Evaluation of New Fungicides and Surfactants for the Fairy Ring in Bermudagrass

Evaluation of New Fungicides and Surfactants for the Management of Fairy Ring Associated with Lycoperdon sp. in Bermudagrass

Carol M. Stiles, Philip F. Harmon, Matthew O. Brecht, and Lawrence E. Datnoff, Plant Pathology Department, University of Florida-IFAS, Gainesville 32611-0680

Corresponding author: Carol Stiles. cstiles@ufl.edu

Abstract

Fungicides were evaluated for control of fairy ring symptoms in bermudagrass maintained at golf course putting green height. In 2004, Heritage and ProStar fungicides tank-mixed with the nonionic soil wetting agent AquaGro had significantly higher quality ratings and lower percent necrotic ring symptoms compared to the untreated check. Insignia significantly reduced the percent necrotic ring when compared to the untreated check although the mean quality ratings were significantly lower than those for Heritage or ProStar treatments. In 2005, when fungicides were applied closer to the onset of symptom development, with the soil surfactant Magnus, Insignia reduced percent necrotic ring symptoms and increased turf quality to levels at or above those of Heritage or ProStar-treated plots. In 2005, Insignia + Magnus resulted in higher quality than Insignia alone. In both 2004 and 2005, neither of the soil surfactants alone was effective at reducing fairy ring development. Treatments containing Insignia (two trials in 2005) and Heritage (one trial in 2005) continued to have significantly higher turf quality, even 6 or 7 weeks after the last fungicide application.

Introduction

Basidiomycete fungi, including Lycoperdon spp., have been associated with necrotic fairy ring and some localized dry spot symptoms accompanied by basidiocarps (8). The role of these fungi in symptom progression and development is not well understood, but some xylem mobile (acropetal translaminar movement) fungicide products are labeled and commonly recommended to help manage symptoms on golf course greens. Necrotic fairy ring, associated with Lycoperdon sp., is a major problem on golf course greens in Florida and the southeastern United States. Fairy ring symptoms are usually categorized into three types (8), depending upon the symptoms and signs present. Type 1 rings have areas of turf that are killed or badly damaged, with considerable necrotic turf present. Type 2 rings have bands of dark green grass, where growth has been stimulated. Type 3 rings have no symptomatic turf, but fruiting bodies of the fungal organism are present; Type 1 and 2 fairy rings may also have basidiocarps present. The fungi typically produce hyphae in a fungal mat somewhere in the organic matter layer (generally referred to as thatch) underneath the turf surface between the most recently senesced turfgrass foliage at the top of the profile and the deepest roots.

In Type 1 rings, the fungal mycelium in the soil likely creates hydrophobic conditions, and the turf is killed or becomes dormant in that area, because the plants are unable to obtain sufficient water (4). Other hydrophobic soil conditions sometimes associated with Lycoperdon spp. produce a mottled chlorotic and necrotic symptom on the green that lacks a defined ring pattern. Such symptoms are generally referred to as localized dry spot. Symptoms of localized dry spot may be caused by a number of factors other than basidiomycete fungi, such as excessive thatch, soil compaction, salt accumulation, soil layering, and poor irrigation coverage (5).

In Florida, necrotic fairy ring primarily occurs on bermudagrass greens from late spring through early fall, but also can occur in winter on overseeded greens. To manage Type 1 fairy ring, golf course superintendents treat with fungicides, primarily flutolanil (ProStar 50 WP; Bayer Environmental Science, Research Triangle Park, NC) or azoxystrobin (Heritage; Syngenta Crop Protection Inc., Greensboro, NC), with or without soil surfactants. Soil surfactants and a brief cycle of irrigation, after fungicide application but before product dries on the turfgrass foliage, sometimes are used to help deliver the fungicide active ingredient into the affected hydrophobic area. Superintendents also use various cultural measures to break up the hydrophobic area such as core aerification or other cultivation techniques.

Elliott et al. (4) showed that flutolanil, with and without the wetting agent AquaGro L, reduced the number of Lycoperdon basidiocarps produced and also prevented necrotic fairy ring symptom development when half of each of nine greens on a golf course were treated preventatively. The use of flutolanil alone in areas where localized dry spot (not associated with basidiocarps) occurred was not effective in reducing the effects of the hydrophobicity (5); thus, localized dry spot effects that are not caused by basidiomycete fungi may be alleviated by the use of soil wetting agents (4). Soil wetting agents alone have been ineffective in controlling necrotic fairy ring associated with Lycoperdon sp. (3,7) and have been shown to lower turfgrass quality due to phytotoxicity in some cases (9). Datnoff and Cisar (3) and Martin (7) showed that azoxystrobin alone or in combination with wetting agents significantly suppressed fairy ring symptoms.

More recently, newer fungicide chemistries are available that are labeled for fairy ring, including pyraclostrobin (Insignia; BASF Corporation, Research Triangle Park, NC) and polyoxin D (Endorse; Cleary Chemical Corp., Dayton, NJ). Because fairy rings may be limited in size and number on research greens and golf courses may not be willing to cooperate with research trials, opportunities for management research often are limited (4). The development of fairy ring symptoms in 2004 and 2005 on the Turfgrass Envirotron Research Golf Green at the University of Florida/IFAS, Gainesville, offered an excellent opportunity to evaluate new fungicide chemistries for curative management.

Superintendents with chronic necrotic fairy ring commonly report to extension pathologists that they often rotate multiple products (applying a different product every 14 days) because the labeled 28- to 30-day interval between applications of single products is insufficient to alleviate and prevent recurrence of symptoms when environmental factors favor growth of the fungus or development of hydrophobic soil (8). Thus, in our experiments, treatments were applied at shorter intervals (14 days) than recommended on product labels. Most treatments consisted of multiple applications of a single product in an attempt to more clearly evaluate the potential of each fungicide tested as a management tool.

The fungus associated with the fairy rings was a Lycoperdon sp., and in 2004 symptoms developed as a nearly complete ring across one side of the green. Despite treatment in 2004, the ring had expanded across the research green by 2005. Several smaller rings and a large localized dry spot associated with several basidiocarps developed inside the circumference of the original ring, enabling the establishment of additional trials. A preliminary 2004 data report has been published (1).

Turf Plot Maintenance and Establishment of Fairy Ring Trials

Fungicide trials were conducted on a USGA-specified ‘Tifdwarf’ bermudagrass green with a 90:10 sand:peat root-zone mix located at the Turfgrass Envirotron research facility in Gainesville, FL. In 2004, turf was maintained at 0.16 inch and irrigated daily for a total weekly average of 1 in. of water. Fertilizer was applied at 0.5 lb of N per 1000 ft² on 24 July, 10 August, 31 August, and 2 September. Insects were controlled with Dursban (0.75 fl oz/1000 ft²) on 26 July.

In 2004, fairy ring symptoms were classified as a Type 1 ring exhibiting a zone of dead grass and a zone of dark green grass. Symptoms progressed in untreated plots from a 2- to 3-inch wide band of dark green grass to a 3- to 4-inch wide band of necrotic turfgrass. Warm and wet weather conditions favored basidiocarp formation early in the development of symptoms. As the trial progressed, little precipitation (excluding daily irrigation) was recorded. No additional basidiocarps formed; however, a necrotic band symptom continued to develop in untreated plots.

Treatments were applied in a randomized complete block design with three blocks of six treatments (Table 1). Boscalid (Emerald; BASF, Research Triangle Park, NC) is a new active ingredient in the carboxamide fungicide group and is a new mode of action against dollar spot (caused by Sclerotinia homoeocarpa). Because the active ingredient is in the same fungicide group (carboxamides) as flutolanil, it was included to investigate possible activity against the fairy ring caused by Lycoperdon sp. Experimental units were 3.3 ft by 3.3 ft and were arranged along the circumference of the ring, such that symptoms transected each plot. Fungicides were delivered with a CO₂-powered boom sprayer at 30 psi and TeeJet 11003 VP nozzles in a volume equivalent to 4.0 gal/1000 ft², but ProStar was applied at 10.0 gal/1000 ft². AquaGro (Aquatrols Corp. of America, Paulsboro, NJ), a nonionic soil wetting agent, was applied alone or was tank-mixed with the fungicides at a rate equivalent to 0.8 oz/1000 ft². Treatments were applied on 15 and 28 July, and 11 and 27 August 2004.

In 2005, fairy ring symptoms began to develop in early September, in the same general area on the green, although the main part of the ring had expanded beyond the symptomatic area of the previous year. Two trials were completed between September and November. The first trial was initiated 9 September. The experiment was arranged so that the necrotic ring symptoms were divided into individual plots (Fig. 1), arranged in a randomized complete block design with three blocks. Plot size was 3.3 ft by 1.6 ft. Although initial quality ratings and percent necrosis were similar to 2004, the first treatment application was completed closer to the development of the symptoms than in 2004. Except with the Insignia-alone treatment, fungicide products were tank-mixed with 4 oz / 1000 ft² of Magnus soil surfactant (a proprietary blend of polymeric surfactants; Precision Laboratories Inc., Waukegan, IL). Treatments (Table 2) were applied every 14 days on 9 September, 23 September, and 6 October 2005 with a CO₂ backpack boom sprayer calibrated to deliver products in 4 gal/1000 ft² through two Teejet flat fan nozzles at 30 psi. Plots were irrigated with 0.25 in. water after treatments were applied, but before fungicide products dried on the turfgrass foliage. Turf was maintained at a height of 0.165 in. using a Toro Greensmaster 1000 reel mower (The Toro Company, Bloomington, MN). Fertilizer was applied monthly at a rate of 0.5 lb of N per 1000 ft². Irrigation was provided as needed to alleviate stress.

Fig. 1. Necrotic fairy ring transecting experimental plots, part of one block in Trial 1 in 2005.

The second 2005 trial was initiated 15 September within the larger necrotic ring and included an area where the turfgrass was damaged badly (bare areas and thinning turf) and numerous Lycoperdon basidiocarps were observed prior to beginning the trial (Fig. 2). Treatments (Table 3) included fungicides in rotation, with and without Magnus. Insignia and Prostar were also applied alone, without any soil surfactant. Treatments were applied every 14 days (except ProStar, which was applied at a one-month interval) with a CO₂ backpack boom sprayer calibrated to deliver products in 4 gal/1000 ft² through two Teejet flat-fan nozzles at 30 psi. The trial area was irrigated with 0.25 inch of water after treatments were applied, but before the fungicide products had dried on the turfgrass foliage. The trial area was divided into experimental units of 3.3 ft by 13.1 ft and the treatments were arranged in a randomized complete block design with four blocks.

Fig. 2. (A) Area of research green used for Trial 2 in 2005, showing mottling symptoms and numerous puffballs observed just prior to beginning of experiment. (B) Typical sporocarp of Lycoperdon sp.

Evaluation of Fairy Ring Severity and Turf Quality

Quality ratings were made on a scale from 1 to 9, where 1= dead turf, 6 = acceptable quality, and 9 = highest turf quality. Percent necrotic ring was determined as a visual estimate of the percent of the ring that transects the plot containing necrotic turf. Plots were rated once a week for eight weeks. Percent necrotic ring and quality ratings at each date were subjected to analysis of variance and means separation by Fisher’s protected least significant difference (LSD) test. When disease ratings are plotted over time, the area under each curve can be calculated and used to compare treatments over the whole time period of a disease epidemic (2). Area under the disease progress curve (AUDPC) values are often used to compare treatments in plant pathological studies, including turfgrass diseases (6,10). In this study, the area under the curve formula was also applied to turf quality ratings to calculate the "area under the turf quality curve" (AUTQC). While significant differences and treatment rankings may vary somewhat at individual rating dates, AUDPC and AUTQC values allow disease ratings and turf quality to be compared over the entire time period of each study. AUDPC’s and AUTQC’s were subjected to analysis of variance and separated by Fisher’s protected least significant difference (LSD) test.

Fairy Ring Development and Fungicide Evaluation in 2004

The mean percent necrotic ring symptoms was 50% of the plot area affected and the average quality rating was 1.7 at the beginning of the experiment, and there were no initial significant differences (P ≤ 0.05) between treatment plots. Treatment differences were evident 2 weeks (quality ratings) and 3 weeks (percent necrotic ring) after initial treatment applications (Table 1). When AUTQC and AUDPC values were compared, plots treated with Heritage or ProStar had significantly higher quality ratings and lower percent necrotic ring symptoms compared to the untreated check (Figs. 3 to 4). Insignia significantly reduced the percent necrotic ring at three rating dates (Table 1) when compared to the untreated check, although AUDPC values were not significantly different (Fig. 4). In addition, mean quality ratings of plots treated with Insignia were below 6.0 at the end of the study (Fig. 3). Emerald is not labeled for fairy ring control and did not provide any significant increase in turf quality. AquaGro, used to alleviate hydrophobicity in soils, did not help to lessen percent necrotic ring, nor did it provide any significant improvement in turf quality as compared to the untreated check (Figs. 3 to 4). Differences in Heritage, ProStar, AquaGro treatments and the untreated control are illustrated one month after first application in Fig. 5. No phytotoxicity was observed.

Fig. 3. Turf quality progress curves based on turfgrass quality ratings in 2004 trial. Each data point is the mean of three replicates. Plotted curves followed by the same letter indicates mean AUTQC’s are not significantly different according to LSD (P ≤ 0.05).

Fig. 4. Disease progress curves based on percent necrotic ring in 2004 trial. Each data point is the mean of three blocks. Plotted curves followed by the same letter indicates mean AUDPC’s are not significantly different according to LSD (P ≤ 0.05).

Fig. 5. Plots treated with (A) Heritage, (B) Aqua-Gro, (C) ProStar, and (D) untreated. Photos taken 12 August 2004 after treatment applications on 15 July, 28 July, and 11 August.

Fairy Ring Development and Fungicide Evaluation in the First Trial, 2005

Initial quality and percent necrosis ratings recorded on 8 September, before the first treatment application, averaged 1.7 and 69.5% respectively, across all plots. The initial quality and percent necrosis ratings for the treatments were not significantly different (P ≤ 0.05). Significant differences among treatment means were first detected on 22 September, when Insignia + Magnus and ProStar + Magnus treatments had significantly higher quality ratings than Insignia alone, Endorse + Magnus, Magnus alone, and the untreated control (Table 2). All fungicide treatments resulted in significantly lower mean percent necrosis ratings compared to the untreated control at three rating dates (Table 2). Plots treated with Magnus alone had significantly lower necrosis on two of the three rating dates; however, percent necrosis in these Magnus-treated plots still ranged from 38.3 to 50% necrosis. Plots treated with Insignia + Magnus and ProStar + Magnus had the greatest decrease in mean percent necrosis. The Insignia + Magnus treatment had lower percent necrosis and higher mean quality ratings than Insignia alone (Table 2), and this difference was significant for quality ratings at 22 September and 30 September.

Rating dates between 6 October and 19 November had similar treatment rankings of percent necrosis and turf quality compared to 22 September, 30 September, and 6 October; however, differences between treatment means were not significant. Differences in fungicide treatments were still apparent for turf quality even seven weeks after the last fungicide application (Table 2, Fig. 6). On 19 November and 27 November, quality ratings for Insignia + Magnus, ProStar + Magnus, and Heritage + Magnus were significantly higher than the other treatments. Overall, quality ratings were somewhat lower at these later dates, due to the onset of cooler temperatures and decreased bermudagrass growth. When AUDPC and AUTQC values were compared, plots treated with Insignia + Magnus, Heritage + Magnus, Insignia without Magnus, and ProStar + Magnus resulted in higher turfgrass quality and lower necrotic ring than the untreated control (Figs. 6,7). Differences in these treatments, after two applications, are illustrated in Fig. 8.

Fig. 6. Turf quality progress curves based on turfgrass quality ratings in Trial 1 of 2005. Each data point is the mean of three blocks. Plotted curves followed by the same letter indicates mean AUTQC’s are not significantly different according to LSD (P ≤ 0.05).

Fig. 7. Disease progress curves for percent necrotic ring in Trial 1 of 2005. Each data point is the mean of three blocks. Plotted curves followed by the same letter indicates mean AUDPC’s are not significantly different according to LSD (P ≤ 0.05).

Fig. 8. Plots treated with (A) Insignia + Magnus, (B) Insignia, (C) ProStar + Magnus, and (D) untreated. Photos taken 25 September 2005, after treatment applications on 8 September and 22 September.

Fairy Ring Development and Fungicide Evaluation in Second Trial, 2005

In the second trial of 2005, initial quality ratings taken on 15 September, before the first application, averaged 1.5 across all plots, and the treatment plots were not significantly different (P ≤ 0.05). Because individual necrotic rings were not visible in the damaged area, only quality ratings were taken. Significant differences among treatment means were first detected on 13 October, with all fungicide treatments having quality ratings higher than the untreated control plots (Table 3). The combination applications of Insignia and ProStar, with and without Magnus were most effective at enhancing turf recovery, based on turf quality which remained high throughout the study for these treatments (Fig. 9). Insignia alone also increased AUTQC over the untreated control, and the AUTQC for Insignia was not significantly different from the combination treatment (Fig. 9). On 20 October, three days after the last application, the two combination treatments and the Insignia alone treatment had significantly higher quality ratings than ProStar alone and the untreated control. The treatments containing Insignia continued to maintain higher turf quality, and these differences were still apparent six weeks after the last fungicide application (Table 3). When AUTQC values were compared, the combination treatments and Insignia alone were significantly higher than the ProStar treatment alone (Fig. 9).

Fig. 9. Turf quality progress curves based on turfgrass quality ratings in Trial 2 of 2005. Each data point is the mean of four blocks. Plotted curves followed by the same letter indicates mean AUTQC’s are not significantly different according to LSD (P ≤ 0.05).

Endorse was included because it has activity against other basidiomycete fungi (Rhizoctonia spp.) and it has a FIFRA (Federal Insecticide, Fungicide, and Rodenticide Act) 2(ee) label for control of fairy ring, including Marasmius spp., Lepiota spp., and Agaricus spp. But Endorse is not labeled specifically for Lycoperdon spp. and did not improve turfgrass quality in this trial.

With the onset of cool weather, some bronzing of all four replicate plots in the combination treatment with Magnus was observed on 26 October and 3 November. As the bermudagrass went into dormancy, this bronzing was less noticeable. Turf quality ratings did not increase above a mean of about 6.0, due to the onset of cool weather and bermudagrass dormancy, however the increased quality and recovery in fungicide-treated plots were still very apparent on 27 November. The use of AUTQC’s allows comparison of turf recovery and turf quality over the entire time period of the study and thus, may be a useful addition to other turfgrass studies.

Fungicide Management Recommendations for Fairy Ring

Heritage and ProStar significantly reduced necrotic ring development and increased turf quality in 2004 and 2005, as previously demonstrated (3,4,7). Among newer fungicides, Insignia also significantly reduced necrotic ring development in 2004, although not as much as Heritage or ProStar, and mean quality ratings were not significantly different from the untreated control. However, in 2005 when treatments were applied closer to the onset of necrosis in the ring and immediately irrigated with 0.25 inch of water, Insignia alone resulted in a response similar to that of other fungicides tank-mixed with Magnus. Insignia tank-mixed with Magnus provided even better control than Insignia alone by improving turf quality ratings, with significantly higher quality ratings on 22 September, 30 September, 19 November, and 27 November 2005. In addition, in 2005, Insignia and Heritage provided longer lasting turf quality than ProStar, for at least six weeks after the last fungicide application. ProStar is very specific for basidiomycete fungi, while Insignia and Heritage have activity against other groups of fungi. The longer lasting turf quality in Insignia and Heritage-treated plots in these trials may be a result of activity against other fungi.

The surfactants alone (AquaGro and Magnus) did not provide any benefit in managing fairy ring associated with Lycoperdon sp., which is consistent with previous work by Elliott et al. (4) using AquaGro L. Further experimentation is needed to elucidate the potential effects of various soil surfactants, timing of applications relative to symptom development, and irrigation options after application to improve fungicide efficacy. In addition, research is needed on non-chemical management practices, including potential biological control measures, for fairy ring associated with Lycoperdon sp.

Acknowledgments

Financial support was provided by the Florida Agricultural Experiment Station, University of Florida IFAS. We wish to acknowledge Dr. Grady L. Miller and the staff of the UF IFAS Turfgrass Envirotron for assistance in establishing and maintaining the experimental plots.

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