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© 2007 Plant Management Network.
Accepted for publication 20 June 2007. Published 11 September 2007.

The Role of Biofungicides and Organic Fertilizer in the Management of Dollar Spot in Bermudagrass

Maria Tomaso-Peterson and D. Hunter Perry, Department of Entomology and Plant Pathology, Mississippi State University, Mississippi State 39762

Corresponding author: Maria Tomaso-Peterson. mariat@pss.msstate.edu

Tomaso-Peterson, M., and Perry, D. H. 2007. The role of biofungicides and organic fertilizer in the management of dollar spot in bermudagrass. Online. Applied Turfgrass Science doi:10.1094/ATS-2007-0911-01-RS.

Abstract

Dollar spot (DS), caused by Sclerotinia homoeocarpa F. T. Bennett, is a foliar disease of warm- and cool-season grasses and occurs frequently throughout the growing season. A three-year study was conducted to evaluate the efficacy of biofungicides for controlling DS of bermudagrass [Cynodon dactylon (L.) Pers. var. dactylon × C. transvaalensis Burtt-Davy]. The biofungicides evaluated in this study were EcoGuard, TurfShield, and Actinovate SP. A slow-release organic fertilizer was applied in conjunction with biofungicide and conventional fungicide treatments in 2006. All biofungicide treatments significantly reduced dollar spot severity (DSSv) in the spring of 2004. However, treatments were similar to the untreated control in 2005. Dollar spot severity was significantly reduced in plots that received organic fertilizer plus biofungicides applied at intervals of 14 days or greater in 2006. In 2004 and 2006, significant reductions in DSSv were observed when EcoGuard and TurfShield were alternated with conventional fungicides. The results of the three-year study indicate EcoGuard, TurfShield, and Actinovate SP applied alone or alternated with conventional fungicides or in conjunction with slow-release organic fertilizer are effective for controlling DS.

Introduction

Dollar spot is a ubiquitous disease that affects all turfgrass species in a number of settings from home lawns to putting greens (8,13,25). The causal organism, Sclerotinia homoeocarpa, infects foliar tissue which results in circular, straw-colored, blighted patches 2 to 3 inches in diameter on closely mown turfgrass. Patches frequently coalesce to create large areas of blighted turf. When turf height is maintained greater than one inch, blighted patches can exceed 5 inches in diameter and appear in irregularly-shaped patterns. Fungal activity commences at 60°F with peak growth and infection occurring between 70 and 80°F coupled with relative humidity greater than 85% within the turf canopy (8,23,25).

Dollar spot is managed to some extent through cultural and fertility practices but intensively managed turf is frequently treated with fungicides, applied in preventative or curative spray programs (1). Fungicide use on turfgrass has been under scrutiny in recent years. Fungicide applications play a primary role in control strategies for turfgrass disease management, however, fungicides can also induce non-target effects (22). Jackson (14) observed increased disease severity of Helminthosporium leaf spot of Kentucky bluegrass (Poa pratensis L.) when fungicides targeted for control of stripe smut were applied. Dollar spot severity increased or was similar to control plots of creeping bentgrass (Agrostis stolonifera L.) or colonial bentgrass (Agrostis capillaries L.) following multiple applications of azoxystrobin (24,27). Multiple applications of benzimidazoles were also reported to increase DSSv of cool-season turfgrass (9) due to the development of resistance.

Within certain regions of the United States, strains of S. homoeocarpa have been identified as resistant to demethylation-inhibitors, benzimidazole, and dicarboximide fungicides (10,11,28). Other turfgrass pathogens have been identified as resistant to certain fungicides. These include strains of Pyricularia grisea (Cooke) Sacc., which cause gray leaf spot and Colletotrichum graminicola (Ces.) G. W. Wils., which causes anthracnose and are reported to be resistant to QoI (strobilurin-like) fungicides (5,26). Turfgrass managers must develop fungicide programs that limit the emergence of pathogens with fungicide resistance.

In addition to an increasing occurrence of fungicide resistance, some fungicides have been removed from the market or application rates and spray intervals have been reduced. In 2006, the Environmental Protection Agency (EPA) completed the registration review of all existing fungicide labels. As a result, EPA has recommended the removal of the turfgrass label for quintozene (PCNB), an important fungicide for controlling snow molds (15,17). Another result of this review dictates the reduction of application rates and spray intervals for thiophanate methyl (3).

In the near future, a reduction in the dependency of conventional fungicides for controlling turfgrass pathogens will be realized. Alternative disease management strategies are currently needed to off-set conventional fungicide use while retaining successful control of turfgrass diseases. Extensive research has been conducted on the use of alternative disease management tools to control DS (7,13,16,19,20,21). Biological agents and use of organic fertilizers have been proven to be effective for suppressing dollar spot in cool-season grasses (16,19,21).

Dollar spot has been documented as more severe under low nitrogen fertility (12,23,25,29). Organic amendments composed of plant and animal meal and other organic sources have been reported to reduce DSSv under various levels of disease pressure. Boulter et al. (7) reported that multiple applications of various compost products reduced dollar spot incidence and severity to a level similar to conventional fungicides. Several sludge and manure composts utilized as fertilizer sources were evaluated for control of DS in creeping bentgrass or annual bluegrass (Poa annua L.) putting greens. The results indicated that compost-amended fertilizers, when applied preventively, controlled DS to levels similar to that of propiconazole (20). Liu et al. (16) identified organic fertilizers that suppressed DS occurrence on creeping bentgrass similarly to the standard fungicide, chlorothalonil.

Biological products amended into topdressings or metabolic extracts have been evaluated for suppression of DS (13,19,21). These products are composed of fungal or bacterial formulations or biologically-based extracts that are prepared in granular or liquid form. They can be applied with minimal difficulty and their efficacy for DS control in some instances has been similar to conventional fungicides when DSSv was high (13,19,21).

As a result of the reported successes of biological and organic amendments for controlling DS in cool-season grasses, a three-year study was initiated to evaluate biofungicides for control of DS in bermudagrass. Additionally in 2006, we evaluated the benefit of integrating a natural, slow-release organic fertilizer into a biofungicide program designed to control DS of bermudagrass.

Evaluating Biofungicides for Suppression of Dollar Spot in Bermudagrass

The study was conducted on ‘Tifgreen’ bermudgrass grown on a Marietta fine sandy loam (fine-loamy, mixed, thermic, siliceous, Aquic Flueventic Eutrocherepts; pH 6.6, OM = 1.35%) at the Rodney R. Foil Plant Science Research Center, Mississippi State University, Starkville, MS. In 2004 and 2005, the study area was fertilized with 0.5 lb of N per 1000 ft² delivered in a 13N-13P-13K or 34N-0P-0K formulation on a monthly basis from April through September. In 2006, ammonium nitrate (34N-0P-0K) was applied at 0.5 lb of N per 1000 ft² in April only. A slow-release organic fertilizer was applied monthly as a treatment throughout the 2006 growing season. The bermudagrass was mowed using a reel mower at 0.25-inch mowing height and irrigated to avoid drought stress. In Mississippi, DS is most severe in bermudagrass swards during spring and fall transition. Therefore, evaluations were conducted in the spring and fall of 2004 and 2006. Treatment plots were maintained throughout spring and fall evaluations for each year. In 2005, a spring evaluation was conducted as dollar spot incidence was low due to unseasonably high temperatures that persisted through October.

Biofungicide applications were based on product label rates and spray intervals (Table 1). Biofungicide treatments were applied for a six week duration beginning 17 May and 7 September 2004, and 9 May and 20 September 2006. In 2005, biofungicide treatments were also applied for a six week duration beginning 24 May only. Two cycles of biofungicide alternated with conventional fungicide treatments on a 14-day interval were achieved for all spring and fall evaluations. In 2004 and 2005, biofungicide treatments were arranged as plots (4 × 6 ft) in a randomized complete block design with four replications. In 2006, treatment plots (4 × 8 ft) were arranged in a randomized complete block design with a split plot arrangement of treatments and replicated four times. Biofungicide treatments were the whole plot factor and slow-release organic fertilizer was the sub plot factor (4 × 4-ft sub-plots). A slow-release organic fertilizer (Nature Safe, Cold Springs, KY) was the nitrogen source and applied monthly, May through October, at 1.0 lb of N per 1000 ft² to biofungicide- and conventional fungicide-treated Tifgreen bermudagrass plots. The organic fertilizer was Nature Safe 8N-3P-5K Stress Guard fertilizer delivered in a fine particle size. The ingredients consist of feather, meat, bone, fish and blood meals, langbeinite, yeast, sugars, carbohydrates and humus with an amino acid content of 49.9%. The nitrogen breakdown consists of 0.20% ammoniacal, 7.20% water-insoluble nitrogen, and 0.90% water-soluble nitrogen.

Table 1. Product name, spray or application interval, product rate, and spray volume included in the three-year biofungicide study.

 ^x Non-ionic surfactant was tank-mixed in ZeroTol treatments.

 ^y Revolution wetting agent was tank-mixed in Actinovate SP treatments.

Three biofungicides were evaluated. EcoGuard (Novozymes, Salem, VA) is a bacterium-based biofungicide with Bacillus lichenformis as the active ingredient. TurfShield (BioWorks Inc., Geneva, NY) is a fungal-based product containing Trichoderma harzianum Rifai. Actinovate SP (Natural Industries Inc., Houston, TX) is a product containing Streptomyces lydicus strain WYEC 108. Three conventional fungicides were also included in the experiments: ZeroTol (BioSafe Systems, Glastonbury, CT), a hydrogen dioxide disinfectant, Daconil Ultrex 82.5 WDG (chlorothalonil), a nitrile contact fungicide, and Chipco 26019 Flo 2SC (iprodione), a dicarboximide localized penetrant.

All treatments, except the granular products, were applied with a CO₂ –pressurized backpack sprayer set to deliver the appropriate spray volume (Table 1) at 40 psi utilizing two nozzles (11002VS or 11004VS flat-fan) spaced 12 inches apart. The granular treatments, TurfShield and organic fertilizer, were distributed by hand within plots using a 1-quart plastic jar with holes in the lid. All ZeroTol treatments were tank-mixed with Activate Plus non-ionic spreader/activator (Riverside/Terra Corp., Sioux City, IA) at 0.25% v/v and Actinovate SP treatments were tank-mixed with Revolution (Aquatrols, Paulsboro, NJ) wetting agent at 6 fl oz/1000 ft².

In 2004, DS occurred naturally in plots. In 2005-2006, plots were artificially inoculated with S. homoeocarpa using a modified ground corncob inoculum method (6). Dried S. homoeocarpa-infested inoculum was applied to all plots using a rotary hand-spreader at 0.3 lb/1000 ft² 7 to 14 days after initial treatment applications. The study area was lightly watered in the early evenings to ensure prolonged leaf wetness to promote S. homoeocarpa infection. In 2004, DSSv was determined by counting the number of infection centers (necrotic spots) in three random samples within a plot using a 1-ft² grid. In 2005-2006, the number of infection centers were counted on a per plot basis and adjusted mathematically to equal number of infection centers per square foot. Visual ratings of turfgrass quality which included a combination of color, density, uniformity, texture, and blighting due to DSSv was based on a scale from 1 to 9 where 9 = best and 6 = acceptable turfgrass quality (18). Dollar spot severity and turfgrass quality ratings were recorded on a weekly basis throughout the duration of the study. Data for each observation date were subjected to analysis of variance and means were separated at P ≤ 0.05 (unless otherwise specified) with Fisher’s protected least significant difference test using the general linear model procedure (2004-2005) and least square means using Proc MIXED (2006) of the Statistical Analysis System (SAS Institute Inc., Cary, NC).

The results discussed herein are single observation dates within years when DS pressure was high. Dollar spot was active in mid-May of 2004 at the onset of this study, however DSSv was highest in mid-June 2004 due to favorable environmental conditions. During this period, turfgrass plots treated with biofungicides and conventional fungicides resulted in significantly fewer infection centers as compared to the untreated control. All biofungicide and conventional fungicide treatments were similar in their efficacy for controlling DS. On 17 June, the untreated control plots averaged 20 infection centers per square foot while infection centers ranged from an average of 2.3/ft² for EcoGuard (7-day spray interval) to 6.7/ft² for TurfShield (28-day application interval). EcoGuard applied on a 7- or 14-day spray interval or alternated with chlorothalonil (14-day interval) reduced DSSv 89%, 77%, and 74%, respectively (Table 2, Figs. 1A and B). TurfShield alone (28-day application interval) or alternated with chlorothalonil (14-day interval) reduced DSSv 67% and 69%, respectively. ZeroTol (7-day spray interval) alone or alternated with iprodione (7-day spray interval), resulted in 86% and 91% reduction in DSSv, respectively. Other conventional fungicides, chlorothalonil and iprodione (14-day interval) reduced DSSv 86% and 78%, respectively (Table 2). Dollar spot severity increased 63% in the untreated control plots over the six week duration of the spring 2004 evaluation while DSSv in the biofungicide and conventional fungicide treatments was reduced 80% to 100% (data not shown) under high disease pressure. Turfgrass quality had an acceptable rating (≥ 6) throughout the 2004 biofungicide evaluation. However, when DSSv was high, turfgrass quality ranged from 6.3 for most biofungicide treatments to 4.8 for the untreated control (Table 3). Tifgreen plots treated with EcoGuard and ZeroTol, (7-day spray intervals), EcoGuard or TurfShield alternated with chlorothalonil, chlorothalonil, and iprodione (14-day spray intervals) had improved turfgrass quality ratings compared to the untreated control (Table 3).

Fig. 1A. Tifgreen bermudagrass treated with EcoGuard applied every 7 days in the spring 2004 evaluation.		Fig. 1B. An untreated control plot of Tifgreen bermudagrass with high dollar spot severity in the spring 2004 evaluation.

Table 2. The effect of biofungicides on dollar spot severity of Tifgreen bermudagrass on selected dates when disease pressure was high.

 ^x Means within columns followed by the same letter are not significantly different at P = 0.05 according to Fisher’s protected least significant difference test. Means are based on four replications per treatment.

 ^y Means within rows followed by the same capital letter are not significantly different at P = 0.05 according to Fisher’s protected least significant difference test. Means are based on four replications per treatment.

 ^z Biofungicide treatments not included throughout the three-year study.

Table 3. The effect of biofungicides on turfgrass quality^w of Tifgreen bermudagrass on selected dates when disease pressure was high.

 ^w Turfgrass quality is based on a visual rating of 1 to 9 where 9 = best, 6 being acceptable.

 ^x Means within 17 Jun 2004 column followed by the same letter are not significantly different at P = 0.10 according to Fisher’s protected least significant difference test. Means are based on four replications per treatment.

 ^y Means within columns followed by the same letter are not significantly different at P = 0.05 according to Fisher’s protected least significant difference test. Means are based on four replications per treatment.

 ^z Biofungicide treatments not included throughout the three-year study.

On 6 June 2005, DS infection centers were evident, however disease pressure was low and DS did not persist after that date. Temperatures rapidly increased throughout June and remained above the optimal temperature for dollar spot occurrence through October 2005. No statistical differences were observed for DSSv or turfgrass quality in the 2005 biofungicide evaluation. Turfgrass quality was reduced throughout the biofungicide evaluation period as a result of limited irrigation.

Dollar spot activity was not observed in the spring or early summer of 2006 due to high temperatures, despite artificial inoculation with S. homoeocarpa. In mid-October 2006, dollar spot symptoms began to appear on the Tifgreen bermudagrass study area. DSSv was highest the fourth week of October. The addition of organic fertilizer to EcoGuard (14-day spray interval), TurfShield (28-day application interval), and Actinovate SP (28-day spray interval) reduced DSSv compared to those same biofungicide treatments without organic fertilizer (Table 2). EcoGuard (14-day spray interval) was 52% more effective for controlling DS when applied with the organic fertilizer. The application of organic fertilizer plus TurfShield (28-day application interval), Actinovate SP (28-day spray interval), and the conventional fungicide ZeroTol (7-day spray interval) reduced DSSv 38%, 40%, and 50%, respectively. Dollar spot severity was also reduced in untreated control plots that received organic fertilizer only (Table 2). However, the addition of organic fertilizer to biofungicide treatments did not significantly improve turfgrass quality compared to those plots treated with biofungicides only (Table 3).

Differences in DS control were noted among treatments that did not receive organic fertilizer applications. EcoGuard (7-day spray interval) was the only "stand-alone" biofungicide treatment that significantly reduced DSSv compared to the untreated control (Table 2). Dollar spot severity was similar for EcoGuard (14-day spray interval), TurfShield (28-day application interval), and Actinovate SP (28-day spray interval); however, EcoGuard (14-day spray interval) had greater DSSv compared to EcoGuard (7-day spray interval) and EcoGuard or TurfShield alternated with chlorothalonil. All biofungicide treatments except EcoGuard (14-day spray interval) were similar to conventional fungicide treatments although DSSv differed between Actinovate SP (28-day spray interval) and chlorothalonil. Stand-alone biofungicide treatments with spray intervals of 14-day or greater resulted in similar DSSv compared to the untreated control (Table 2). Turfgrass quality was significantly improved in Tifgreen bermudagrass plots (no organic fertilizer) treated with EcoGuard (7-day spray interval) compared to the untreated control (Table 3). Turfgrass quality was similar for all other biofungicide and convention fungicide treatments, including the untreated control (Table 3).

When biofungicides were applied in conjunction with organic fertilizer, there were no significant differences in DS control among treatments. Turfgrass quality on 23 October 2006 was improved in Tifgreen bermudagrass plots treated with organic fertilizer plus EcoGuard (7-day spray interval), EcoGuard or TurfShield alternated with chlorothalonil, ZeroTol (7-day spray interval), and ZeroTol tank-mixed with chlorothalonil as compared to the untreated control. Turfgrass quality in plots treated with EcoGuard (14-day spray interval), TurfShield (28-day application interval), Actinovate SP (28-day spray interval) and chlorothalonil were similar to the untreated control (Table 3). Phytotoxicity was not observed in plots treated with biofungicides or conventional fungicides throughout the three-year biofungicide study.

Conclusion

EcoGuard (stand-alone) was effective for controlling DS when applied at a short spray interval. EcoGuard, TurfShield, and Actinovate SP were effective for controlling DS when alternated with conventional fungicides. The results of this study indicate these biofungicides can be successfully used as alternative tools for DS management in bermudagrass. EcoGuard (7-day spray interval) was shown to be efficacious for controlling DS of bermudagrass throughout the three-year study. In two of three years, turfgrass quality was significantly enhanced in EcoGuard 7-day treated plots. The reduction of DSSv resulting from EcoGuard applications as well as the benefit of nitrogen (0.1 lb/1000 ft² per application) contained in the product improved turf quality. TurfShield alternated with chlorothalonil controlled DS under high disease pressure. The added benefit of applying organic fertilizer with stand-alone biofungicide applications was evident due to a significant reduction of DSSv. Organic fertilizer applications complimented the effectiveness of the biofungicides for controlling DS in 2006. Other research has reported the enhanced benefits of applying organic fertilizer in conjunction with conventional fungicides for reducing DSSv (18). This biofungicide study supports the results of published successes of biological control methods for DS on cool-season turfgrasses (7,13,16,20,21). However, this is the first report of biofungicides successfully controlling DS on warm-season turfgrass.

The integration of biological products for disease control of warm- and cool-season turfgrasses relies on the implementation by turfgrass managers. The products evaluated in this three-year biofungicide study are environmentally friendly and promote environmental stewardship. The integration of biological disease management approaches are a good fit in the Audubon Cooperative Sanctuary Program for Golf Courses which promotes the benefits of improved environmental quality (2). Documented reports of S. homoeocarpa-resistance to demethylation-inhibitors, benzimidazoles, and dicarboximides are currently available (10,11,28). As conventional fungicide use becomes more restricted and fungicide resistance increases among turfgrass pathogens, turfgrass managers will have to rely more on alternative disease management tools such as biologically-based products. Continued research is warranted to further determine the efficacy of biofungicides for control of other warm-season turfgrass diseases.

Acknowledgments

Funding for the biofungicide study was provided by the IR-4 Project, under a cooperative agreement with the United States Environmental Protection Agency and approved for publication as Journal Article No. J-1112 of the Mississippi Agricultural and Forestry Experiment Station, Mississippi State University. The authors would also like to thank Novozymes, BioWorks Inc., Natural Industries Inc., BioSafe Systems, and Nature Safe for product contributions. Mention of trademark or proprietary product does not constitute a guarantee or warranty of the product by Mississippi Agricultural and Forestry Experiment Station and does not imply its approval to the exclusion of other products that also may be suitable.

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