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Above: Dollar spot trial on bentgrass turf at the University of Illinois. Photos courtesy: Randy Kane. Below: Heavy dollar spot in bentgrass fairway. 18 sporfsTURF

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Above: Dollar spot trial on bentgrass turf at the University of Illinois. Photos courtesy: Randy Kane.Below: Heavy dollar spot in bentgrass fairway.

18 sporfsTURF

DevelopmentOf FungicideResistance OnIntensivelyManagedTurf

By R. T. Kane And H. T. Wilkinson,Chicago District Golf Association And University Of Illinois

Golf course greens, tees, fairways are undoubtedly the mostintensively managed turf areas in the U.S., although somesports fields are approaching this level of management.

Disease control on these intensively managed turf areas isachieved primarily through application of fungicides. In fact,statistics show that golf greens receive the greatest fungicideinput per surface area of any U.S. crop, and the dollar value ofthe turffungicide market is greater than for any other U.S. crop.Because of this intensive use pattern, fungicide resistanceproblems often show up on golf turf prior to any other crop appli-cation.

Fungicide resistance on golf turf is a fairly hot topic right now,primarily because of recent reports of dollar spot control fail-ures with the newer systemic fimgicides. However, fungicide resis-tance is not a new problem. Benzimidazole fungicides were intro-duced in the late 1960s; these products were the first widely usedsystemic fungicides, which displayed excellent long term pre-ventative activity on a number of diseases. Disease control wasso good with this revolutionary new chemistry that widespread,repeated, and intensive use of benzimidazole derivatives insued.

continued on page20

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Fungicide Resistancecontinued from page 19

Subsequent reports of dollar spot("Sclerotinia") control failures with beno-myl surfaced by 1973-74, about fouryears after registration.

The purpose of this article is to bringeveryone up to date on current system-atic fungicide use patterns and modes ofaction, fungicide resistance problemswe have observed in illinois and aroundthe ~idwest, and current thinkingregarding ways to best avoid developmentof a fungicide resistance problem onyour intensively managed turf.Benzimidazoles

This class of systematic fungicidesincludes benomyl (e.g. Tersan 1991)and the thiophanates (Cleary 3336,Fungo 50). When first introduced ben-zimidazoles were widely used t~ con-trol dollar spot and brown patch. Themode of action of these products is at aspecific biochemical site ("single-sitei~hibitor"), which means that only asingle gene alteration or mutation by afungal pathogen could produce reducedsensitivity, or in some cases, near immu-nity to the fungicide. Dollar spot controlfailures are the most common resis-tance problem with benzimidazoles, butwe- also have observed loss of control ofanthracnose (Colletotrichum graminicola)on Poa annua and creeping bentgrass.~b.tests show that the sensitivity to ben-zimidazoles of the resistant C. gramini-cola isolates is 100-fold less than "wild-type" isolates obtained from golf courseswhere no control problems have occurred.

Reduced sensitivity to benzimida-zoles also has been reported by other turfscientists for Microdochium nivale (pinksnow mold) and Laetisaria fusiformis (redthread). Also, in 1991 we identified a ben-zimidazole-resistant type of dollar spoton a Chicago area golf course where~se of these products was suspendedIn the late 1970s because of diseasecontrol failures. Even after more than 10years without exposure, the fungi stillmaintained their benzimidazole-resistanttraits-Leo this type of resistance isvery stable. It is also interesting to notethat there (apparently) have been noreports of Rhizoctonia brown patch resis-tance to benzimidazoles. Perhaps the ben-z~midazol~ fungicides have multipleSIteS of act~on against Rhizoctonia fungi,thus making genetic changes towardfungicide resistance more difficult.Phenylamides

This special class of fungicides is tar-gete~ at Phycomycote fungi includingPythium and Phytophthera species, and

20 sporfsTURF

includes metalaxyl (Subdue, Apron).Metalaxyl was introduced to the turfmarket in the late 1970s as the firstsy.stemic fungicide to control Pythiumblight, and has been widely used since.The first report of disease control failuredue to fungicide resistance was in 1984.We have documented one case of meta-laxyl resistance in Illinois, in 1988.Laboratory tests again showed a near 100-fold decrease in sensitivity of Pythiumaphanidormatum taken from the failuresite as compared to wild-type isolates.

Inthelasttwoyear~we have had our first

reports of controlfailures with DMlon

turf in the U.S.Like benomyl, metalaxyl is a single-

s~te inhibitor that can be overcome by asIng~e gene change in a developingPythium population. In some cases it isbelieved that the population shift towardinsensitivity is not due to a newly occur-ring mutation, but to selection over timeof an already existing resistant genotypethat was present in a very low percent-age of the population.

Keep in mind that we have seen onlyone true case of metalaxyl resistance inlllinois over the 10 or so years of the prod-uct's use. Most disease control "fail-ures" with this product can be attribut-ed to one of the following: application ratesare too low for a certain disease pressure·application is made too late (metalaxylworks best on a preventative basis witha 48-hour lead time); or, interval timebetween applications is too long.

On a related note, there are two fair-ly new systemic fungicides for control ofP;Ythium blight-propamocarb hydrochlo-ri de (Banol) and fosetyl-aluminum(Aliette). So far, we have seen no reportsof fungicide resistance or loss offield con-trol with these products, althoughSanders and coworkers at Penn State~ave induced resistance to fosetyl-AlIn the laboratory. The models of actionof both may be such that field resis-tance is unlikely.Demethylation Inhibitors (DMIs)

This broad class of fungicides includethe triazole derivative systemic fungicidessuch as triadimefon (Bayleton), propi~conazole (Banner), and myclobutanil(Systhane or Eagle). Also included arepyrimidine-methanol derivatives such asfenarimol (Rubigan). The site of actionin sensitive fungi is the biochemicalpathway for synthesis of a fungal sterol

called ergosterol, so you may see this classof fungicides referred to as sterol biosyn-t~esis inhibitors (SBIs) or ergosterolbiosynthesis inhibitors (EBIs). It is nowknown that toxicity to fungi stems frominhibiting demethylation of ergosterol pre-cursors, thus the name "demethylationinhibitors." .

DMI fungicides are considered tohave a single-site (or perhaps two-site)mode of action. This would seem to putthese products at the same risk level forresistance development as benzimidazolesor phenylamides. However, until recent-ly there were very few reports of field resis-tance to DMIs. Reports of reduced effec-tiveness of DMIs have appeared on anumber of agricultural and fruit crops-primarily from Europe where DMI useis more intensive.

In the last two years, we have had ourfirst reports of control failures withDM.I ~n turf in the U.S. The culpritagam IS dollar spot. In the Chicago area,we have documented one golf coursesite where DMI products have graduallylost there effectiveness in controllingdollar spot. The level of control on affect-ed fairways is now totally unaccept-able. Laboratory tests of dollar spot iso-lates from this site indicate that thedecrease in fungicide sensitivity is fair-ly low (lO-fold), i.e. the fungi havebecome "tolerant" of the fungicide, nottotally resistant as with benzimida-zoles. We may see development of moreof a problem with DMIs over the next fewyears, if use patterns don't change (moreabout this later).

Another important aspect of DMIuse on golf courses is application ofgrowth retardants such as paclobutra-zol (TGR) and flurprimidol (Cutless).~ac.lobutrazol is a triazole compoundsimilar to the triazole fungicides, and flur-primidol is a pyrimidine-methanol deriva-tive similar to fenarimol. The mode ofaction of these growth retardants isalso very similar to the fungicides; theyare sterol biosynthesis inhibitors. Plantgrowth rates are reduced by inhibitingsyntheses of the hormone gibberellin, atype of sterol molecule found in plants.Repeated use of DMI fungicides andgrowth retardants on fine turf can haveseveral consequences. One is possibleadverse effects on health of desirable grassspecies from an overdose of DMIs.Phytotoxicity, increased or prolongedgrowth suppression, increased coarsenessor steminess, and increased susceptibilityto certain diseases have all been observed.Dicarboximides

This class of fungicides includes theturf fungicide iprodione (Chipco 26019)

and vinclozolin (Vorlan, Curalan). Theseproducts are broad spectrum and gen-erally regarded as contact fungicides,although they have been shown to havesome systemic activity. The mode ofaction of these products is not wellknown, but they are usually consideredalong with single-site inhibitors. Fieldresistance to these fungicides has beenobserved for a number of years on fruitand vegetable crops, and a few reportsof dollar spot and pink snow mold resis-tance have appeared in the turfgrass lit-erature. We have not observed any resis-tance problems with these fungicidesin Illinois.Avoiding Resistance Problems

Fungicide resistance usually resultsfrom repeated long-term use of a systemicfungicide to control a particular targetdisease. For benzimidazoles and pheny-lamides, resistance may develop in as lit-tle as two to three years of repeateduse. We have seen resistance develop inIllinois in as little as three years with met-alaxyl, while development of DMI resis-tance dollar spot was observed aftereight years of frequent (though notexclusive) use.

The current thinking is that to avoidresistance, single-site inhibitor systemicfungicides should be tank-mixed or alter-nated with multi-site inhibitor contactfungicides such as chlorothalonil (Daconil2787) or anilazine (Dyrene), Anotherapproach is to tank mix or alternatesingle-site systemics with differentmodes of action. Mixing or alternatingproducts within one class of fungicides(e.g. DMIs) will not provide any pro-tection. In most cases, this would bethe same as applying one fungicide overand over. Also, cutting application ratesand extending application intervals--espe-cially in times ofheavy disease pressure--may contribute to more rapid develop-ment of resistance.

Perhaps of even greater importancein avoiding disease problems and devel-opment of fungicide resistance is theidea of using overall disease managementstrategies (IPM) instead of thinkingonly in terms of fungicide management.Use of IPM strategies that take intoconsideration the overall health of yourturf can go a long way toward reducingyour dependance on fungicides. Diseasepressures can often be reduced by: main-taining adequate and balanced fertility;controlling irrigation amounts and tim-ing; improving localized climates throughsubsurface drainage, aerification, andincreasing air movement and sun pen-etration; and, reducing cultural (man-agement) stresses-for example by rais-

ing cutting heights, reducing mechani-cal wear, etc.

The current climate is poor for devel-opment of new fungicides to replaceolder products that fail registration or loseeffectiveness. Older, multi-site contactfungicides may fall by the wayside. It isimportant that all turf managers reex-amine their fungicide use patterns anddisease control strategies, and be morewilling to use alternative controlmethods. 0

Editor's Note: Dr. Randy Kane is theturfgrass advisor for the ChicagoDistrictGolf Association and an adjunct assis-tant professor of plant pathology at theUniversity of Illinois in Urbana-Champaign. Dr. Hank Wilkinson is anassociate professor of turfgrass pathol-ogy at UIUC. Both earned their plantpathology Ph.D.s from Cornell University.

August, 1992 21