Best managementpractices foranthracnose on annualbluegrass turfAlthough our understanding of anthracnose disease on Poaannua greens is incomplete, several cultural and managementpractices can reduce its occurrence and its severity.

••• •• •• •• •• •

Anthracnose (caused by Colletotrichum cere-ale) is a destructive fungal disease of weakenedturf that occurs throughout the U.S., Canada andWestern Europe (15) and is particularly severe onannual bluegrass (Poa annua). The frequency andseverity of anthracnose epiphytotics on golf coursegreens has increased over the past decade (13,14)and is thought to be associated with some of themanagement practices used by superintendents toimprove playability and ball-roll distance. Com-binations of management factors may be enhanc-ing the severity of this disease.

Scientists within the NE-1025 multi state turfresearch project are studying the biology, ecologyand management of anthracnose of annual blue-grass turf on golf courses. They are examining thebiology of the pathogen, assessing fungicidal con-trol and fungicide resistance development, evalu-ating the effect of cultural practices on anthrac-nose severity and developing annual bluegrassand bentgrass selections for resistance to this dis-ease. Completed and ongoing field trials withinthis five-year project (2005-2010) have evaluatedregistered and experimental fungicides, fungi-cide programs and annual bluegrass managementpractices, including nitrogen fertility, chemicalgrowth regulation, mowing, rolling, topdressing,verticutting and irrigation as well as the potentialinteraction among practices. Ultimately, resultsfrom these experiments will be used to devise acomprehensive set of best management practicesfor the control of anthracnose disease on golfcourses.

Host susceptibilityAnthracnose can be found on cool- and warm-

season turf in roughs, fairways and tees, but oftenthe disease is most destructive on annual bluegrassmaintained at a putting green height of cut. Out-breaks are also increasingly common on creepingbentgrass (Agrostis stolonifera) and may develop onother cool-season turf species including ryegrasses(Lolium species), fescues (Festuca species), Ken-tucky bluegrass (Poa pratensis) and velvet bent-grass (A. canina).

Although the disease is often most severe dur-ing warm weather, outbreaks may occur through-out the year, causing either a foliar blight or a basalrot of leaf sheaths, crowns and stolons (15).

Anthracnose is often present on turf mowedat a higher height without producing severe dam-age, which suggests that plant health (vigor andstress) is a major factor that determines diseaseseverity. The disease can cause extensive injury onturf maintained at low fertility, very low mowingheights or turf grown under suboptimal conditions(drought stress, excess shade, high humidity).

The greater susceptibility of annual bluegrassto anthracnose is probably related to a number offactors including the weak perennial nature of thisgrass species. Annual bluegrass is well known forits prolific seedhead (flowering) expression thatoccurs predominantly in the spring (April throughearly June). Seed head development requires con-siderable metabolic energy, which reallocates pho-tosynthate away from roots and shoots towardseedheads just before the most stressful time of

James Murphy, Ph.D.Frank Wong, Ph.D.Lane Tredway, Ph.D.Jo Anne Crouch, Ph.D.John InguagiatoBruce Clarke, Ph.D.Tom Hsiang, Ph.D.Frank Rossi, Ph.D.

August 2008 GeM 93

••• •• •• •• •• •

the growing season. Summer stress tolerance hasbeen associated with increased root depth andnumber; thus, the reallocation of photosynthateaway from roots and crowns probably weakensannual bluegrass and increases its susceptibility toanthracnose. Breeding for improved tolerance toanthracnose disease is one objective of the annualbluegrass breeding program in Pennsylvania andthe bentgrass breeding program in New Jersey.

The true causal agent ofanthracnose on cool-season turf

For more than 90 years, the pathogen respon-sible for turfgrass anthracnose was known by thesame name as the fungus that causes anthracnosedisease in corn, Colletotrichum graminicola G .W.Wils., because the pathogens so closely resemble

lone another. Recent DNA fingerprinting studies,however, indicate that the pathogen responsiblefor anthracnose in cool-season turf, while closelyrelated to the corn pathogen, is a distinct fungalspecies, C. cereale Manns (5). Thissame fungushas been found across North America coloniz-ing numerous cool-season grasses in field crops,prairies, residential lawns, ornamental grassesand other environments (4,5). Outside of thegolf course environment, it appears that C. cere-ale rarely induces disease because the fungus cancolonize other host plants with9ut causing visibledamage.

Annual bluegrass putting green turf shows initial symptoms of anthracnose. Photo courtesy of B. Clarke

94 GeM August 2008

Even though C. cereale can be found on manycool-season grasses, DNA fingerprints of individ-ual isolates collected from North America, Japan,Australia and Europe indicate that this fungus issubdivided into groups of host-specific popula-tions (4,5). With few exceptions, turf grass patho- .gens are members of different populations of C.cereale than those found on other grass hosts. Inaddition, the populations of C. cereale infectingannual bluegrass are distinct from the populationsthat infect creeping bentgrass. Such host-speci-ficity is illustrated on golf courses by the appear-ance of the disease on one grass species at a timein mixed swards of annual bluegrass and creep-ing bentgrass (15). Although anthracnose can befound on many plants, the host specificity of Col-letotrichum species indicates that stands of non-turf grass hosts are not likely to harbor strains thatcould cause anthracnose on turf grasses.

Research with DNA fingerprinting indicatesthat C. cereale does not inhabit warm-seasongrasses (4). Anthracnose outbreaks on warm-sea-son turfgrass, caused by other species of Colletotri-chum, are rare and typically cause little damage.

Biology and epidemiologyBecause the anthracnose pathogens on turf and

certain field crops were thought to be the sameorganism throughout most of the 20th century,much of the ecology, epidemiology and pathogenicprocess of Colletotrichum cereale are inferred fromresearch on corn and sorghum. There appear to beenvironmental and host factors that promote bothanthracnose foliar blight and basal rot in cool-sea-son turfgrasses, but these are poorly understood.In addition, the increase in anthracnose disease onturf during the past decade has given rise to specu-lation that more virulent strains of C. cereale mayhave emerged; however, no research data support-ing this hypothesis have been reported. Althoughannual bluegrass has been successfully inoculatedwith C. cereale in the field, detailed studies of thebiology of t,his path~gen have been hindered, inpart, because a reliable method for infecting turfunder controlled conditions in the greenhouse andgrowth chamber is lacking. Such studies are cur-rently being conducted by NE-I025 scientists, butdefinitive results have yet to be published.

Symptomology and the disease cycleOn .annual bluegrass, symptoms first 'appear

as orange to yellow-colored spots that range from0.25 to 0.5 inch (0.64-1.3 centimeters) in diam-eter. As the disease spreads, spots may coalesceinto large, irregularly shaped areas of infected turfon greens, tees and fairways. Older or senescing

leaves are often colonized first, resulting in yel-low leaf lesions. In close-cut turf, the lower stemsmay become affected, resulting in water-soaked,blackened tissue that is easily pulled from infectedcrowns.

Infested foliar or stem tissue are often coveredwith numerous acervuli (reproductive structures)with distinctive black spines (setae) that are used asdiagnostic features for disease identification. Fromthese acervuli, the pathogen produces massesof reproductive spores called conidia that can bespread by water or mechanically (foot traffic, mow-ing, etc.) to healthy plants. Once in contact witha susceptible plant, spores germinate to producehyphae and a specialized structure known as anappressorium that adheres to the host tissue, allow-ing the fungus to penetrate into the plant (12).Based on studies of corn and sorghum, C. cerealeis thought to overwinter in turf as dormant restingstructures called sclerotia or as fungal mycelium ininfected plant debris.

Temperature required for infectionAnthracnose foliar blight is generally favored

by higher temperatures (85 F-95 F [29.4 C-35C)) in the summer and autumn. However, basalrot symptoms can be observed year-round, oftenoccurring simultaneously with foliar blight symp-toms during periods of heat stress. Laboratorystudies indicate that some isolates of C. cerealegrow best between 70 F and 88 F (21.1 C-31.1 C)and are able to cause foliar infection between 81 Fand 91 F (27.2 C-32.7 C) (7). These observationscorrelate with summer outbreaks of foliar blightand basal rot, but do not explain the developmentof anthracnose basal rot symptoms under coolconditions (winter or spring). Additional researchis needed to ascertain the optimal temperaturesrequired for infection by cool-weather strains ofthis pathogen.

••• •• •• •• •• •research

Colletotrichum cereale colonizes older senescing leaves of annual bluegrass. Photo courtesyof J. Inguagiato

Acervuli with setae on leaf sheath. Photos courtesy of T. Hsiang

Germinating anthracnose conidium produces an appressorium on plant tissue.

Anthracnose management:chemical control

Research and experience indicate that pre-ventive fungicide applications are far more effec-tive than curative applications for the control ofanthracnose on putting greens. However, becausewe lack knowledge regarding the disease cycle andepidemiology of anthracnose, the best timing forpreventive applications remains unknown. Gen-erally, it is recommended that superintendentsinitiate a preventive fungicide program at leastone month before the normal onset of anthrac-nose in their area.

Fungicides belonging to eight chemical classesare currently available for anthracnose control:

15 microns-

August 2008 GeM 95

••• •• •• •• •• •

the benzimidazoles, dicarboximides (specifically,iprodione), DMIs (demethylation inhibitors),nitriles, phenylpyrroles, phospho nates, polyoxinsand QoIs (strobilurins) (Table 1).

These products can be separated into twogroups: multi site inhibitors and single-site inhibi-tors. As the name implies, multisite inhibitorsinhibit several to many biochemical processes inthe fungal cell. In contrast, single-site inhibitorssuppress only one biochemical process. This is animportant distinction because it determines therisk of a given product for fungicide resistance;single-inhibitors have a moderate or high risk forresistance development, whereas multisite inhibi-tors generally have a low resistance risk.

Preventive versus curativeIn addition to being more effective, preventive

applications also expand the number of productsavailable for use. Of the eight chemical classes

available for anthracnose control, only thebenzimidazole, DMI and QoI classes havesignificant curative activity. The nitrile,phenylpyrrole, phosphonate and polyoxinfungicides have little to no curative activityagainst anthracnose, but are very effectivein tank-mixes or when applied on a preven-tive basis (6,17). Moreover, in New Jerseytrials, using tank-mixtures and alternat-ing among the eight che~ical groups havegenerally been more efficacious than usinga single product sequentially.

Although the benzimidazole, DMIand QoI chemistries have curative activ-ity, superintendents should not rely solelyon curative applications for anthracnosecontrol. These chemistries are also at riskfor fungicide resistance, as discussed laterin this article, and curative applicationsmay encourage resistance development in

Trade name, manufacturerResistance riskUtilityTopical mode of actionCommon name

FunQicides for anthracnose control

- -- -----I thiophanate-methylBenzimidazole acropetal penetrant preventive/curative high Cleary's 3336, Cleary Chemical

Fungo, The Scotts Co.SysTec, Regal Chemical

T-Storm, LescoDicarboxirTiTdes iprodione localized penetrant preventive moderate Chipco 26GT, Bayer

- . - Iprodione Pro, BASFDMI fenarimol acropetal penetrant preventive/curative moderate Rubigan, Gowan Co.

metconazole acropetal penetrant preventive/curative moderate Tourney, Valentmyclobutanil acropetal penetrant preventive/curative moderate Eagle, Dow AgroSciences

propiconazole acropetal penetrant preventive/curative moderate Banner Maxx, SyngentaPropiconazole Pro, Micro Flo Co.

Sawi, Regal ChemicalSpectator, Lesco

triadimefon1-_ acrop~~.Qenetrant preventive/curative moderate Bayleton, Bayer--------

triticonazole acropetal penetrant preventive/curative moderate Trinity, BASF...,...,.,., Triton, Bayer

-NTtril8---- '. chlorothalonil contact preventive low Daconil, SyngentaChloroStar, Regal Chemical

Concorde, Griffin LLCEcho, Sipcam Agro USA

- Manicure, Lesco__ Phenylpyrro!~ __•__. it- f1udioxonil contact preventive low Medallion, Syngenta

Phosphonates I fosetyl-AI true systemic preventive low Chipco Signature, BayerIl Prodigy, Lesco

phosphite salt --- true systemic preventive low Alude, Cleary ChemicalMagellan, Nufarm Americas

Resyst, Regal ChemicalVital, Phoenix Environmental Care

POlyoxlriS --- polyoxin 0 localized penetrant preventive moderate Endorse, Cleary and Arysta LifeScience- - 001-~~-

~strobin acro~9.Lpenetrant preventive/curative high Heritag~~Yi!gentafluoxastrobin acropetal penetrant preventive/curative high Disarm, Arysta LifeScience

~. pyraclostrobin acropetal penetrant preventive/curative high Insignia, BASF~i trifloxystrobin acropetal penetrant preventive/curative high Compass, Bayer

",,,..w ..'''' .,.

Chemical class

Note. This listof products and manufacturers is not intended to be complete. Other turffungicide products containing the same active ingredients may be available.

Table 1. Currently available fungicides for anthracnose control.

96 GeM August 2008

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anthracnose populations.

IComparing fungicide control

How resistance developsResistance typically results from repeated use

of fungicides from a single fungicide class and canresult in immunity or tolerance to that fungicideclass. Resistance to each fungicide class developsindependently (for example, a QoI-resistant fun-

Fungicide resistanceFungicide resistance has complicated anthrac-

nose management. Resistance has not been an issuefor multisite fungicides like chlorothalonil, but itis a concern for those with a site-specific mode ofaction. Resistance has developed in anthracnose tosite-specific fungicide classes including the Qols,benzimidazoles and DMI fungicides (21).

30

Figure 1. Comparison of phos-phonate fungicides for preventivecontrol of anthracnose on annualbluegrass (top) and creepingbentgrass (bottom) greens.All fungicides were applied ona 14-day interval in 2 gallonswater/1 ,000 square feet with acarbon dioxide-powered sprayerat 40 pounds/square inch (275.8kilopascals) using TeeJet 8004nozzles. Applications to annualbluegrass were initiated May 23,2005, and data were collectedon Aug. 15, 2005. Applications tocreeping bentgrass were initiatedJune 29, 2006, and data werecollected Aug. 6, 2006.

10 15 20 25

Anthracnose inciaence {%)5

Signature(4 ounces)

Alude(6 fluid ounces)

Daconil Ultrex(3.2 ounces)

Signature +Daconil Ultrex

(4 + 3.2 ounces)Alude +

Daconil Ultrex(6 + 3.2 ounces)

Untreated

Signature(4 ounces)

Alude(6 fluid ounces)

Daconil Ultrex(3.2 ounces)

Signature +Daconil Ultrex

(4 + 3.2 ouncesAlude +

Daconil Ultrex(6 + 3.2 ounces)

Untreated

0

Application techniquesProper application techniques are essential to

a successful fungicide program for the control ofanthracnose. Research in Pennsylvania indicatesthat fungicides should be applied in 2 gallons ofwater/1,000 square feet (81.5 milliliters/squaremeter) using nozzles that produce medium tocoarse droplet sizes. Applications in lower watervolumes or using extremely coarse droplet sizescan significantly reduce fungicide performance.

PhosphonatesAlthough primarily used to control Pythium

diseases, the phosphonates have recently beenshown to be very effective against anthracnosewhen used preventively. Fosetyl-Al, released inthe early 1980s, was the first phosphonate fungi-cide labeled for use on turf. Originally marketedas Aliette and now sold as Chipco Signature orProdigy, fosetyl-AI is a complex molecule that isbroken down to release the phosphite ion P03' inthe plant after application.

Since 2000, a new generation of phosphonateshas been released into the turf market: the phos-phite salts. These products contain phosphite(P03') in the form of a sodium (Na+), potassium(K+) and/or ammonium (NH/) salt. Phospho-nates have direct fungicidal properties and arealso thought to reduce anthracnose by improv-ing overall turf health and stimulating hostdefense responses. The risk of fungicide resis-tance for phosphonates is considered low to mod-erate because of these potential multiple modesof action. Certain formulations of fosetyl-AIalso contain a copper phthalocyanine pigment,which imparts a green or blue-green color to theturf after application. Copper phthalocyaninesare large macrocyclic molecules that absorb andrefract light, conduct electricity and have avarietyof other biological properties. These pigments areknown to increase the overall quality of puttinggreen turf after several successiveapplications.

Research in North Carolina and Pennsylvaniahas focused on evaluating fosetyl-AI and phos-phite salts for anthracnose management. Whenapplied on a preventive basis, fosetyl-AI has pro-vided excellent control on both creeping bent-grass and annual bluegrass. Although the phos-phite salts have been very effective on annualbluegrass, these products have only providedmoderate anthracnose control on creeping bent-grass over three years of testing in North Caro-lina (Figure 1).

August 2008 GeM 97

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Figure 2. This is a simplified model of a multiple-step process over time, where repeated applica-tions of a single-site mode of action fungicide select for naturally resistant individuals from a

population. As more fungicide applications are made, the frequency of resistant survivors increases.In anthracnose populations, eventually, a high frequency of resistance can be selected for.

Figure 3. Patterns of resistance development to 001, benzimidazole and OMI fungicides. Sensitivepopulations (A, D) change in response to repeated fungicide applications over time (8, E). For Ools

and benzimidazoles, a fungicide-immune population develops that cannot be controlled at all byfungicide applications, and it completely dominates the population (C). For OMls, the population

becomes more fungicide-tolerant, but most OMI-tolerant individuals can still be controlled with high-rate applications (F). For each fungicide group, the green line represents the highest labeled rate offungicide; the proportion of the population that is sensitive to the fungicide and can be controlled isshown in the white boxes to the left, and the proportion of the population that is no longer sensitive

to the fungicide and cannot be controlled is shown in the red areas to the right. Adapted fromProfessor Wolfram Koeller, Cornell University

gal population may be sensltlve to benzimid-azoles and vice versa). Repeated applications ofthe same fungicide or fungicides from the samefungicide class over time can quickly select for ahigher frequency of resistant individuals (Figures2,3). Unfortunately, once resistance to a chemicalclass develops, it does not go away as long as theresistant isolates persist in the population, even iffungicides from that chemical class are not usedor are used sparingly in the future. Resistant iso-lates are as "fit" as sensitive ones with the addedbonus of being able to survive certain fungicideapplications.

Delaying resistanceThe development of resistance can be delayed

by limiting the number of applications from onefungicide class. Repeated sequential applica-tions, late curative applications and low-Iabel-rate applications tend to encourage the develop-ment of resistance. The use of multisite, contactfungicides is an important strategy for reducingthe overall potential for resistance developmentbecause it can reduce the total amount and num-ber of high-risk, single-site fungicide applications.Tank-mixing fungicides (especially with multi-site fungicides) may not stop resistance develop-ment, but it can prevent total control failure froma fungicide application; for example, a tank-mixof chlorothalonil with a QoI fungicide still selectsfor QoI resistance, but the chlorothalonil willcontribute to disease control of individuals thatare both resistant and sensitive to QoIs.

QoI fungicidesThe QoI fungicide azoxystrobin (Heritage)

was commercially released for use on turf in1997. Resistance of Colletotrichum cereale to theQoI fungicides (Heritage, Compass, Disarm andInsignia) developed quickly (1) and was fairlywidespread in the U.S. by 2004. QoI-resistantindividuals of C. cereale are immune and cross-resistant to all fungicides in this chemical class,even when the fungicides are applied at 10 timesstandard rates or higher.

Thus, the use of QoI fungicides for anthrac-nose control should be discontinued for locationswith a history of poor QoI performance and/orresistance confirmed by laboratory testing. Thereis no evidence that QoI resistance in fungal popu-lations will decrease over time; resistance is likelyto be permanent. However, for any given location,resistance may be localized to one or only a fewgreens. Subsequently, Qols may still be effectiveon other greens where resistance has not devel-oped. QoI fungicides can also still be used for thecontrol of other diseases (for example, Rhizoctonia

Resistant

ii.11

~ ......••..

DMI fungicidesOols and benzimidazoles

".. f(

Reproduction .~ .

~Survivor

population

98 GeM August 2008

diseases and summer patch) where the anthrac-nose pathogen has developed resistance to theQoI fungicides.

BenzimidazolesBenzimidazole fungicides have been used on

turf since the 1960s, and currently only thiophan-ate-methyl is labeled for use on cultivated grasses.Resistant isolates of Colletotrichum cereale werefound as early as 1989 in Michigan (10) and morerecently in a number of other locations through-out the U.S. (21). Like QoI-resistance, resistanceto the benzimidazoles results in complete immu-nity for individuals and is permanent in estab-lished populations of anthracnose. Benzimidazoleuse for anthracnose control should be discontin-ued at locations with a history of poor benzimid-azole performance and/or resistance confirmed bylaboratory testing.

DMI fungicidesDMIs have been used on turf grasses since the

1980s, and severalDMIs are currently availableforuse on cultivated grasses. Whereas Colletotrichumcereale can quickly develop resistance to QoI andbenzimidazole fungicides, it gradually develops atolerance to DMI fungicides, which means thatgood control may be achieved with high labeledrates or shorter application intervals. In Califor-nia, isolates that are two to 10 times more tolerantto propiconazole (for example, Banner MAXX,Syngenta) than sensitive isolates have been foundon greens, but these isolates could still be con-trolled with the high label rate (2 fluid ounces[59.1 milliliters]) of Banner MAXX when appliedat 14-day intervals (21). This suggests that patho-gens that have developed tolerance to DMIs arestill manageable with high rates ofDMIs. To bothmaintain the utility of these fungicides and mini-mize non-target effects of excessiveuse (potentialplant growth regulation), it is prudent to alternatethe DMIs with other fungicide chemistries.

Additionally, there is a clear difference in theintrinsic activity of the different DMI fungicides(22). On average, propiconazole was roughly fivetimes more toxic to C. cereale than myclobutanil(Eagle, Dow AgroSciences) and 40 times moretoxic than triadimefon (Bayleton, Bayer) in labo-ratory studies. In New Jersey fieldwork, season-long applications resulted in anthracnose sever-ity of 7.5% (Banner Maxx), 33% (Eagle) and79% (Bayleton) (17). The intrinsic activities ofnew DMIs such as triticonazole (Trinity, BASF;Chipco Triton, Bayer)and metconazole (Tourney,Valent) are being examined at this time.

The potential for resistance development to

••• •• •• •• •• •research

the DMIs can be reduced by alternating fungi-cide chemical classes, using the most intrinsicallyactive DMI (propiconazole) and applying a higherlabeled rate during cooler temperatures (phyto-toxicity or thinning can occur at high label rates

.when some DMIs are applied during high tem-peratures) to obtain the maximum disease controlwith this fungicide class.

Multisite fungicidesSince multisite fungicides have a low risk for

resistance, these are important tools in an anthrac-nose management program. Chlorothalonil usedalone or in a tank-mixture can be very effica-cious, especially when used preventively.As men-tioned above, tank-mixes can also provide betterdisease control if QoI, benzimidazole or DMIapplications are made to resistant populations orpopulations with reduced sensitivity. Since 2001,seasonal limits have been imposed for the use ofchlorothalonil on golf courses, so it is importantto conserve its use for difficult-to-control diseasessuch as anthracnose.

Other fungicidesSo far, no casesof resistance have been reported

for the other classes of site-specific fungicidesused to control anthracnose including the poly-oxins, phenylpyrroles and phosphonates. Ofthese, the polyoxins and phenylpyrroles are morelikely to have future resistance problems becauseof their mode of action, so these should be usedjudiciously.

Anthracnose management: culturalpracticesNitrogen fertility

Minimizing nitrogen fertility is one approachused by superintendents to increase ball-roll dis-tance (greenspeed) on putting green turf. However,management trials on annual bluegrass greens in

Anthracnose and nitrogen, 2004

Nitrogen intervalt

Every 28 daysEvery 7 days

tNitrogen was applied as an NH4N03 solution containing 0.1 pound nitrogen/1 ,000 square feet(0.49 gram/square meter) from May 7 to Oct. 9, 2004.

tMeans followed by different letters are significantly different from one another.

Table 2. Anthracnose disease response to nitrogen fertilization of annual bluegrass turf mowed at0.125 inch (3.2 millimeters) in North Brunswick, N.J., during 2004.

August 2008 GeM 99

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INew Jersey indicate that soluble nitrogen appliedevery seven days at a low rate of 0.1 pound/1,000square feet (0.49 gram/square meter) from latespring through summer can reduce anthracnoseseverity 5% to 24% compared to the same niteof nitrogen applied every 28 days (11) (Table 2).Additionally, fungicide efficacy for the control ofanthracnose was increased in plots that receivedanadditional 0.125 pound of nitrogen/1,000 squarefeet (0.61 gram/square meter) every 14 days fromMay through August (6). Specific mechanismsassociated with reduced anthracnose severity inplants with greater nitrogen fertility are currentlyunknown, although increased plant vigor has beenproposed (20).

Superintendents have frequently asked aboutthe potential role, if any, of late- and early-seasongranular fertilization and are seeking guidance

. on the relevance of this practice to controlling

(Anthracnose resoonse: 2004 and 20015: ~~ 1

Embark (mefluidide * Primo (trinexapac-ethyl)fiAuid ounce ,000 square feet

0 0 65.0 84.9

0 0.125 51.3 86.5

0.69 0 57.4 82.0

0.69 0.125 50.3 85.3

0 0 48.9 66.6

0 0.125 43.0 67.6

0.69 0 50.0 69.0

0.69 0.125 25.1 45.9LSD# 6.77 9.45

tNitrogen was applied as an NH4N03 solution containing 0.1 pound nitrogen/1 ,000 square feet from May7 to Oct. 9, 2004, and May 21 to Aug. 3, 2005.

*Mefluidide (Embark 0.2L) was applied as a split application of 0.69 fluid ounce/1,OOO square feet (0.22milliliter/square meter) on April 7 and 21, 2004, and April 6 and 20, 2005.

fiPrimo MAXX 1ME was applied at 0.125 fluid ounce/1,OOO square feet (0.04 milliliter/square meter) every14 days from April 7 to Sept. 22, 2004, and April 6 to Aug. 10, 2005. Initial Primo application wasdelayed on turf previously treated with Embark until April 21 in 2004 and April 20 in 2005.

#LSD (least significant difference). The difference between two means (that are within the same level asthe other two factors) must be equal to or greater than the LSD value to be considered statisticallydifferent.

Table 3. Anthracnose disease response to nitrogen fertilization, Embark and Primo application on annualbluegrass turf mowed at 0.125 inch (3.2 millimeters) in North Brunswick, N.J., during 2004 and 2005.

100 GeM August 2008

anthracnose on annual bluegrass turf. Work onanthracnose foliar blight of fairway turf indicatedthat annual nitrogen fertilization should be mod-erate (3 pounds nitrogen/1,000 square feet [14.6grams/square meter]), and a greater proportion ofthe annual nitrogen fertilizer should be appliedin autumn rather than spring to reduce diseaseseverity (8). These effects may be eXplained bya depletion of carbohydrate reserves induced byaggressive spring nitrogen fertilization and exac-erbated by low net photosynthesis during summerstresses.

Annual nitrogen rate and season of fertiliza-tion need to be evaluated for anthracnose basal rotunder putting green conditions as well as the pos-sibility of an interaction between summer appli-cations of soluble nitrogen and granular nitrogenfertilization programs. Research trials addressingthese objectives will be initiated in late summer2008 in New Jersey.

Plant growth regulatorsPlant growth regulators (PGRs) are widely

used to reduce shoot growth between mow-ing, improve shoot density, increase stress toler-ance and enhance playability of putting greensurfaces. Primo (trinexapac-ethyl, Syngenta)applied to annual bluegrass greens at 0.125 fluidounce/1,000 square feet (0.039 milliliter/squaremeter) every 14 days from May through Augustreduced disease from late June to late July (6).Other research in New Jersey from 2003 through2007 indicated that Primo or Embark (mefluid-ide, PBI Gordon) used alone had infrequent andinconsistent effects on anthracnose, but did notgreatly aggravate disease severity.Additionally, inplots where Embark and Primo were used in com-bination, anthracnose severity was reduced 6% to14% compared to plots that received only one ofthese plant growth regulators during the last twoyears of a 3-year trial (11). At advanced stages ofdisease (end of the season), the combination ofweekly nitrogen fertilization with Embark andPrimo application provided the greatest reductionin disease severity (Table 3).

Many superintendents were using chemi-cal growth regulation strategies not addressed inprevious research; thus, further assessment wasconducted from 2005 to 2007. Treatment effectsevaluated included rate (0.1, 0.125 and 0.2 fluidounce/1,000 square feet [0.03, 0.04 and 0.06 mil-limeter/square meter]) and frequency (seven ver-sus 14 days) of Primo application, and combina-tions of Primo with Embark or Proxy (ethephon,Bayer), which are commonly used to regulateseedhead development of annual bluegrass. Data

from this trial have not been completely analyzed,but it is clear that use of these growth regula-tors alone or in combination are not increasinganthracnose severity.

VerticuttingVerticutting is another common management

practice used on greens to minimize puffiness asso-ciated with thatch accumulation and to improvesurface playability. Verticutting has been reputedto enhance wounding of host plant tissue andthereby increase anthracnose severity (9,13,15).Contrary to this perception, verticutting to ashallow depth (0.1 inch [3.0 millimeters]) did nothave a substantial effect on anthracnose severityin New Jersey (11). Infection studies with Colle-totrichum in annual bluegrass and corn have dem-onstrated that wounds are not required for hostpenetration (3,16,19). However, other research-ers (18) have reported that verticutting to a 0.2-inch (5-millimeter) depth increased anthracnosein annual bluegrass. Thus, verticutting to a depththat cuts crowns and stolons (severe wounding)and removes thatch may enhance plant stress andincrease anthracnose severity,whereas verticuttingto groom (light vertical mowing) the leaf canopyappears to have little effect on disease severity.

Mowing and rolling practicesIt is well known that a lower cutting height

will increase ball-roll distance (green speed) on aputting green. Lower cutting height has also beenassociated with increased anthracnose severity (2).More frequent mowing (double- or triple~cutting)is used to increase green speed and is thought tointensify wound.ing ofleaf tissue. Moreover, light-weight rolling is used to smooth the turf canopyand improve ball-roll distance. Frequent use ofthese practices either alone or in combination wasthought to increase stress and susceptibility toanthracnose on putting greens.

As expected, research in New Jersey during2004 and 2005 found that a 0.015-inch (0.38-millimeter) increase in mowing height (0.110 to0.125 inch, or 0.125 to 0.141 inch [2.8 to 3.2millimeters, or 3.2 to 3.6 millimeters]) was suf-ficient to reduce anthracnose severity (Table 4).Contrary to expectations, increasing mowing fre-quency from a single daily mowing to double-cut-ting daily did not increase anthracnose severity,and lightweight vibratory rolling every other dayeither had no effect or slightly reduced anthrac-nose severity (Table 5).

Additional analysis of this data is under way;but it appears that the practices of double-cut-ting and rolling (rather than lowering the cutting

••• •• •• •• •• •research

tMeans followed by different letters are significantly different from one another.

Table 4. Anthracnose disease response to mowing height on annual bluegrass putting green turfin North Brunswick, N.J., during 2004.

~nthracnose and rolling, 2004

lightweight rolling

None

Every other day

tMeans followed by different letters are significantly from one another.

Table 5. Anthracnose disease response to lightweight rolling on annual bluegrass putting greenturf in North Brunswick, N.J., during 2004.

height) should be used to improve ball roll with-out intensifying anthracnose severity.

Research in New York is currently evaluatingthe possibility that mower setup including walk-behind mower design, bedknife position and fre-quency of clip may affect basal rot anthracnose.Moreover, traffic stress from maneuvering mowingand rolling equipment on the edge of greens hasbeen suggested as a potential cause of enhancedanthracnose on greens. A trial has been initiatedin New Jersey to determine whether routine mow-ing and rolling operations can affect anthracnose,depending on the location of the equipment traf-fic on a putting green, that is, perimeter (edge)or center.

Topdressing practicesTopdressing used to smooth putting surfaces

and manage thatch accumulation has been sug-

August 2008 GeM 101

••• •• •• •• •• •

Irrigation managementProper irrigation management IS critical to

maintaining plant health and the playability ofputting green turf. A trial was established in NewJersey to determine whether irrigation regime(that is, 100%, 80%, 60% and 40% of referenceevapotranspiration, ET) influences anthracnosedisease. This trial is being continued in 2008, butinitial data indicate that anthracnose severity wasincreased in plots irrigated with 40% or 60% ETocompared to turf receiving 80% or 100% ETo.Further data collection and analysis is needed todetermine the veracity of these results.

SummaryCurrently, best management practices for the

control of anthracnose disease on annual blue-grass putting green turf include implementing afrequent low-nitrogen-rate fertility program initi-ated in late spring and continuing through sum-mer. Soluble nitrogen applied every seven days at0.1 pound/l,OOO square feet (0.49 gram/squaremeter) from late spring through summer hasbeen effective at reducing disease severity. How-ever, the annual nitrogen rate and seasonal aspectof fertilization need to be further studied as wellas the possibility of an interaction between sum-mer applications of soluble nitrogen and granularnitrogen fertilization, programs.

Chemical growth regulation strategies includ-ing the use of Embark, Proxy and Primo do not

gested as contributing to anthracnose epidemics.Trials were initiated in New Jersey to determinewhether rate and frequency of sand topdressinginfluenced disease development. Initial data anal-yses indicate that sand topdressing may slightlyincrease anthracnose at early stages of the diseasebut later reduces disease severity. Light, frequentapplications (topdressing every seven or 14days at1 or 2 cubic feet/l,OOOsquare feet [304.8 or 609.6cubic centimeters/square meter]) provided themost rapid and substantial reduction of anthrac-nose. Sand topdressing every 21 or 42 days at a

, higher rate (4 cubic feet/l,OOOsquare feet [1,219.2I cubic centimeters/square meter]) also reduced dis-

ease by August in 2006 and 2007.A companion study in 2005 and 2007 assessed

whether methods of sand incorporation and sandparticle shape (that is, round versus subangular)affect disease severity.The incorporation methodsevaluated in this study (that is, stiff-bristled brush,soft-bristled brush, vibratory rolling or none) hadno effect on anthracnose. Moreover, both sandtypes at first enhanced disease in July, but con-tinued topdressing reduced disease severity laterin the season (August and September) each yearcompared to turf that was not topdressed.

Light, frequent sand topdress-ing buries and protects

crowns and leaf sheaths. Notethe depth of crowns in the

middle (1 cubic foot/1 ,000square feet/week [0.0003

cubic meter/square meter])and right (2 cubic feet/1 ,000

square feet/week [0.0006cubic meter/square meter])profile samples are greater

than the profile sample on the. left (no topdressing). Photo

courtesy of J. Inguagiato!

102 GeM August 2008

intensify disease severity and, on occasion, mayreduce severity. Relatively large reductions in dis-ease severity have also occasionally been observedwhere frequent low-nitrogen-rate fertilization iscombined with the use of seedhead suppressants(Embark or Proxy) in the spring and sequentialapplications of the vegetative growth regulatorPrimo throughout the growing season.

If it is feasible, superintendents should usedouble-cutting and lightweight rolling instead oflowering mowing heights to achieve greater ball-roll distance (green speed). Increasing mowingheight as little as 0.015 inch (0.38 millimeter) candecrease anthracnose severity, whereas daily dou-ble-cutting and lightweight rolling increase ball-roll distance and do not intensify disease. In fact,rolling may slightly reduce disease severity.

Preventive fungicide applications (generallyonemonth before the normal onset of symptoms) arefar more effective than curative applications. Thebenzimidazole, DMI, dicarboximide (iprodione),nitrile, phenylpyrrole, phosphonate, polyoxin andQol fungicide chemistries can effectively controlanthracnose, but resistance has been a problemwith several of these gro~ps. Repeated sequentialapplications of single-site (benzimidazole, DMIand Qol) fungicides, late curative applicationsand low-label-rate applications tend to encour-age the development of resistance and, therefore,should be avoided. The use of multisite contactfungicides is an important strategy for reducing ordelaying the overall potential for resistance devel-opment. Tank-mixtures and alternation of thesechemical groups are often more efficacious thansingle product applications and should be usedto reduce the potential for fungicide resistance"Recent research suggests that fungicides shouldbe applied in 2 gallons of water/1,000 square feet(81.5 milliliters/square meter) using nozzles thatproduce medium to coarse droplet sizes.

ConclusionsAlthough much has been learned about the

biology and management of anthracnose throughthis project, many questions remain unanswered.We must continue to gain a more comprehen-sive understanding of the anthracnose system onannual bluegrass and bentgrass that will enable usto develop more specific and better targeted man-agement programs. Very little is known about thelife history of Colletotrichum cereale and the epide-miology of anthracnose, including where and howthe pathogen survives and the weather conditionsthat drive infection and symptom expression.Such information would aid in the developmentof a useful predictive model for basal rot anthrac-

nose. Moreover, this knowledge would enablesuperintendents to more effectively target fungi-cide applications or other management practicesto key points in the disease cycle. For example, ifthe timing of initial infections was known, thensuperintendents could apply preventive fungicideapplications at the most effective time(s), therebypotentially providing more effective control withthe most efficient (reduced) chemical inputs.

Fungicide resistance remains a problem foranthracnose control, and is a continuing risk fornew site-specific fungicides. Scientists are activelyinvestigating how pathogen populations respondto fungicide applications, how resistance devel-ops over time and which resistance management .strategies are most effective. Continuing culturalmanagement research will clarify the effect of top-dressing, irrigation and traffic on anthracnose dis-ease severity, from which best management prac-tices can be enhanced. And, continuing work onselecting and breeding annual bluegrass may leadto new varieties of annual bluegrass with improvedtolerance to anthracnose disease.

DisclaimerUse pesticides only according to the directions on the label.

No endorsement is intended for products mentioned, nor is criti-cism meant for products not mentioned. Trade names are usedonly to give specific information; this publication does not recom-mend one product instead of another that might be similar.

FundingThe authors thank USDA Hatch Regional Hatch Project NE-

1025, GCSAA, USGA, GCSA of New Jersey, U.S. EnvironmentalProtection Agency, The Land Institute, Tri-State Turf ResearchFoundation, and Rutgers Center for Turfgrass Science for sup-porting this work. A portion of the research described in thispaper has been funded by the U.S. EPA under the Science toAchieve Results (STAR) Graduate Fellowship Program. EPA hasnot officially endorsed this publication, and the views expressedherein may not reflect the views of the EPA.

AcknowledgmentsGraduate student Joseph Roberts, technician IJ. Lawson

and numerous student assistants contributed greatly to thisresearch. We also thank the participating golf superintendentsand their clubs for allowing us to do research on their courses.

Literature cited1. Avila-Adame, C., G. Olaya and W. Koller. 2003. Characteriza-

tion of ColletotJichum graminicola isolates resistant to strobi-lurin-related 001 fungicides. Plant Disease 87:1426-1432.

2. Backman, P., G. Stahnke and E. Miltner. 2002. Anthracnoseupdate: Cultural practices affect spread of disease in north-west. Turfgrass Trends 11:T1-T2, T4.

3. Bruehl, GW., and J.G. Dickson. 1950. Anthracnose of cere-

••• •• •• •• •• •

The Multistate Research Project NE-1025, Biology, Ecology, and Managementof Emerging Pests of Annual Bluegrasson Golf Courses has many participatingscientists. Other scientists involved inthe anthracnose research portion of theproject are:

-+ Stacy Bonos, Ph.D., RutgersUniversity

-+ Michelle DaCosta, Ph.D., Universityof Massachusetts, Amherst

-+ Peter Dernoeden, Ph.D., Universityof Maryland

-+ Brad Hillman, Ph.D., RutgersUniversity

-+ David Huff, Ph.D., Pennsylvania StateUniversity

-+ Geunhwa Jung, Ph.D., University ofMassachusetts, Amherst

-+ John Kaminski, Ph.D., University ofConnecticut

-+ Peter Landschoot, Ph.D.,Pennsylvania State University

-+ Joseph Roberts, Rutgers University-+ Wakar Uddin, Ph.D., Pennsylvania

State University

August 2008 GeM 103

••• •• •• •• •• •

The research says

~ Controlling anthracnosedisease on annual bluegrass greens

requires initiating a frequent low-nitro-gen-rate fertility program in late springand continuing it through summer. Fur-

ther study is needed on annual nitrogenrate, seasonal aspects of fertilization

and the possibility of an interac-tion between summer applications of

soluble nitrogen and granular nitrogenfertilization programs.

~ Using Embark, Proxy andPrimo does not intensify anthracnose

disease severity and may reduce it.Frequent low-nitrogen-rate fertilization

combined with the use of seed headsuppressants in spring and sequential

applications of Primo throughout thegrowing season may reduce disease

severity.~ Increasing mowing height

as little as 0.015 inch can decreaseanthracnose severity; daily double-cut-

ting and lightweight rolling increaseball-roll distance and do not intensify

disease; and rolling may slightly reducedisease severity.

~ Preventive fungicide applica-tions are more effective than curative

applications. Repeated sequentialapplications of single-site fungicides

from the same class, late curativeapplications and low-label-rate appli-

cations tend to encourage the develop-ment of resistance.

~ Multisite fungicides have anegligible risk of resistance and can

help reduce overall selection pressurefor resistance. Tank mixes can be more

efficacious and reduce the impactof resistance, but resistance to the

individual mixing partners must still bemanaged.

~ Topics for future researchinclude clarifying the effect of top-

dressing, irrigation and traffic onanthracnose disease severity, andunderstanding where and how the

anthracnose pathogen survives and theweather conditions that drive infection

and symptom expression.

104 GeM August 2008

als and grasses. Technical Bulletin 1005. USDA, Washing-ton, D.C.

4. Crouch, J.A. 2008. Evolution of Colletotrichum speciesinhabiting grasses in diverse ecosystems. Ph.D. disserta-tion, Rutgers University, New Brunswick, N.J.

5. Crouch, J.A., B.B. Clarke and B.I. Hillman. 2006. Unravel-ing evolutionary relationships among the divergent lineagesof Colletotrichum causing anthracnose disease in turfgrassand corn. Phytopathology96:46-60.

6. Crouch, J.A., E.N. Weibel, J.C. Inguagiato, P.R. Majum-dar, et al. 2003. Suppression of anthracnose on an annualbluegrass putting green with selected fungicides, nitrogen,

. plant growth regulators, and herbicides. 2003 Rutgers Turf-grass Proceedings 35 :183-192.

7. Danneberger, lK., J.M. Vargas Jr. and A.L. Jones. 1984.A model for weather-based forecasting of anthracnose onannual bluegrass. Phytopathology74:448-451.

8. Danneberger, lK., J.M. Vargas Jr., P.E. Rieke and J.R.Street. 1983. Anthracnose development on annual blue-grass in response to nitrogen carriers and fungicide appli-

. cation. Agronomy JoumaI75:35-38.9. Dernoeden, P.H. 2002. Creeping bentgrass management:

summer stresses, weeds, and selected maladies. JohnWiley & Sons, Hoboken, N.J.

10. Detweiler, A.R., J.M. Vargas Jr. and W.L. Brendt. 1989.Resistance of Colletotrichum graminicola to benomyl. Pro-ceedings of the International Turfgrass Research Confer-ence 6:359-362.

11. Inguagiato, J.C., J.A. Murphy and B.B. Clarke: 2008.Anthracnose severity on annual bluegrass influenced bynitrogen fertilization, growth regulators, and verticutting.Crop Science 48.1595-1607.

12. Khan, A., and l Hsiang. 2003. The infection process ofColletotrichum graminicola and relative aggressiveness onfour turfgrass species. Canadian Joumal of Microbiology49:433-442.

13. Landschoot, P., and B. Hoyland. 1995. Shedding somelight on anthracnose basal rot. Golf Course Management63(11):52-55.

14. Mann, R.L., and A.J. Newell. 2005. A survey to determinethe incidence and severity of pests and diseases on golfcourse putting greens in England, Ireland, Scotland, andWales. Intemational Turfgrass Society Research Joumal10:224-229.

15. Smiley, RW, P.H. Dernoeden andB.B. Clarke. 2005. Com-pendium of turfgrass diseases. 3rd ed. APS Press, St.Paul.

16. Smith, J.D. 1954. A disease of Poa annua. Joumal of theSports Turf Research Institute 8:344-353.

17. Towers, G., K. Green, E. Weibel, P. Majumdar and B.B.Clarke. 2003. Evaluation of fungicides for the control ofanthracnose basal rot on annual bluegrass, 2002. Fungi-cide and Nematicide Tests58:T017.

18. Uddin, W., M.D. Soika and E.L. Soika. 2006. Influence ofnitrogen source and rate on severity of anthracnose basalrot in mixed annual bluegrass and creeping bentgrass

greens. Phytopathology93:S86.19. Vernard, C., and L. Vaillancourt. 2007. Penetration and colo-

nization of unwounded maize tissues by the maize anthrac-nose pathogen Colletotrichum graminicola and the relatednonpathogen C. sublineolum. Mycologia 99:368-377.

20. White, D.G., R.G. Hoeft and J.l Touchton. 1978. Effect ofnitrogen and nitrapyrin on stalk rot, stalk diameter, and yieldof corn. Phytopathology68:811-814.

21. Wong, F.P., and S. Midland. 2004. Fungicide resistantanthracnose: bad news for greens management. Golf CourseManagement 72(6):75-80

22. Wong, F.P., and S.L. Midland. 2007. Sensitivity distribu-tions of California populations of Colletotrichum cereale tofour sterol demethylation inhibitor fungicides: propiconazole,myclobutanil, tebuconazole and triadimefon. Plant Disease91 :1547-1555.

James Murphy (murphy@aesop.rutgers.edu) and Bruce Clarkeare Extension specialists at Rutgers University, New Brunswick,N.J. Frank Wong is an associate Cooperative Extension plantpathology specialist and associate plant pathologist in thedepartment of plant pathology and microbiology, University ofCalifornia, Riverside. Lane Tredway is an associate professorin the department of plant pathology, North Carolina StateUniversity, Raleigh. Jo Anne Crouch is a post-doctoral associateand John Inguagiato is a graduate student in the department.of plant biology and pathology, Rutgers University, NewBrunswick, N.J. Tom Hsiang is a professor in the department ofenvironmental biology, University of Guelph, Ontario, Canada.Frank Rossi is an associate professor in the department ofhorticulture, Cornell University, Ithaca, N.Y.