”, such as spray adjuvants; these compounds can lead to a decrease in immune function, and learning and memory impairment in bees. It is vital that these knowledge gaps be addressed and that new risk management strategies are developed to protect bees.

Tips for protecting bees from fungicides

• Avoid fungicide applications during crop bloom.
• Avoid tank mixing fungicides with other chemicals, and space treatments as much as possible
• Spray after sunset or before sunrise, or when the temperature is below 50^oF.
• Use IPM practices to reduce fungicide applications and to increase treatment efficiency.
• Use drift reduction practices.
• Remove any flowering weeds from crop plantings.
• Develop a pollination contract and bee safety plan with your beekeeper.
• Establish bee-friendly habitat away from crops and protected from sprays.
• Keep up to date on current research and new strategies to protect bees on your farm.

Known effects of fungicides on honey bee health

Cellular function and lowered detoxification ability

• Lower ATP levels (lower energy) after fungicide exposure ¹
• Oxidative stress after fungicide exposure²
• Inhibition of detoxification pathways, increasing the toxicity of some pyrethroids and neonicotinoids ²
• Negative effect on oxygen consumption rate of mitochondria³
• Fungicides caused hypothermia at dose levels much lower than field rates⁴

Larvae

• Increased larval mortality from fungicides^{2, 5}
• Abnormal worker pupae development due to failure to eclose (emerge) properly⁵
• Significantly higher toxicity to larvae than adults⁶
• Increased cell death in larvae midguts⁷

Behavioral changes

• Impairment in olfactory learning, reducing the ability to find food and to communicate location of food sources to others
• Learning and memory impairment from spray adjuvants commonly used with fungicides⁸  

Susceptibility to diseases

• Increased virus titers after fungicide exposure⁹
• Some fungicides significantly reduce a bee’s ability to survive infection¹⁰
• Bees exposed to fungicides were 3x as likely to have microsporidial infection than unexposed bees⁸
• Prepupae down-regulated pathogen recognition genes after exposure to fungicides¹¹

Lower viral defense genes and higher incidence of Black Queen Cell Virus when larvae exposed to organosilicone spray adjuvants and pathogens together¹²

The link between fungicides and nutrition. Pollen is the sole source of protein for a honey bee colony, and is essential for the growth of the developing bees.  Pollen is modified into a substance known as bee bread, which is stored as a long-term food source for larvae when fresh pollen is not available.  Fungicides are thought to affect the formation of bee bread, risking the long-term nutrition and feed availability for the colony.                            

Bee bread stored in a hive. Sarah Scott

Fungicide effects on bee bread and nutrition

• Decreased pollen consumption in fungicide treated pollen¹
• Reduced protein digestion after fungicide exposure¹
• Decreased beneficial gut bacteria for making bee bread¹³
• Toxic to yeasts in floral nectar, may influence pollination services as well as bee nutrition¹⁴
• Significantly reduced pollen viability for up to 48 hours¹⁵
•  Fungicide treatments in orchards reduce bee bread fungi ^16,17

1. Decourtye, A., et al. 2004. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis millifera. Arch Environ Contam Toxicol 48: 242-250. 2 Johnson, R.M. 2015. Honey Bee Toxicology. Annu Rev Entomol 60: 415-434. 3 Campbell, J.B., et al. 2015. The fungicide Pristine inhibits mitochondrial function in vitro, but not flight metabolic rates in honey bees. J Insect Phys 86(2016): 11-16. 4 Vandame, R., and L.P Belzunces. 1998. Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neurosci. (1998): 57-60. 5 Mussen, E.C., et al. 2004. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera. Environ Entomol 33(5): 1151-1154. 6 Zhu, W., et al. 2014. Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS ONE 9(1). 7 Gregorc, A., and J.D. Ellis. 2011. Cell death localization in situ in laboratory reared honey bee (Apis mellifera) larvae treated with pesticides. Pest Biochem and Physiol 99: 200-207. 8 Ciarlo, T.J., et al. 2012. Learning impairment in honey bees caused by agricultural spray adjuvants. PLoS ONE 7 (7). 9 Degrandi-Hoffman, G., et al. 2015. Effects of oral exposure to fungicides on honey bee nutrition and virus levels. J Econ Entomol 108(6):2518-2528. 10 Pettis, J.S., et al. 2013. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8(7). 11 Cizelj, I., et al. 2015. Prochloraz and coumaphos induce different gene expression patterns in three developmental stages of Carniolan honey bee. Pest Biochem and Physiol 2015. 12 Fine, J.D., et al. 2017. An inert pesticide adjuvant synergizes viral pathogenicity and mortality in honey bee larvae. J Sci Rep 7: 40499. 13 Kakumanu, M.L., et al. 2016. Honey bee gut microbiome is altered by in-hive pesticide exposures. Front Microbio 7:1255. 14 Bartlewicz, J., et al. 2016. Effects of agricultural fungicides on microorganisms associated with floral nectar: Susceptibility assay and field experiments. Environ Sci Pollut Res 23(19): 19776-19786. 15 Fell, R.D., et al. 1983. Effects of fungicide sprays during apple bloom on pollen viability and honey bee foraging. Environ Entomol 12: 1572-1575. 16 Yoder, J., et al. 2012. Fungicides reduce symbiotic fungi in bee bread and the beneficial fungi in colonies. Honey Bee Colony Health: Challenges and Sustainable Solutions: 193-214. 17 Yoder, J.A., et al. 2013. Fungicide Contamination reduces beneficial fungi in bee bread based on area-wide field study in honey bee, Apis mellifera, colonies. J Toxicol Environ Health 76(10):587-600.