Fungicides and Their Effects on Non-Target Organisms, Especially Honey Bees

Fungicides are currently the “state of the art” tool in the management of flower, foliar, and fruit diseases of many crops worldwide, especially when cultivars with natural host resistance are not available. For example, in almond, stone fruit, grapes, and other fruit and nut crops in California, some devastating diseases such as brown rot, shot hole, powdery mildew, and anthracnose have been managed using fungicides since these crops were introduced into the state. Furthermore, several fungicide chemistries, i.e., dicarboximides, benzimidazoles, and DMIs with unique modes of action have been used for over 60, 40, and 30 years, respectively. Many of these diseases initiate their disease cycles during host flowering. Thus, without the use of fungicides for managing bloom and foliar diseases, these diseases would be limiting to crop production. One might argue that developing host resistance is the best approach; however, this is very difficult in perennial tree and vine crops and requires many years. Furthermore, crop characteristics selected by the breeder to meet consumer demands often result in higher disease susceptibility of the crop.

In registration processes, all pesticides are extensively evaluated for their efficacy against diseases and their effect against non-target organisms. Toxicity data for new pesticides are required from each registrant and data are evaluated at federal (US Environmental Protection Agency) and sometimes at state (California Department of Pesticide Registration) regulatory agencies. Organisms required to be tested include European honey bees, aquatic invertebrates (e.g., Daphnia spp.), aquatic plants, and vertebrates (e.g., fish, birds, and mammals). For honey bees, the tests are directed to determine acute, short-term toxicity levels by contact and ingestion by adults. If a fungicide is found to be toxic to the adult honey bee, then additional tests are required against the brood. If any toxicity to non-target organisms is found, then a warning or prohibition is placed on the label to limit or restrict usage. Currently registered fungicides are either non-toxic or are practically non-toxic to adult honey bees exposed to extremely high levels of the fungicides. All fungicides registered have been approved only after these requirements are met.

Recently, European honey bees have been affected by Colony Collapse Disorder (CCD), where worker bees suddenly disappear, leaving the hive without a sustained source of honey and pollen. The cause of this disorder is still unknown. Numerous factors have come into scrutiny, including exposure to pesticides. With their longstanding regulatory requirements for pesticides to protect beneficial insects such as honey bees, the US-EPA, however, has no data demonstrating that any EPA-registered pesticide used according to the label instructions has caused CCD. Recent research indicates that it is more likely that a combination of factors, including poor nutrition, parasites (e.g., varroa mite), new diseases (e.g., Israeli Acute Paralysis virus, Nosema species), and changes in bee management (e.g., insect and mite control with pesticides inside the hives and migratory stress and drought, etc. brought about by anthropogenic movement of honey bees long distances) may be responsible for the disorder (http://www.epa.gov/pollinator-protection/colony-collapse-disorder). Other considerations include changes to honey bee populations due to breeding programs that render hives more susceptible to environmental stress, pests, and pathogens, as well as apicultural practices that place bee hives next to highways with high traffic.

Insecticides and Fungicides

More recently, many new insecticides have been introduced that have high toxicity to honey bees and systemic activity in plants. The systemic neonicotinoids and phenylpyrazoles represent two groups that can directly affect honey bee health and may have long residual activity in plants. Although new application methods help to minimize direct exposure of bees to these compounds, the potential negative outcome is that honey bees may instead be exposed to these pesticides over extended periods of time in pollen, nectar, and plant exudates such as water guttation from leaves (http://www.apidologie.org/articles/apido/pdf/2010/03/m09141.pdf) Additionally, the regulatory system governing pesticide use directly in bee hives may also contribute to the problem. Some of the older miticides have become ineffective and thus, new hive-applied pesticides have been recently introduced that may contribute to honey bee management stress.

Chronic exposures to neurotoxic insecticides and their combinations with other pesticides, including fungicides, are known to increase the toxicity of insecticides and elicit reductions in honey bee fitness. Still, no direct association of these pesticide combinations has been shown with CCD. The following guidelines aim to minimize exposure of bees to fungicides applied during flowering of fruit and nut crops. This information was adapted from Mussen and Brandi, 2010[i], Mussen (U.C. Apiaries Newsletter– Jan/Feb 2012), and combined with current fungicide use strategies.

Current research on colony collapse is focused on four general categories of possible causes. These include:

1. Pathogens: Among others, scientists are considering Nosema ceranae and N. apiss (pathogenic gut fungus), Israeli Acute Paralysis Virus, and possibly unknown pathogens as possible culprits for CCD. USDA-ARS research has indicated that the presence of no one pathogen of any class directly correlates with the majority of CCD incidents. Rather, a higher total pathogen load of viruses and bacteria correlates more directly with CCD than any one specific pathogen. The anthropogenic movement of honey bees especially nationally and internationally is one of the most dangerous practices that have been followed by industry that has led to consequences of introduced pathogens.
2. Parasites: Varroa mites are often found in honey bee colonies that are affected by CCD. It is not known if the Varroa mites are directly involved or if the viruses that Varroa mites transmit (similar to the way mosquitoes transmit the malaria virus) are a factor in causing CCD. 
3. Management stressors: Among the management stressors that are possible contributors to CCD are poor nutrition due to apiary overcrowding and increased migratory stress brought on by the honey bees being transported to multiple locations across the country. 
4. Environmental stressors: Such stressors include the impact of pollen/nectar scarcity, lack of diversity in pollen/nectar, availability of only pollen/nectar with low nutritional value, and limited access to water or access only to contaminated water. Stressors also include accidental or intentional exposure to pesticides at lethal or sub-lethal levels.

Use of pesticides during flowering of agricultural commodities -

Insecticides should never be applied with fungicides during the bloom period of tree crops and many other agricultural crops. Acaricides/insecticides (e.g., all neonicotinoids, all pyrethroids) may be synergistic with chlorothalonil and all DMI fungicides and the toxicity of the acaricide/ insecticide to honey bee brood may be increased. For example, mixing a pyrethroid, IRAC Code 3A, with chlorothalonil or a DMI may increase toxicity of the insecticide. Chlorpyrifos and other organophosphates (IRAC Code 1B), mixed with SDHI and QoI fungicides FRAC Codes 7 (e.g., boscalid) and 11 (e.g., pyraclostrobin) may increase toxicity of the insecticide to honey bees.

Insecticides are often mixed with fungicides for many tree crops in the growing season. When using systemic insecticides (e.g., neonicotinoids), be aware that they may be long lasting in the plant and may affect honey bees and other insects for several months after application.

Thus, fungicides are less involved in honey bee colony collapse than previously considered. Still, for selection and usage, choose fungicides that do not accumulate in honey bee products (e.g., bee bread). Johnson et al. (2010) (http://www.apidologie.org/articles/apido/pdf/2010/03/m09141.pdf) indicated that possible fungicides that may accumulate to high levels in pollen are chlorothalonil, captan, and iprodione. These fungicides can be used after bloom for other foliar and fruit diseases during the season.

Follow UC-IPM Honey Bee Best Management Practices for Almonds (http://www.almonds.com/sites/default/files/content/attachments/honey_bee_bmp_practices_quick_guide_for_almonds.pdf). Some important aspects are listed below:

1. Most fungicides are formulated with adjuvants including wetting agents, spreaders, and stickers. Unless a registrant specifically indicates on the product label that an adjuvant should be added, most fungicide products do not need additional adjuvants mixed into the sprayer tank to improve performance. With few exceptions, adjuvants do not statistically improve the efficacy of fungicides for managing diseases of fruit and nut commodities. Although there is limited information on the interaction of adjuvants and fungicides with honey bees, it is best to follow a conservative approach. Because adjuvants may increase the wettability of bees and subsequently the potential toxicity of fungicides, adjuvants should not be used in fungicide applications during bloom or when there is high honey bee activity in the field.
2. Do not apply fungicides when honey bees are in flight in orchards. Contaminated foraging worker bees will carry the fungicide back to the hive where other worker bees will clean them and contaminate the hive’s food supply.
3. Do not apply fungicides when pollen is available. Pollen is released when temperatures reach 13°C (55°F) in the morning and is often removed by honey bees by late afternoon. Thus, from late afternoon until very early the next morning, the amount of fresh pollen available is at the lowest levels of the day.
4. Apply fungicides in the evening or at night or when temperatures are less than 13°C (55°F).
5. Turn off sprayer near hives.
6. Follow UC guidelines and make a single delayed bloom application at 20-30% bloom if environmental conditions are not conducive for disease development, to minimize the total number of fungicide applications during bloom.
7. Follow UC guidelines on fungicide resistance management to limit honey bee exposure to any one fungicide product by following the “RULES” (see Fungicide Resistance).

[i] Mussen, E. and Brandi, G. 2010. Relationships of Honey Bees and Pesticides. http://entomology.ucdavis.edu/files/147612.pdf (accessed 12/14/2015)