Alternative Treatments for Turf Disease

Fungicides are a critical tool for controlling fungus-incited diseases on amenity turf, as well as in commercial and residential plantings of selected herbaceous plants, shrubs and small trees. While the heaviest fungicide use occurs on intensively managed turf such as golf course greens, fungicides are also used on home lawns and, to a lesser extent, on greenhouse crops and woody plants like roses. Because these fungicides work to quickly remove disease and recover turf and ornamentals, grounds managers are often tempted to repeatedly use “the same ones that worked last time.” However, over-reliance on one or several fungicides, particularly those that attack a single site in fungal cells, has resulted in control failures due to declining sensitivity or resistance in some plant pathogenic fungi. As expected, golf courses have been the focal point of nearly all of the resistance-related control failures reported on amenity turf and ornamentals.

FUNGICIDE FAILURE

The most catastrophic control failure due to resistance in a target fungus occurred in the early 1970s with the systemic benzimidiazole fungicide benomyl. When introduced, benomyl, which interferes with microtubule formation in the nucleus, had better activity against dollar spot on cool- and warm-season turfgrasses than any other fungicide. Golf course superintendents embraced this superior product and largely abandoned other dollar spot fungicides. Within a year or two of heavy benomyl use, dollar spot control failures cropped up on golf courses across the United States. A mutation in one gene had rendered strains of Sclerotinia homoeocarpa almost immune to benomyl. Those resistant strains still make up a sizable percentage of S. homoeocarpa populations found on golf courses today. Benomyl-resistant target fungi are also cross-resistant with other benzimidiazole fungicides, such as thiophanate-methyl.

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Resistance to thiophanate-methyl was also recently identified in Colletotrichium gloeosporioides, the causal fungus of anthracnose on container-grown euonymus. Presumably, the benzimidiazole-resistant form of this fungus has been widely distributed throughout landscapes in New England.

RIPE FOR RESISTANCE

Sclerotinia homoeocarpa is one of a group of plant pathogenic fungi where selection of fungicide-resistant strains is common. Resistance to the dicarboximide fungicides, such as iprodione and vinclozolin, and demethylation inhibitors (DMIs) — a type of sterol biosynthesis inhibiting (SBI) fungicide — such as triadimefon, propiconazole, fenarimol and myclobutanil, has also been reported. Resistance to one dicarboximide or DMI fungicide almost always results in cross-resistance with other fungicides that have the same mode of action. Resistance to two or three of the above fungicide groups has been identified in S. homoeocarpa collected from a few golf courses. As is the case with the benzimidiazole-resistant strains, the dicarobximide and DMI-resistant populations, which are nearly as fit as the wild type S. homoeocarpa, will persist without the selective pressure from these fungicides.

Resistance in other fungi has been reported to dicarboximide fungicides. As few as six applications of recommended rates of iprodione have resulted in the appearance of resistant strains of Microdochium nivale, the causal agent of pink snow mold. This fungus has developed resistance to benzimidiazole fungicides, as well. Although few resistance-induced control failures with dicarboximide fungicides have been noted on ornamentals, resistance to iprodione in Botrytis cinerea, the causal fungus of grey mold on landscape and greenhouse floral crops, is widespread.

Unlike other fungicide groups, control failures due to resistance are relatively rare for DMI fungicides such as fenarimol, myclobutanil, propiconazole, triadimefon and trifloxystrobin. With the exclusive use of one or more DMI fungicides, the target fungal population gradually shifts from highly sensitive to a level of insensitivity that results in the recommended rates failing to give effective disease control. Of course, the more often you apply a DMI fungicide, the faster this shift in sensitivity occurs. Given the intensive disease control programs on bentgrass and annual bluegrass greens, the appearance of a highly tolerant or resistant strain of an adaptive fungus like S. homoeocarpa took only a few years.

Resistance to the DMI fungicide propiconazole was recently identified in S. homoeocarpa isolates taken from several locations in Georgia. These isolates were cross-resistant with other DMIs except for triadimefon. Dependence on DMI fungicides to control pink snow mold will result in appearance of DMI-resistant strains of M. nivale. Due to limited exposure, no problems with DMI-resistance in fungal pathogens of landscape ornamentals have been observed. However, powdery mildew fungi have a history of quickly becoming tolerant to this class of fungicides.

The strobilurin [QoI] fungicides azoxystrobin, pyraclostrobin and trifloxystrobin are equally as likely as a benzimidiazole fungicide to suffer from a catastrophic resistance-induced control failure. Fungal strains that develop resistance to one strobilurin fungicide will be cross-resistant to all of them. While azoxystrobin and trifloxystrobin are ineffective against dollar spot, over-using them could accelerate the appearance of strains of S. homoeocarpa resistant to pyraclostrobin. Widespread use of strobilurin fungicides to control grey leaf spot on perennial rye grass fairways has already resulted in the appearance of resistant strains of Pyricularia grisea. Strobilurin resistance in Colletotrichum graminicola, the causal fungus of anthracnose in bentgrass and annual bluegrass, and Pythium aphanidermatum, the causal fungus of Pythium blight on bentgrass and perennial ryegrass, have also been reported. There is also a high risk that a strain of the pink snow mold fungus M. nivale with resistance to a strobilurin fungicide may appear.

With over-reliance on the phenylamide fungicides — metalaxyl and its replacement, mefenoxam — you run the risk of selecting out a resistant population of the fungi Pythium and Phytophthora. While resistant strains are most likely to appear following the intensive use of the above fungicides on greens, greenhouses and container nurseries, their occurrence has been sporadic. So far, mefenoxam, when rotated with fungicides with other modes of action, is an effective component in the near year-round Pythium blight control programs that are required to maintain bentgrass greens across the South.

REDUCED RESISTANCE

While some fungi appear prone to develop resistance to a wide range of single-site fungicides, others, for a number of reasons, remain sensitive to benzimidiazole, dicarboximide and DMI fungicides. For example, Rhizoctonia solani, the causal fungus of brown patch on bentgrass and annual bluegrass greens, along with St. Augustinegrass and zoysiagrass lawns, can still be controlled with timely applications of the benzimidiazole, dicarboximide or DMI fungicides. After 20 years of use, iprodione remains one of the fungicides of choice for the control of Bipolaris, Exserohilum and Drechlera leaf spot as well as crown rot fungi.

Resistance to fungicides that attack multiple sites in a fungal cell is rare. Chlorothalonil and mancozeb, which are marketed under a number of trade names, continue to provide effective control of a wide range of target diseases on amenity turf and ornamentals. Among Pythium fungicides, etridiazole and chloroneb, as well as the systemic propamocarb, fosetyl Al and related phosphorous acid fungicides, remain effective and are considered very low risks for resistance-related control failures.

Fungicide control failures not always can be blamed on resistance. They are often caused by other factors relating to the time of disease identification and onset; weather patterns; fungicide specificity and placement; application rate and timeliness; residual activity in the target zone; and a variety of cultural practices. These factors also can influence selection pressure on at-risk fungicide groups.

AVOIDING RESISTANCE

While it is a little late to worry about benzimidiazole, dicarboximide and possibly phenylamide resistance, there is still time to avoid resistance-related control failures to the DMI and particularly strobilurin fungicides. Establishment of disease-resistant cultivars of ornamentals and turfgrasses, particularly those prone to attack by fungi that are likely to develop fungicide resistance under intense management, is the first step in the development of a comprehensive disease management program. Use best management practices to promote plant health and minimize stress, while altering the environment at vulnerable sites to delay or suppress disease onset.

Guidelines for resistance avoidance for dicarboximide, DMI, phenylamide and strobilurin fungicides have been established by the Fungicide Resistance Action Committee (FRAC). You can find these guidelines on the Internet at www.frac.com. You should apply these fungicides on a preventative and not a curative or rescue basis. When a disease like Pythium blight is active, one or more applications of a multi-site, low-risk fungicide is your best option. On golf courses, use a disease advisory to improve application timing and limit the number of applications of at-risk fungicides. If an advisory is not available, do some research so that you're familiar with weather patterns that favor disease onset, and initiate a preventative treatment program when necessary.

Strobilurin and DMI fungicides, when applied alone, must not make up any more than ⅓ or ½, respectively, of the total number of applications in your disease management program. As a general rule, make no more than two consecutive applications of a strobilurin fungicide at any time, regardless of the target disease. When tank-mixed with a fungicide with a different mode of action, the total number of applications of a strobilurin fungicide may not exceed ½ of those made to a particular site during a production cycle or year. Although tank-mix combinations of a DMI with an unrelated fungicide may make up more than ½ of total fungicide applications, limiting the number of DMI applications, particularly to greens to control dollar spot and pink snow mold, will enhance their longevity. To facilitate the use of resistance-suppressing tank-mix combinations, you can implement formulations of thiophanate methyl or one of several DMI fungicides with chlorothalonil, flutolanil or thiram. To reduce selection pressure, use the recommended rates of these fungicides at proper treatment intervals. Increase application rates or shorten treatment intervals as needed to prevent disease development. Target the use of an at-risk fungicide just before onset and then rely on a multi-site fungicide when pathogen activity is low. You can also apply the above guidelines to reduce your risk of selecting phenylamide and dicarboximide-resistant fungal strains.

FOLLOW UP

Strobilurin and DMI fungicides have proven highly effective in controlling a wide range of destructive diseases on amenity turf and ornaments. However, the use of these fungicides will be greatly restricted if you do not follow the above guidelines for avoiding the selection of DMI- and strobilurin-resistant plant pathogenic fungi. I encourage you to monitor the success of your disease management programs that employ at-risk fungicides and report suspected resistance to your state's extension plant pathologist.

Austin Hagan is an extension specialist and professor at Auburn University (Auburn, Ala.).

RESISTANCE RISK CLASSIFICATION FOR SELECTED SINGLE-SITE INHIBITORY FUNGICIDES
Fungicide Class Common Name Selected Trade Name(s)
High Risk
benzimidazole thiophanate-methyl Cleary's 3336, OPH 6672, Systec 1998, Cavalier, Fungo, Proturf Fluid Fungicide, T-Strom
phenylamide mefenoxam Subdue Maxx, Subdue 2G, Quell
strobilurin azoxystrobin Heritage
pyraclostrobin Insignia
trifloxystrobin Compass
Moderate Risk
dicarboximide iprodione Chipco GT, Chipco 26019, Sexton, Proturf Fungicide X
vinclozolin Curalan, Touche
DMI (sterol biosynthesis inhibiting) fenarimol Rubigan
myclobutanil Eagle, Systhane
propiconazole Banner Maxx, Spectator, Propiconazole Pro
triadimefon Bayleton T/O, Proturf Fungicide VII, LESCO Granular Turf Fungicide
Low Risk
phosphonate fosetyl-Al Aliette WDG, Aliette Signature, Prodigy
phosphorous acid Potassium salts of phosphorous acid Alude
carbamate propamocarb Banol

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