McGrath, M.T. 2004. What are Fungicides. The Plant Health Instructor. DOI: 10.1094/PHI-I-2004-0825-01. Updated 2016.
Diseases are a major source of crop and plant damage that can be caused by a number of plant pathogenic (disease-causing) organisms. Fungi are the number one cause of crop loss worldwide. Viruses, nematodes, and bacteria also cause diseases in plants (Figures 1, 3, 4). Symptoms resembling those caused by pathogens can be caused by abiotic (non-living) factors, such as nutrient deficiency and air pollution (compare Figures 2, 5, and 6), and also insects (Figure 6).
Fungicides, herbicides and insecticides are all pesticides used in plant protection. A fungicide is a specific type of pesticide that controls fungal disease by specifically inhibiting or killing the fungus causing the disease. Not all diseases caused by fungi can be adequately controlled by fungicides. These include the vascular diseases Fusarium and Verticillium wilt (Figure 7). Diseases caused by other types of organisms, disorders caused by abiotic factors, and insect damage are not controlled by fungicides. Thus it is essential to first determine the cause of symptoms before applying a fungicide.
Diseases are a common occurrence on plants, often having a significant economic impact on yield and quality, thus managing diseases is an essential component of production for most crops. Broadly, there are three main reasons fungicides are used: (a) To control a disease during the establishment and development of a crop. (b) To increase productivity of a crop and to reduce blemishes. Diseased food crops may produce less because their leaves, which are needed for photosynthesis, are affected by the disease (Figures 8 - 11). Blemishes can affect the edible part of the crop (Figures 6 and 14) or, in the case of ornamentals, their attractiveness (Figures 12 - 13), which both can affect the market value of the crop. (c) To improve the storage life and quality of harvested plants and produce. Some of the greatest disease losses occur post-harvest (Figures 14 and 15). Fungi often spoil (render unusable) stored fruits, vegetables, tubers, and seeds. A few which infect grains produce toxins (mycotoxins) capable of causing severe illness or even death in humans and animals when consumed. Fungicides have been used to reduce mycotoxin contamination in wheat affected by Fusarium head blight, but most fungicides developed so far have not been sufficiently effective to be useful for managing mycotoxins associated with other diseases.
Plant diseases are best managed by integrating a number of control practices that may include: crop rotation, selection of disease-tolerant or disease-resistant crop cultivars (cultivars genetically less susceptible than other cultivars), time of planting, level of fertilization, micro-climate modification, sanitation, and application of fungicides. Fungicides are often a vital part of disease management as (a) they control many diseases satisfactorily, (b) cultural practices often do not provide adequate disease control, (c) resistant cultivars are not available or not accepted in the marketplace for many diseases, and (d) certain high value crops have an extremely low tolerance for disease symptoms.
In contrast with most human medicines, most fungicides need to be applied before disease occurs or at the first appearance of symptoms to be effective. Unlike with many diseases of humans and animals, applying fungicides cannot heal symptoms already present, even if the pathogen is killed. This is because plants grow and develop differently than animals. Fungicides typically only protect new uninfected growth from disease. Few fungicides are effective against pathogens after they have infected a plant. Those that do have “curative” properties, which means they are active against pathogens that have already infected the plant, have limited ability to do so, often only being active on a pathogen within a few days of infection.
Many fungicides have targeted activity that imparts high efficacy against specific pathogens, which means low potential for toxicity to humans and other organisms, but also results in a high risk of pathogens developing resistance to the fungicide. A resistant pathogen is less sensitive to the action of the fungicide, which results in the fungicide being less effective or even ineffective. Fungicides that are designed to target specific enzymes or proteins made by fungi do not damage plant tissue, thus they can penetrate and move inside leaves enabling curative properties and increasing the amount of plant tissue protected to more than just where fungicide was deposit when applied. Since the mode of action of these fungicides is so specific, small genetic changes in fungi can overcome the effectiveness of these fungicides and pathogen populations can become resistant to future applications. Disease management strategies that rely heavily upon curative application of fungicides often lead to more resistance problems due to (a) the large size of the pathogen population when the application is made from which resistant individuals are being selected and (b) the difficultly in eradicating a pathogen entirely from inside the plant. Fungicide resistance is covered in more detail in a separate section.
Growers often use disease forecasting systems or action thresholds, when these are available, to ensure fungicides are applied when needed and to avoid the expense and possible environmental impact of unnecessary applications. Forecasting systems have been developed for a number of diseases based on an understanding of the environmental conditions favorable for their development. Typically these are based on temperature and relative humidity or leaf wetness in the area where the crop is grown. Threshold-based fungicide programs involve routinely scouting the crop for symptoms, then applying fungicides when the amount of symptoms reaches a critical level beyond which the disease cannot be controlled adequately. An example of a critical level is one disease spot per five leaves examined. Knowledge of the disease cycle of the pathogen is important when developing and using forecasting systems and thresholds. Important aspects of the disease cycle include whether the disease is monocyclic (one generation per year) or polycyclic (multiple generations) and latent period (time between infection and symptom expression).
Economics often influence the choice of fungicide and application timing. Expensive fungicides and numerous applications are used on valuable plantings that might incur substantial economic loss in the absence of treatment, such as fruit trees and golf courses. Recognizing that with some diseases crop yield is not impacted when severity is low, an economic threshold is used to determine when fungicide treatment is needed. The crop tolerance level, or damage threshold, can vary depending upon the stage of the crop development when attacked, crop management practices, location and climatic conditions.
Fungicides are applied as dust, granules, gas, and, most commonly, liquid. They are applied to:
Fungicides are used as a formulated product consisting of an active ingredient plus inert ingredients that improve the performance of the product. Fungicides are typically mixed with water then applied by spraying. Application equipment ranges from small hand-held and back-pack sprayers to large spray units carried by tractors or aircraft (Figures 16-22). A few fungicides are applied as dusts. Fungicides can also be applied in greenhouses as smoke, mist, fog or aerosol. Coverage of all parts of the plant susceptible to the disease is critical because very few fungicides can move adequately throughout a plant. Advancements are continually being made to nozzles and sprayers to improve coverage (Figures 17 and 19).
For many diseases, effective control necessitates multiple applications of fungicides, sometimes as frequently as every 5 days. Repeated applications are needed to protect new growth and to replace fungicide lost from the plant by chemical decomposition, UV-light degradation, and erosion by wind and water.
Fungicides are categorized in several ways based on different characteristics. The most common characteristics used and the categories are described below. Table 1 (Adobe Acrobat PDF) is a list of selected fungicides currently registered in the United States that represent the major fungicide groups and chemistry within these groups.
Fungicide resistance is a stable, heritable trait that results in a reduction in sensitivity to a fungicide by an individual fungus. This ability is obtained through evolutionary processes. Fungicides with single-site mode of action are at relatively high risk for resistance development compared to those with multi-side mode of action. Most fungicides being developed today have a single-site mode of action because this is associated with lower potential for negative impact on the environment, including non-target organisms.
When fungicide resistance results from modification of a single major gene, pathogen subpopulations are either sensitive or highly resistant to the pesticide. Resistance in this case is seen as complete loss of disease control that cannot be regained by using higher rates or more frequent fungicide applications. This type of resistance is commonly referred to as “qualitative resistance”.
When fungicide resistance results from modification of several interacting genes, pathogen isolates exhibit a range in sensitivity to the fungicide depending on the number of gene changes. Variation in sensitivity within the population is continuous. Resistance in this case is seen as an erosion of disease control that can be regained by using higher rates or more frequent applications. Long-term selection for resistance in the pathogen by repeated applications may eventually result in the highest labeled rates and/or shortest application intervals not being able to adequately control the disease. This type of fungicide resistance is commonly referred to as “quantitative resistance”. Comments about resistance risk of fungicides are included in Table 1 (Adobe Acrobat PDF) and in a table of fungicides at the FRAC web site (http://www.frac.info/frac/).
Fungal isolates that are resistant to one fungicide are often also resistant to other closely-related fungicides, even when they have not been exposed to these other fungicides, because these fungicides all have similar mode of action. This is called cross resistance. Fungicides with the same Group Code are likely to exhibit cross resistance. Occasionally negative cross resistance occurs between unrelated fungicides because the genetic change that confers resistance to one fungicide makes the resistant isolate more sensitive to another fungicide.
Managing fungicide resistance is critically important to extend the period of time that an at-risk fungicide is effective. The primary goal of resistance management is to delay its development rather than to manage resistant fungal strains after they have been selected. Therefore, resistance management programs need to be implemented when at-risk fungicides first become available for commercial use. The objective of resistance management is to minimize use of the at-risk fungicide without sacrificing disease control. This is accomplished by using the at-risk fungicide with other fungicides and with non-chemical control measures, such as disease resistant cultivars, in an integrated disease management program.
It is critical to use an effective disease management program to delay the build-up of resistant strains. At-risk fungicides should be used at the manufacturer’s recommended rate (full rate) and application interval. Using full rates is expected to minimize selection of strains with intermediate fungicide sensitivity when resistance involves several genes (quantitative resistance). At-risk fungicides should be used in alternation with other at-risk fungicides with different modes of action or different chemical groups, and they should be combined or alternated with fungicides that have a low resistance risk.
When one crop could serve as a source of inoculum for a subsequent crop, the alternation scheme among at-risk fungicides should be continued between successive crops such that the first at-risk fungicide applied to a crop belongs to a different cross-resistance group than the last at-risk fungicide applied to the previous crop. Some at-risk fungicides are formulated as premix products with other fungicides to manage resistance. At-risk fungicides should be used only when needed most. The most critical time to use them for resistance management is early in an epidemic when the pathogen population is small. Multi-site contact fungicides should be used alone late in the growing season, where they have been shown to provide sufficient disease control to protect yield. Another important component of resistance management is assessing disease control and reporting any loss of efficacy potentially due to resistance.
To promote resistance management, companies registering fungicides are voluntarily putting on the labels guidelines developed recently by EPA through a joint effort with the Canadian Pest Management Regulatory Agency (PMRA) under the North American Free Trade Agreement (NAFTA). These are described in Pesticide Registration (PR) Notice 2001-5 (www.epa.gov/opppmsd1/PR_Notices/pr2001-5.pdf). Group codes for designating chemical groups were developed as part of these guidelines (see Table 1 (Adobe Acrobat PDF)).
Legislation and Public Health
The two major laws governing fungicides and other pesticides in the United States are the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA), and Federal Food, Drug, and Cosmetic Act (FFDCA).
FIFRA was passed by Congress in 1947. Primary responsibility for its enforcement was initially with the United States Department of Agriculture (USDA), then transferred to the EPA in 1970. The Office of Pesticide Programs of EPA is chiefly responsible for regulating pesticides today. All pesticides must be registered before they can be sold and used in the U.S. unless their active and inert ingredients are deemed sufficient low risk to not require FIFRA regulation. To obtain registration, manufacturers of a pesticide must demonstrate that it does not have the potential to cause an adverse impact on the environment or non-target organisms, including people. This requires conducting several defined toxicology tests and investigating environmental fate. Additionally, the EPA must ensure that no endangered or threatened species or their habitat are harmed through use of registered pesticides. This assures compliance with the Endangered Species Act (ESA) of 1973 which prohibits any action that can adversely affect these species. In addition to federal registration with EPA, all pesticides must be registered with appropriate agencies in each state before they can be used.
FFDCA regulates the establishment of pesticide tolerances, which are the maximum permissible level of pesticide residues allowed in or on commodities for human food and animal feed. Manufacturers must include residue data in their registration materials. The Delaney Clause to FFDCA prohibited the presence in food of additives, including pesticides, considered carcinogenic. While well-intended, implementing this amendment became difficult as technology improvements enabled detection of additives at extremely low concentrations that were well below the dose necessary to cause cancer. Paradoxically, alternative pesticides could be allowed although they posed higher risks, if these were non-cancer risks. The Food Quality Protection Act (FQPA) passed in 1996 replaced the Delaney Clause with a new health-based standard for evaluating food-use pesticides that includes a ‘reasonable certainty of no harm’ provision. Under the new standard, EPA establishes tolerances by considering (a) aggregate exposure to a pesticide from food as well as residential and other non-food uses, (b) cumulative effects to human health from other pesticides with a common mode of toxicity, (c) potential of increased sensitivity of infants and children as compared to adults, and (d) effect of the pesticide on estrogen and the endocrine system. EPA is reevaluating all existing pesticide tolerances under FQPA. As a consequence of FQPA and stricter EPA standards for pesticide registration, some older pesticides are not being re-registered and it is more difficult to register new products.
A pesticide label is a legal document. Therefore it is against federal law to apply a pesticide in a manner other than that described on the label, such as using a higher rate or shorter application interval. Federal law requires specific information be included (pep.wsu.edu/factsheet/understanding.htm) (http://www.epa.gov/grtlakes/). Labels for fungicides registered in the USA are accessible on-line (www.cdms.net/manuf/manuf.asp)(www.epa.gov/pesticides/pestlabels). Figure 23 is a fictitious example fungicide label with the type of information found in most labels.
Pesticide applicators are affected by additional regulations as well, including the Worker Protection Standard (WPS). Some pesticides are considered restricted and consequently can only be applied by certified applicators who have passed an exam demonstrating an understanding of pesticides and safety (www.epa.gov/pesticides/health/worker.htm).
Additional information on pesticide regulations is available on-line (www.epa.gov/pesticides/regulating/index.htm). Information on potential hazards associated with a pesticide and directions for safe use are provided on the label and in its Material Safety Data Sheet (MSDS). An MSDS is required for all chemicals considered hazardous as defined by the U.S. Government's Occupational Safety and Health Administration (OSHA). MSDSs include information on physical data (melting point, boiling point, flash point etc.), toxicity, health effects, first aid, reactivity, storage, disposal, protective equipment, and spill/leak procedures (www.ilpi.com/msds/faq/parta.html#whatis).
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I thank V. Morton for providing input throughout the preparation of this paper. I also thank M. Braverman, S. Broscious, H. Chen, J. Huether, R. Kaiser, S. Matten, M. Mahoney, and N. Ragsdale for reviewing drafts of this work and M. Daughtrey, G. Geitz, J. Hartman, S. A. Johnston, D. Rosenberger, P. Shoemaker, and P. Vincelli for providing figures.