Banner graphic that reads, 'Introducing H. H. Flor Distinguished Reviews. A landmark series from M P M I advancing the science of molecular plant-microbe interactions'
APS Online Publications
Skip main navigation
Previous
Next
RESEARCHFree Access icon

Investigations into Economic Returns Resulting from Foliar Fungicides and Application Timing on Management of Tar Spot in Indiana Hybrid Corn

    Affiliations
    Authors and Affiliations
    • Tiffanna J. Ross1
    • Tom W. Allen2
    • Sujoung Shim1
    • Nathanael M. Thompson3
    • Darcy E. P. Telenko1 †
    1. 1Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
    2. 2Delta Research and Extension Center, Mississippi State University, Stoneville, MS 38776
    3. 3Department of Agricultural Economics, Purdue University, West Lafayette, IN 47907
    Published Online:19 Feb 2024https://doi.org/10.1094/PDIS-05-23-0932-RE

    Abstract

    Tar spot, caused by Phyllachora maydis, is the most significant yield-limiting disease of corn (Zea mays L.) in Indiana. Currently, fungicides are an effective management tool for this disease, and partial returns from their use under different disease severity conditions has not previously been studied. Between 2019 and 2021, two separate field experiments were conducted in each year in Indiana to assess the efficacy of nine foliar fungicide products and nine fungicide application timings based on corn growth stages on tar spot symptoms and stromata, canopy greenness, yield, and influence on partial returns. All fungicides evaluated significantly suppressed tar spot development in the canopy and increased canopy greenness over the nontreated control. Additionally, applications of mefentrifluconazole + pyraclostrobin, metconazole + pyraclostrobin, cyproconazole + picoxystrobin at tassel, and propiconazole + benzovindiflupyr + azoxystrobin between the tassel and dough growth stages were the most effective at significantly reducing disease severity, increasing canopy greenness, protecting yield, and offered the greatest partial return. Fungicide products varied in their ability to protect yield under low and high disease severity conditions relative to the nontreated control. Consistently, positive yield increases were observed when disease severity was high, which translated to greater profitability relative to low severity conditions. On average, the yield increases across foliar fungicide products and timed application treatments were 544.6 and 1,020.7 kg/ha greater, and partial returns using a grain value of $0.17/kg were $92.6/ha and $173.5/ha greater, respectively, when high severity conditions occurred. This research demonstrates that foliar fungicides and appropriately timed fungicide applications can profitably be used to manage tar spot in Indiana under high disease severity conditions.

    Hybrid corn (Zea mays L.) is one of the most important crops grown in the United States. During 2020 and 2021, corn production was estimated between 32.9 and 34.5 million ha nationally (USDA-NASS 2022). Within the United States corn production system, Indiana ranks fifth for hybrid corn production with an estimated 26,104 million kg produced on approximately 2.1 million ha annually (USDA-NASS 2023). However, the environmental conditions in this region are suitable for the development of several economically important corn diseases (Wise et al. 2016). In 2018, Indiana experienced the first yield limiting epidemic of tar spot, caused by Phyllachora maydis Maubl., a foliar fungal disease of corn that can decrease quality and quantity of grain and silage production (Telenko et al. 2019a). In 2021, corn yield losses resulting from tar spot in the United States accounted for an estimated 5,883 million kg and in Indiana accounted for an estimated yield reduction of 4.0% of corn production valued at $253.5 million (Crop Protection Network 2022a; Mueller et al. 2022).

    Tar spot was initially detected in the north central United States in 2015 in Illinois and Indiana (Ruhl et al. 2016; Valle-Torres et al. 2020). At that time, only seven counties in Indiana were confirmed to contain tar spot-infected corn. However, as of 1 November 2022, tar spot has been collectively confirmed in 86 of Indiana’s 92 counties (https://corn.ipmpipe.org/tarspot/; D. E. P. Telenko, personal observation). Since the initial observations of tar spot on the North American continent, the disease has been observed in 16 states from as far south as Florida to as far north as Minnesota and into Ontario, Canada (Athey 2020; Collins et al. 2021; Kness 2022; Malvick et al. 2020; Mottaleb et al. 2019; Moura et al. 2023; Pandey et al. 2022; Tenuta 2020; Valle-Torres et al. 2020; Wise et al. 2023). Signs of tar spot include brown-black, circular to semicircular fungal fruiting bodies (stromata) embedded in the surfaces of corn foliage and husks of ears on plants of any age (Parbery 1967; Telenko et al. 2021; Valle-Torres et al. 2020). In heavily infested fields, green foliage becomes blighted and prematurely senesces, resulting in death of the plant (Liu 1973; Valle-Torres et al. 2020). Infection is initiated by the pathogen’s ascospores, which favor cool temperatures (20 to 25°C), extended periods of leaf wetness (>7 h), and high relative humidity (≥75%) (Bajet et al. 1994; Groves et al. 2020; Hock et al. 1989; Valle-Torres et al. 2020). Infested corn residue can harbor ascospores that serve as the overwintering and the primary source of inoculum for the subsequent season (Groves et al. 2020; Kleczewski et al. 2019b).

    Currently, management suggestions for tar spot include crop rotation, tillage for residue management, planting moderately tolerant hybrids, and application of foliar fungicides (Crop Protection Network 2022b; Da Silva et al. 2021a; Kleczewski et al. 2019a; Telenko et al. 2019a, 2021, 2022a, b; Wise et al. 2019). The use of fungicides in hybrid corn production has increased considerably in the United States, even under low disease severity conditions due to the perceived benefits of increased yield in the absence of disease, delayed leaf senescence, and decreased lodging at harvest (Paul et al. 2011; Tedford et al. 2017; Wise and Mueller 2011). Fungicides vary in efficacy when protecting crops from diseases (Crop Protection Network 2022b), and since 2005/2006, the economic benefit of applying a fungicide in the absence of disease has been debated (Mallowa et al. 2015; Mueller et al. 2021; Paul et al. 2011; Wise and Mueller 2011). Certain fungicide active ingredients have been reported to increase yield even in the absence of disease, such as those in the quinone inside inhibitor (QoI) class (Zhang et al. 2010). However, fungicide applications may not always be economically beneficial, especially in situations where disease does not occur (Bartlett et al. 2002; Paul et al. 2011; Venancio et al. 2003). On average, fungicides can provide protective disease efficacy for 14 to 21 days following application; however, some newer fungicide products have been observed to provide enhanced residual protection beyond 21 days (T. W. Allen, unpublished data; Mueller et al. 2013). Tar spot has a latent period of between 12 and 15 days before noticeable symptoms and signs develop at the field level (Carson 1999; Hock et al. 1995; Telenko et al. 2021). Hence, a well-timed fungicide application program can be important in reducing severity, protecting yield in the presence of disease, and achieving a positive return on investment (ROI). For many foliar corn diseases, the current suggestion for fungicide application is at the anthesis-crop development stages, between tassel (VT) and silk (R1), or as late as milk (R3) stage (Abendroth et al. 2011; Mueller et al. 2021). Applications made at or during these growth stages may be economically beneficial but are dependent on the particular foliar disease, hybrid, and environmental conditions (Mueller et al. 2021; Paul et al. 2011; Tedford et al. 2017). Additionally, a carefully timed fungicide application between the late vegetative (V14 to VT) and early reproductive growth stages (R1 to R3) oftentimes targets disease management and grain productivity and is most likely to produce a positive ROI when conditions are favorable for disease development (Mueller et al. 2021; Paul et al. 2011; Tedford et al. 2017). A study evaluating corn yield response to foliar fungicides in the United States and Ontario, Canada, concluded that foliar fungicides could significantly increase corn grain yield, but growers needed to focus on applications at the tassel (VT) growth stage to ensure the likelihood of a positive ROI (Wise et al. 2019). Notably, a positive return to fungicide investment is most likely to occur at locations and in years when disease incidence and severity levels are high and a negative return in years when severity levels are low (Edwards et al. 2012; Ransom and McMullen 2008; Wegulo et al. 2011; Wiik and Rosenqvist 2010). The partial returns from fungicide treatments are also dependent on the treatment cost, treatment application method, and most notably on commodity price. Information regarding fungicide efficacy, application timing, and the economic return associated with fungicide programs is needed to help growers make more informed management decisions for tar spot. To our knowledge, the partial returns from hybrid corn under fungicide programs at different stages of tar spot disease progression and under different levels of disease has not been studied quantitatively in Indiana or the United States for that matter. Currently, there are no thresholds established for fungicide applications based on tar spot severity levels in the United States, making it difficult to recommend to corn growers when to apply fungicides. Even though treatment thresholds do not exist for tar spot or any of the other foliar diseases of corn, guidelines regarding effective treatment selection have been reported. Telenko et al. (2022a, b) reported that several fungicides were available and useful for managing tar spot and that those with a two- and three-mode-of-action mixture were more efficacious and beneficial in reducing disease severity and a three-mode-of action product was best for protecting yield. Nevertheless, the question remains which of these fungicides available for tar spot management will produce the greatest economic return to Indiana corn growers.

    The goal of this study was to conduct small-plot field experiments evaluating the application timing and efficacy of foliar fungicides for tar spot management in Indiana. The study objectives were to assess the effectiveness of commercially available foliar fungicides and application timing strategies on disease severity and canopy greenness in the presence of tar spot. In addition, trial data would be used to estimate the yield response and partial ROI from fungicide treatments under high and low disease severity conditions. Results from the current study will aid corn growers with the information necessary to manage tar spot on corn economically and will also serve as a foundation for stochastic methods to quantify and forecast losses associated with tar spot of corn.

    Materials and Methods

    Study locations and experimental design

    Between 2019 and 2021, two field experiments were conducted in each year to evaluate tar spot management: (i) a set of fungicide efficacy trials that compared multiple fungicide products and (ii) a set of fungicide application timing trials in which the effect of a single fungicide product at multiple application timings based on corn plant growth stages was tested. The corresponding field trials were each established at two of Purdue University’s research centers: Pinney Purdue Agricultural Center (PPAC) in Wanatah, Indiana, and the Agronomy Center for Research and Education (ACRE) in West Lafayette, Indiana. Wanatah is in northwestern Indiana, whereas West Lafayette is in west-central Indiana. The two locations differ in environmental conditions and history of tar spot. However, in 2021, field experiments were not conducted at the West Lafayette location due to extremely low disease incidence in previous years. Detailed trial information is presented in Table 1.

    Table 1. Field experiment information for two fungicide efficacy trials conducted as a comparison of nine fungicide products and a nontreated control and a fungicide timing trial with nine application timings based on corn growth stage using one fungicide product and a nontreated control to manage tar spot in hybrid corn at two locations in Indiana between 2019 and 2021

    Each set of experiments was conducted as a randomized complete block design with 10 treatments replicated four times. Plots were 3.0 m wide and 9.1 m long and consisted of four rows spaced 76.2 cm apart separated by a 1.5-m fallow alley. The two center rows of each four-row plot were used for data collection. All fields were previously established with corn, and standard agronomic practices for corn production in Indiana were followed. Corn hybrid W2585SSRIB (Wyckoff Hybrids, Inc., Valparaiso, IN), previously observed to be susceptible to tar spot, was planted at a density of 13,759 seeds/ha for all trials. The fungicide efficacy experiment at Wanatah was supplemented with overhead irrigation weekly (approximately 25 mm) when natural precipitation did not reach 25.4 mm per week. All fungicide treatments in the efficacy experiment included a nonionic surfactant (NIS) (as 0.25% v/v of Preference, WinField Solutions, St. Paul, MN). In the timing experiment, a NIS was not used due to the risk of arrested ear syndrome in applications made before tassel (VT) (Stetzel et al. 2011). Fungicide treatments were applied using either a CO2 backpack sprayer or a Lee self-propelled sprayer (Spider Spray Trac 3000, LeeAgra, Inc., Lubbock, TX) equipped with a 3.0-m boom and fitted with four nozzles spaced 0.5 m apart delivering fungicides at 140.3 liters/ha at 275.8 kPa.

    Fungicide treatments

    For the fungicide efficacy experiment, the field trial was designed to evaluate the efficacy and partial returns from nine fungicide products as compared to a nontreated control. The nine fungicide product treatments included various active ingredients from different chemical groups both alone and as mixtures of active ingredients representing several different Fungicide Resistance Action Committee (FRAC) codes (Fungicide Resistance Action Committee 2021). The specific fungicide products included a stand-alone quinone outside inhibitor (QoI; strobilurin) representing FRAC code 3 as pyraclostrobin (Headline at 0.42 liters/ha, BASF Corporation, Research Triangle Park, NC) and stand-alone C-14 demethylation inhibitor (DMI; triazole) representing FRAC code 11 as propiconazole (Tilt at 0.28 liters/ha, Syngenta Crop Protection, Greensboro, NC). In addition, several premix combinations of the QoI and DMI class included cyproconazole + picoxystrobin (Aproach Prima at 0.48 liters/ha, Corteva Agriscience, Wilmington, DE); mefentrifluconazole + pyraclostrobin (Veltyma at 0.49 liters/ha, BASF); metconazole + pyraclostrobin (Headline AMP at 0.73 and 1.02 liters/ha, depending on year, BASF); and prothioconazole + trifloxystrobin (Delaro at 0.56 liters/ha, Bayer Crop Science, St. Louis, MO). Succinate dehydrogenase inhibitors (SDHIs, carboxamides) representing FRAC code 7 were included in two combinations with either a DMI as flutriafol + bixafen (Lucento at 0.35 liters/ha, FMC Corporation, Philadelphia, PA) or as a three-way mixture with a QoI and DMI as mefentrifluconazole + fluxapyroxad + pyraclostrobin (Revytek at 0.56 liters/ha, BASF) and propiconazole + pydiflumetofen + azoxystrobin (Miravis Neo at 0.96 liters/ha, Syngenta). All fungicide products were applied at the tassel-silk (VT/R1) corn growth stage. The manufacturer’s recommended dosages for each product were followed. Initially, the highest rate of metconazole + pyraclostrobin was used in 2019 but was reduced to 0.73 liters/ha in subsequent years based on updated recommendations. Additional products were added after 2019 due to availability of new fungicides on the market and included a single DMI product for additional comparison. See Table 2 for details on percent active ingredient, FRAC code, application rate, cost of fungicide application program for ground and aerial method, and year evaluated.

    Table 2. Summary information regarding the fungicide treatments used for managing tar spot of hybrid corn at two locations in Indiana between 2019 and 2021 including FRAC code, active ingredients, fungicide product, application rate, average cost of fungicide by method of application, and the year each product was evaluated

    For the application timing experiment, the field trial was designed to identify the appropriate application timing and partial economic return of the mixed mode of action fungicide propiconazole + benzovindiflupyr + azoxystrobin (Trivapro as 0.96 liters/ha, Syngenta). The experiment included 10 treatments based on growth stage at time of application, of which one was a nontreated control for comparison purposes. While application timings were targeted for specific growth stages, there was some overlap across years in some cases, and as a result, the growth stages in those instances were grouped together for presentation purposes (e.g., V6/V7). Corn plants at each application timing were growth staged by counting the number of collars on each plant from the ground moving up the plant (Abendroth et al. 2011). See Table 1 for details on specific application timings.

    Tar spot field assessments

    The severity of tar spot was assessed weekly from the first detection in each trial to corn growth stage dent (R5) or physiological maturity (R6). The disease severity assessment included two variables: percent tar spot foliar symptoms (necrotic/chlorotic tissues) and percent tar spot stromata (fungal fruiting bodies) on three leaves within the plant canopy considering the ear leaf as a midpoint, in the lower-canopy as the ear leaf minus two leaves, and in the upper-canopy defined as the ear leaf plus two leaves. Evaluation of leaf material was made in each canopy zone based on a standardized rating scale for tar spot of 0 to 100% of the leaf surface (Telenko et al. 2021). Since multiple evaluators were used each season, an interrater reliability test was performed before data collection to reduce data biases and to ensure some level of data consistency. Percent tar spot stromata was rated by visually assessing the leaf area (0 to 100%) covered with fungal stromata. Five plants per plot (subsamples) were arbitrarily selected, and disease severity was rated in the canopy. The five plants were then averaged for a single disease severity estimate value for each plot for the ear leaf minus two (lower canopy), ear leaf, and ear leaf plus two (as upper canopy). Green leaf material remaining in each plot posttreatment (canopy greenness) was determined by visually assessing the amount of whole plant canopy (0 to 100%) that remained green at the dent (R5) or physiological maturity (R6) corn growth stage.

    At R6, yield from the two center rows of each plot was harvested using a small plot combine (Kincaid 8XP, Kincaid Equipment Manufacturing, Haven, KS) outfitted with a HarvestMaster grain gauge (Juniper System, Ind., Logan, UT). Yield was standardized to 15.5% moisture prior to analysis. Changes in yield due to fungicide application compared to the nontreated plots was calculated using the following formula: Yield Increase (Ydiff) = Yf – Yc, where Yf is the yield due to fungicide application, and Yc is the yield of the nontreated control. Ydiff(s) were used in the economic analysis.

    Economic analysis

    A partial budgeting approach was used to calculate the partial returns for each fungicide treatment focusing only on the revenues and costs that changed based on the decision to apply a foliar fungicide. The current approach does not include all revenues and expenses faced by the grower. Partial returns (PR) were calculated in dollars per hectare ($/ha) using the following modified equation originally developed by Munkvold et al. (2001):

    PR=P*Ydiff−N(Fpc)

    where P is the corn price ($/kg), Ydiff is the change in yield due to fungicide application as compared to the nontreated control (kg/ha), N is the number of fungicide applications, and Fpc is the cost of the fungicide program ($/ha), which includes the cost of the fungicide product and application method. Both ground and aerial methods for fungicide application were assessed even though all applications in the current study were made via ground. The costs of each fungicide product and application program used in this study are presented in Table 2. Fungicide program costs were obtained from representatives of agricultural-based companies/industries manufacturing these products and by inquiring with corn growers and those who conduct custom application operations and taking the average across the three years. An average corn price of $0.17 per kilogram was used in this study, which was obtained from data provided by the United States Department of Agriculture (USDA) National Agricultural Statistics Service (NASS) (USDA-NASS 2022) for 2017 to 2021.

    Environment

    Environmental data for each location were downloaded from the cli-MATE online data portal through the Midwestern Regional Climate Center’s online weather database (https://mrcc.purdue.edu/). Data were collected to represent each year from each location (Wanatah 2 WNW, and West Lafayette 6 NW) and encompass dates that considered the growing season for each year (1 June to 1 November). The Wanatah weather station was approximately 1.2 km from the study field, while the West Lafayette weather station was approximately 1.3 km from the study field. In addition, data ormal for the respective months were downloaded to consider the overall deviation from the norm for each year. Weather data norms were based on the calculated norms between the period considering 1991 and 2020 which encompass the most recent 30-year normal. The specific environmental data considered from each location were temperature minimum and maximum (°C) and precipitation (cm).

    Data analysis

    Disease severity values recorded 15 to 19 days after tassel/silk application (DAT) at blister (R2), 24 to 27 DAT at late milk-early dough (R3/R4), 47 to 50 DAT at dent (R5), and 55 to 56 DAT at maturity (R6) growth stages were used to develop disease progress/suppression curves for the fungicide efficacy experiment. Disease severity values recorded 83 to 89 days after planting (DAP) at R2, 94 to 100 DAP at R3/R4, 118 to 124 DAP at R5, and 129 to 130 DAP at R6 were used to develop disease suppression/progress curves for the application timing experiment to visualize the effectiveness of treatment on disease severity for each site-year (location × year) over time. Additionally, the area under the disease progress curve (AUDPC) was calculated using the trapezoidal integration method as outlined by Madden et al. (2007) for disease accumulated in the lower canopy, on the ear leaf, and in the upper canopy over time and averaged across years for data analysis. AUDPCs were standardized (sAUDPC) by dividing AUDPC by the total length of the disease assessment period to make direct comparisons among tar spot epidemics over time.

    Prior to statistical analysis and to aid in the assessment of the yield response and partial economic returns from foliar fungicides and fungicide application timing, site-years were grouped into two baseline disease severity categories determined by the percent disease severity in nontreated plots at a 5% cutoff. Paul et al. (2011) proved that this subjective 5% cutoff helped to justify the significance of success in using fungicides for managing gray leaf spot (caused by Cercospora zeae-maydis Tehon & E.Y. Daniels). Based on this criterion, the two baseline disease severity categories established and used were i) high tar spot severity condition (TS high) where tar spot severity in the nontreated plots was ≥5% severity and ii) low tar spot disease severity condition (TS low) where tar spot severity in the nontreated plots was <5% severity. Following the 5% baseline disease severity criterion established for assessing yield response and partial returns, trials in Wanatah were analyzed as TS high and trials in West Lafayette as TS low.

    All data were analyzed using a generalized linear mixed model analysis of variance performed using the PROC GLIMMIX procedure in SAS (version 9.4, SAS Institute, Cary, NC) (Littell et al. 2006). In the model, fungicide treatment was considered as the only fixed effect. The random effect accounted for the heterogeneity of variance among experiments, which included an intercept along with replicate by year as the subject effect. For all analyses, a normal distribution was used with Kenward-Rogers degrees of freedom as defined as the ddfm = kr option in the model statement to account for missing observations (Littell et al. 2006). To determine which fungicide treatments (products and application timing) were most effective in managing tar spot, disease data (sAUDPC) and canopy greenness data were combined across site-years. To assess which treatment(s) offered yield protection and profitability to growers, yield data and partial returns were combined across years and analyzed based on disease severity condition groups (TS high and TS low). Treatment least-squares means (lsmeans) of fungicide treatments were computed and compared (α = 0.05). All pairwise differences among lsmeans were compared only if the F-test was significant (P ≤ 0.05) (Piepho 2012).

    Results

    Tar spot field assessments

    For both the fungicide efficacy and application timing experiment, tar spot was present at both study sites in each year except at West Lafayette in 2019, where the disease was not observed (Table 1). Additionally, disease severity was extremely low at West Lafayette in 2020 with no tar spot symptoms and 0.1% stromata on leaves consisting of approximately one or two stromata at R6; therefore, the experiments were not repeated in 2021 at West Lafayette.

    At the Wanatah location, tar spot development (% tar spot symptoms and stromata) varied across years and within the corn canopy in both experiment types (Supplementary Figs. S1 to S4). Across years, disease severity increased in the canopy over time where significantly greater disease severity was recorded in the nontreated control. In 2019 and 2021, favorable environmental conditions contributed to disease severity (% tar spot stromata) that was greater than 25% on all three canopy levels, whereas environmental conditions in 2020 were less favorable, and tar spot severity was less than 25% (Supplementary Figs. S3 and S4). However, in all years, tar spot was observed prior to the VT/R1 fungicide application, on average 49 days post-planting and between 3 and 28 days (V7 to VT growth stages) prior to fungicide application (Table 1). In the fungicide timing trial, in West Lafayette, converse to what was observed at Wanatah, tar spot was not detected in 2019 while in 2020, the disease was first observed 77 days post-planting and 6 days following the R5 application timing (Table 1).

    In the fungicide efficacy experiment, tar spot symptom severity as presented by sAUDPC was reduced at all canopy levels by all fungicide products when compared to the nontreated control (P = <0.0001) (Table 3). For the purposes of presentation in the results section, differences between treatments on tar spot symptoms and stromata were considered by comparing the reduction in symptom expression and stromata following application with each product as compared to the nontreated control in the lower canopy, on the ear leaf, and in the upper canopy. Significant reductions in symptom severity in the lower canopy were observed among fungicide products and the nontreated control and ranged from a low of 23.1% following an application of propiconazole + pydiflumetofen + azoxystrobin to a high of 51.4% following an application of prothioconazole + trifloxystrobin (Table 3). Similar reductions in symptoms were observed at the ear-leaf level within the canopy based on the specific fungicides with the lowest reduction in symptom expression (34.5% following an application of flutriafol + bixafen). Conversely, the greatest reduction of 55.5% followed an application of prothioconazole + trifloxystrobin. In general, an overall reduction in symptom expression greater than 50% when comparing the average sAUDPC of the fungicide treated plots occurred between the lower and upper canopy regardless of the active ingredient contained within the fungicide products (Table 3).

    Table 3. Effect of foliar fungicide products and application timing on tar spot management and canopy greenness in hybrid corn research trials conducted at two locations in Indiana between 2019 and 2021

    The sAUDPC associated with stromata was significantly reduced with all fungicides at all three assessed canopy levels (Table 3). The reductions in stromata ranged from a low of 21.6% to a high of 57.8% following an application of flutriafol + bixafen and prothioconazole + trifloxystrobin, respectively. The reductions in stromata at the ear-leaf level ranged from a low of 19.7% to a high of 55.3% with the same fungicide products (Table 3). The overall reductions in the sAUDPC for stromata in the upper canopy were similar to those in the other parts of the canopy; however, the greatest reduction, 49.2%, occurred following an application of mefentrifluconazole + pyraclostrobin while the lowest reduction of 20.3% occurred following an application of propiconazole and flutriafol + bixafen. Similar to the observations of symptom expression as presented as sAUDPC, the overall presentation of stromata decreased from the lower to the upper canopy regardless of the active ingredients contained in fungicides. On average, sAUDPC for stromata decreased by 34% from the lower to the upper canopy.

    In the application timing trial, the greatest significant reductions in the sAUDPC associated with symptom severity in the lower canopy, between 52.3 and 81.0%, were observed following applications at R2 and R3, respectively (Table 3). Similar reductions were observed on the ear leaf as well as in the upper canopy. In addition, the same fungicide application timings resulted in similar reductions on the ear leaf and in the upper canopy, a 50.5 to 85.4% reduction on the ear leaf and 68.8 to 96.3% reduction in the upper canopy following the R2 and R3 application timings, respectively.

    In the application timing experiment, significant reductions in the sAUDPC for stromata in the lower canopy were observed following applications made between VT/R1 and R3. The greatest reduction in sAUDPC for stromata was 49.5% following the R2 application, while the lowest, indicated by a 12.6% increase in stromata compared to the nontreated control, was observed following application at R5. Similar observations were made on the ear leaf and in the upper canopy; however, a greater overall reduction in the sAUDPC for stromata on the ear leaf was observed at R2 with a 52.2% reduction, and a 9% increase following an R5 application compared to the nontreated control.

    In the fungicide efficacy trials, the canopy was significantly greener for all fungicide products as compared to the nontreated control except mefentrifluconazole + fluxapyroxad + pyraclostrobin and flutriafol + bixafen in Wanatah and propiconazole and prothioconazole + trifloxystrobin at West Lafayette (Table 3). At Wanatah, increases in greenness compared to the nontreated control ranged from 8.4%, albeit nonsignificant, to 18.2%. The greatest increase in greenness was observed following an application of prothioconazole + trifloxystrobin (18.2%) at Wanatah and mefentrifluconazole + fluxapyroxad + pyraclostrobin (13.5%) at West Lafayette. In the application timing trial, applications made prior to R2 resulted in the least benefit to canopy greenness, except for the sequential application at V6 to V8 fb VT/R1. Observational benefits to canopy greenness at Wanatah following the applications at V6/V7 through VT/R1 resulted in a low of 0.5% following the V6/V7 application to a high of 12.9% following the V10/V11 application compared to the nontreated control. The greatest benefit to canopy greenness at the Wanatah location occurred following applications made between R2 and R5, with increases between a 28.1% benefit at R2 to a 17.7% benefit following an application made at R5 (Table 3). Fungicide applications made at the different growth stage timings at West Lafayette were not significant, and in some cases, did not enhance greenness compared to the nontreated control.

    In terms of percent symptom severity in the fungicide efficacy trial, differences were observed within the canopy (low, ear leaf, and upper) within each trial year (Table 4). By far, the greatest disease severity was observed at Wanatah in 2021. In terms of differences between years and symptom presentation within the canopy, disease was lowest in 2020; however, percent disease severity was between 4.1 and 6.5 times greater during 2019 and 7.0 and 19.2 times greater in 2021 than 2020, respectively. Similar observations were made in the fungicide timing trials; however, depending on where symptom severity was observed within the canopy, severity was between 3.6 and 6.2 times greater in 2019 than 2020 and 4.1 and 10.8 times greater in 2021 than 2020, respectively (Table 4). The observed differences in tar spot stromata were similar in both trials in that the percent severity of stromata was reduced in 2020 compared to 2019 or 2021. Differences between the years were generally between 1.0 and 2.5 times greater, with the greatest difference observed in the upper canopy of the fungicide efficacy trials during 2021 as compared to 2020 (Table 4). On average, the greatest measurable yield was observed at West Lafayette as compared to Wanatah, likely due to low levels of disease in the two years conducted in West Lafayette (Table 4).

    Table 4. Maximum disease severity (%) and yield (kg/ha) in the nontreated control at each location and year for field experiments conducted in Indiana between 2019 and 2021 to manage tar spot in two trial types

    Increases in corn grain yield differed by fungicide product applied. No significant yield differences were observed among fungicide products in TS low scenarios regardless of experiment type (Table 5). Corn grain yield was significantly increased over the nontreated control in TS high scenarios by all fungicide products except flutriafol + bixafen, which was not significantly different than the nontreated control and accounted for approximately 68% less yield than corn receiving mefentrifluconazole + pyraclostrobin, which was the treatment producing the greatest yield (Table 5). In TS low situations, between fungicide products, yield response ranged from −492.8 to 696.7 kg/ha with an average yield increase of 123.4 kg/ha. In TS high scenarios, yield increases ranged from 297.3 to 921.2 kg/ha with an average yield increase of 668.0 kg/ha (Table 5). In a low tar spot situation, only four fungicides accounted for yield increases that were less than the average of all fungicide products and nonsignificant while the remainder of the products, five, accounted for yield increases that were greater than the average and nonsignificant. Similarly, in the TS high scenario, four fungicide products produced yield that was lower than the average (668.0 kg/ha), with the remainder producing yield that was greater than the average (Table 5).

    Table 5. Least-squares means of yield response and partial returns resulting from foliar fungicide programs under low (TS low) and high (TS high) tar spot disease severity conditions from two types of foliar fungicide trials conducted in Indiana between 2019 and 2021 using ground or aerial application methods

    Increases in corn grain yield also differed among fungicide applications at different growth stages. An application of propiconazole + benzovindiflupyr + azoxystrobin did not result in significant yield increases regardless of growth stage when compared to the nontreated control in the TS low situation (Table 5). In the TS high situation, corn grain yield increase was significantly greater that nontreated control following an application of propiconazole + benzovindiflupyr + azoxystrobin made at all growth stages except at the V6/V7, V8/V9, and R5 growth stages (Table 5). Although the R5 application was not significantly different from all other application timings. The greatest yield response was observed following an application made at R2 with general reductions in yield increase declining from that growth stage point forward (Table 5). Overall, yield differences between treatments ranged from a 99.9% reduction between an application made at V6/V7 and the R2 growth stage to a 3.1% reduction in yield following an application made at R3 as compared to the R2 timing. The average response of an application of propiconazole + benzovindiflupyr + azoxystrobin regardless of application timing was 892.9 kg/ha in TS high severity situations and ranged from −502.6 to 88.9 kg/ha, while in the TS low situations, the average yield increase of −127.8 kg/ha would account for a yield loss following fungicide application (Table 5). When considering the average yield increase between the growth stage timed applications in the TS high situation and accounting for the sequential application, an average increase of 892.9 kg/ha was observed when fungicide applications were made at the less optimal timings of V8/V9, V10/V11, and R5, which produced less yield than the optimum timings of VT/R1, R2, R3, and R4 with an average yield increase of 1,291.6 kg/ha.

    Economic analysis

    Partial returns were greater in situations where high disease severity (≥5%) was observed compared to low disease severity (<5%); however, partial returns varied by product in the fungicide efficacy trial (Table 5). Even though the fungicides were applied by ground, analyses considered the partial returns based on the additional cost of aerial application.

    In the fungicide efficacy trial, no significant differences in partial returns were observed regardless of application method in TS low conditions (Table 5). The fungicide producing the greatest partial return was mefentrifluconazole + pyraclostrobin. Based on that particular product, three additional fungicides produced a significantly greater partial return when compared to the nontreated control but were neither greater nor less than mefentrifluconazole + pyraclostrobin. However, reductions in partial return were on the order of a reduction of 14.5 to 30.5% with metconazole + pyraclostrobin and prothioconazole + trifloxystrobin, respectively. The average partial return was $84.8/ha when all fungicides were averaged with four fungicides, which produced a partial return less than the average, and the remainder was between $7.7/ha and $43.2/ha greater than the average. Similar partial returns were observed when the cost of aerial application was included; however, a reduced number of fungicide products resulted in a significant increase compared to the nontreated control. Whereas four fungicides resulted in significant increases in partial ROI compared to the nontreated control by ground application, only two fungicides resulted in significant increases in partial ROI by aerial application.

    Similar to the fungicide efficacy trial, no significant differences were observed for partial returns in the TS low scenario regardless of application timing. In fact, regardless of application timing, all fungicides produced a negative partial return (Table 5). The average partial return for ground applications was −$54.5/ha and −$61.2/ha for aerial applications. However, there were significant differences observed in the TS high scenario. Significant increases in partial returns were not observed prior to the VT/R1 timing. Four application timings, VT/R1, R2, R3, and R4, resulted in significant increases in partial returns compared to the nontreated control. The greatest partial return was observed following an application made at R2, and while the applications at VT/R1, R3, and R4 did not significantly differ from the R2 application, there were minimal reductions in partial return that ranged from a 3.6 to 19% reduction in partial return from the R3 or R4 application, respectively. The average partial return in the TS high environment was $119.0/ha, with four timings producing a partial return greater than the average and the remainder of the timings, five, being less than the average (Table 5). Similar observations occurred when aerial application costs were added to the returns. However, aerial application overall would reduce the partial returns by approximately $6.7/ha.

    Environment

    The environment varied between the two study locations during the duration of the field trials (Table 6). At Wanatah, the deviation in temperature minimum and the 30-year norm was greater for 10 of 15 trial months. Conversely, the deviation in temperature maximum and the 30-year norm was greater for nine of the months (Table 6). Temperature at West Lafayette was similar to Wanatah with temperature increases in nine of the 10-month duration of the trials. The average of either minimum or maximum temperature was greater than the 30-year norm for four of the five site-years with increases ranging from a low of 1.2% for the maximum temperature at Wanatah in 2020 to a high of 15.1% for the minimum temperature at Wanatah in 2021. The only average temperature decrease over the three years was a 0.4% decrease in maximum temperature at Wanatah in 2019.

    Table 6. Environmental variables presented as the minimum and maximum temperature (°C) and precipitation (cm) for each location and year along with the deviation from the 30-year normal from locations where tar spot management trials were conducted in Indiana during 2019, 2020, and 2021

    Rainfall increases compared to the 30-year norms were recorded at Wanatah during 2019 and 2021 and ranged from a 2.3 to 18.9% increase in the rainfall received over the 5-month period for the respective year. However, decreases in rainfall at Wanatah and West Lafayette ranged from 3.0 to 28.7% of the 30-year norm in 2019 in West Lafayette and 2020 in Wanatah, respectively (Table 6). Supplemental irrigation was applied to the efficacy trials in Wanatah when rainfall totals did not equal 25.4 mm for the week during the season, which would have limited the influence of the reduced rainfall recorded in both 2019 and 2020 for this trial location.

    Discussion

    A multifaceted disease management program is necessary for tar spot under heavy disease pressure. Hybrid resistance will be key for long-term tar spot management, although at present there is a lack of knowledge on hybrid resistance. Limited partial resistance has been observed, while the bulk of the commercial hybrids available are susceptible (Singh et al. 2023; Yan et al. 2022). Fungicides are currently the most effective tool available for managing tar spot in hybrid corn. Several fungicide products have been labeled for tar spot, and a list of available products with relative efficacy against tar spot and additional foliar diseases of corn is available based on research by unbiased extension and research professionals across the corn belt (Crop Protection Network 2022b). In previous published reports, several fungicide products were proven to be effective in reducing tar spot foliar symptoms while protecting yield (Telenko et al. 2022a, b). Even though several years of tar spot research have been conducted prior to the current report, there continue to be gaps in information regarding the most efficacious application timings for managing tar spot. Conducive environmental conditions favored the development of tar spot in Wanatah and contributed to disease severity reaching a maximum of 100% for tar spot symptoms and >30% for stromata severity across years in the nontreated plots. Contrastingly, less-than-favorable environmental conditions as well as reduced levels of inoculum in West Lafayette resulted in disease severity reaching a maximum 0.3% for tar spot symptoms and <1.0% for stromata severity. Temperature that ranges from 16 to 23°C and relative humidity greater than 75% have been reported to be necessary for tar spot development (Hock et al. 1995; Valle-Torres et al. 2020; Webster et al. 2023). The increase in total rainfall received in Wanatah as well as the presence of residue-based inoculum during the 2021 season greatly influenced tar spot development and severity. Even with a reduction in the total rainfall received during September 2021, tar spot still reached severe levels in the lower-to-middle canopy. In this year the disease was initially observed at the earliest date of the three-year study (9 July 2021). The temperatures were also slightly elevated as compared to those previously reported to be conducive for disease development, 1.7 to 2.0°C in August and September, when compared to the 30-year normal at Wanatah. Environment influences the incidence and severity of most plant diseases. However, in the case of tar spot, while environment can increase disease incidence and severity, a general source of inoculum typically in the form of residue from the previous season is necessary for the disease to initiate each season (Groves et al. 2020).

    Assessment of disease progress over time showed an increase in disease severity (tar spot stromata) in the canopy where severity of tar spot was consistently greater in the nontreated plots. Results from analysis of variance of the sAUDPC determined that all fungicide products applied at VT/R1 were significantly effective in reducing tar spot severity compared to the nontreated control. In addition, fungicides effectively reduced disease on the ear leaf and in the upper canopy as compared to the lower canopy during reproductive growth stages, which relates to the most important parts of the canopy for protecting yield (Mallowa et al. 2015). The current research provided results which were consistent with previously published reports, which concluded that the fungicides evaluated significantly reduced tar spot severity on the ear leaf compared to the nontreated control (Telenko et al. 2022a, b). Fungicides usually protect the leaves to which they are applied for approximately 14 to 21 days depending on product and class of chemistry; however, some of the most recently released fungicide products (circa 2021) that contain members of the SDHI class appear to provide greater residual efficacy depending on the targeted pathogen (T. W. Allen, unpublished data; Mueller et al. 2013). These data therefore suggest that the effectiveness of fungicides to provide protection against tar spot will not only depend on the active ingredients within a given product but will also rely strongly on appropriate application timing to prevent disease and thereby protect yield more effectively. However, application timing to effectively manage tar spot and produce the greatest yield benefit may differ from the more general VT/R1 application timing, which has become popular through the enhanced marketing of the QoI compounds that has occurred since 2006 (Mallowa et al. 2015; Paul et al. 2011; Wise and Mueller 2011; Wise et al. 2019). Our results suggest that applications made at R2 or even as late as R3 produced the greatest yield benefit and subsequent economic return in tar spot high disease situations. In fact, previously published research suggested applications made within this application window provided protection to leaves in the upper canopy and ensured photosynthetic activity continued to benefit the corn plant through important grain fill stages (Abendroth et al. 2011; Maddonni et al. 1998; Mallowa et al. 2015; Munkvold 1997). Moreover, it should be noted that the bulk of the research that suggested the VT/R1 timing was the most effective was based on results using DMI fungicides that were commercialized in the 1990s, which was prior to the release of some of the more commonly used fungicides in the early 21st century. In addition, prior to the current results, fungicide applications at VT/R1 timings were targeted for tar spot management. Most importantly, fungicide application timing may differ for specific disease-causing organisms. For example, when considering management of southern rust (caused by Puccinia polysora Underwood), fungicide applications at the VT/R1 timing provide greater disease control than later application timings (Faske and Emerson 2021). Based on our current results, the reevaluation of fungicide application timing when tar spot severity threatens yield appears to have produced results which should aid in providing economical results in commercial corn production settings. However, future research should consider an additional timing of fungicide application based on predictive modeling (Webster et al. 2023).

    In the current study, results from the application timing experiment determined that the use of propiconazole + benzovindiflupyr + azoxystrobin was most effective at reducing tar spot severity with a single application at or between VT/R1 and the R4 growth stage or a sequential application between V6 and V8 fb VT/R1 over the nontreated control. Applications made prior to the VT/R1 growth stage were too early to provide residual efficacy and reduce disease progression for the remainder of the season. In fact, in some instances, fungicide applications preceded the onset of disease such as those applications made at the V6/V7, V8/V9, and V10/V11 growth stages. In instances where the fungicide was applied prior to disease onset, the residual efficacy of the fungicide likely dissipated prior to significant disease development in the canopy. Likewise, fungicide applied after the R4 growth stage was less effective in suppressing disease severity in the canopy. For example, the R4 applications in Wanatah in 2020 and 2021 were made after the pathogen was established in leaf tissue for between one and two months, and based on the presentation of the disease progress curves, this rendered these applications less efficacious. As a result of these observations, making an appropriately timed fungicide application is necessary for tar spot management and largely depends on the environmental conditions encountered throughout the growing season as well as field history as it relates to the previous tar spot incidence. The application window between VT/R1 and R4 identified for propiconazole + benzovindiflupyr + azoxystrobin may vary with the use of alternative fungicide products, different locations, varying disease pressure, and susceptibility of a corn hybrid to tar spot (Coulter 2010; Wise and Mueller 2011).

    Apart from disease control, certain fungicide classes have previously been reported to provide physiological advantages such as promoting what has more generally been referred to as “plant health” or acting to prolong green plant tissue within the crop canopy, often referred to as “stay green,” by promoting the growth hormone cytokinin and delaying or suppressing ethylene biosynthesis, which plays a role in senescence (ripening) (Grossmann and Retzlaff 1997; Paul et al. 2011). Generally, in our study, more green leaf tissue was observed in the crop canopy with all fungicide products and applications of propiconazole + benzovindiflupyr + azoxystrobin at the V10/V11, R2, R3, R4, and R5 growth stages compared to the nontreated control. The greener crop canopy may be attributed to the fungicide slowing disease progression. Consequently, more of the crop canopy is producing photosynthates for grain fill and thus contributing to yield potential. One interesting observation from our current study was greater overall crop canopy greenness in tar spot low situations (<5%) with several fungicide products at the West Lafayette location. Numerous reports have been made regarding the effect of foliar fungicide applications on “plant health” by delaying senescence (Bradley et al. 2008; Byamukama et al. 2013; Weisz et al. 2011). A major marketing strategy of chemical companies has been to promote fungicide application to increase photosynthesis whereby yield benefits or increases that translate into economic gain would be expected. In contrast, most university researchers promote foliar fungicide applications to profitably offset losses associated with plant diseases and not as a method to simply increase yield in the absence of disease; something more along the lines of integrated pest management or “apply as needed” in situations where yield losses that result from yield-reducing diseases are oftentimes prevented. Our results were clear in that the crop canopy was significantly greener than the nontreated control in tar spot high situations as compared to the tar spot low situations. Moreover, even though application of some specific fungicide products at the West Lafayette location resulted in a greener crop canopy, that did not translate into positive ROI compared to the nontreated control. In fact, economically speaking, the greener plant tissue translated into losses in value which did not offset the cost of the fungicide or application.

    Even though all fungicide active ingredients significantly reduced tar spot severity over the nontreated control, not all fungicide products consistently translated into significant yield benefits especially with varying disease severity. For example, all fungicide products except flutriafol + bixafen resulted in significantly greater yield increases over the nontreated control under high disease severity conditions. Conversely, no yield differences were observed among treatments when low disease severity conditions were encountered. Additionally, significant yield increases were observed only with application of propiconazole + benzovindiflupyr + azoxystrobin made at the V10/V11, VT/R1, R2, R3, R4, and the sequential application between V6 and V8 fb VT/R1 over the nontreated control when high disease severity conditions occurred. These results are consistent with several published technical reports on the impact of fungicides on tar spot which reported a limited number of fungicides protected yield over the nontreated control (Ames and Kleczewski 2020; Chilvers et al. 2019; Da Silva et al. 2020a, b, 2021b; Ross et al. 2020a, b, 2021a, b; Telenko et al. 2019b; Waibel et al. 2021a, b). Yield response varied among fungicide products as well as between disease severity conditions. Consistently negative yield responses were observed under TS low conditions, while consistently positive yield responses occurred under TS high severity. The average yield increase among fungicide products evaluated accounted for 123.4 kg/ha greater yield in the low disease situations and 668.0 kg/ha greater yield in high disease situations. However, average yield was different in the application timing study where only a single fungicide production was applied. In low TS scenarios, an overall loss of yield was observed on the order of −127.8 kg/ha as compared to the nontreated control. Our results suggest that corn producers should ultimately scout their corn fields and consider field history since knowing the level of tar spot over a period of years is important to understand the contribution of residue in a field and how that contributes to disease progression in the presence of a conducive environment. On average, yield increase across fungicide products was 544.6 kg/ha greater, and timed applications was 1,020.7 kg/ha greater when disease severity was high relative to when disease severity was low. Our results related to the level of disease in field situations, whether low or high, are similar to those previously reported whereby corn generally responds more positively in situations where the fungicide is managing a foliar disease (Mallowa et al. 2015; Paul et al. 2011).

    Nevertheless, one of the more important considerations for corn farmers to make prior to fungicide application is whether or not yield protection is enough to offset the cost of the fungicide based on the product and method of application. Our current results provide guidelines through examination of partial returns resulting from the purchase of the fungicide product in addition to the associated application costs under both low and high disease severity conditions. Positive returns from fungicide use are more common when disease severity is high (Faske and Emerson 2021; Paul et al. 2011; Wise et al. 2019). Under low disease severity, fungicide application is not likely to be profitable and thus may have little direct impact on enhancing ROI (Johnson 1987; Mallowa et al. 2015; Paul et al. 2011; Wise et al. 2019). In the current study, 44.4% of the fungicide applications resulted in positive partial ROI when disease severity was low; however, all fungicides resulted in positive partial ROI when disease severity was high based on the costs of application associated with either a ground or aerial method. In general, while sometimes more convenient, aerial application adds $6/ha to the cost of a fungicide application but may allow application to the field when conditions limit ground access; however, aerial application may not be as efficacious when considering a disease that has been reported to begin in the lower canopy (Penney et al. 2021; Valle-Torres et al. 2020; Webster et al. 2023). On average, the partial return from foliar fungicides using either a ground or aerial application method was $92.6/ha greater when the severity of tar spot was high relative to when severity was low. For the fungicide applications made at different growth stages, the average partial ROI based on the costs associated with a ground or aerial method was $173.5/ha greater when tar spot severity was high relative to when the severity was low. These greater returns are a result of more substantial yield differences recorded when high tar spot severity conditions were observed compared to the recorded yield when disease severity was low. The current study demonstrates that foliar fungicides and appropriately timed fungicide applications could be used profitably to manage tar spot in Indiana, but the profitability of a positive partial ROI is more likely under high disease conditions. Our results are consistent with previous research that assessed the economical use of fungicides on corn (Johnson 1987; Tedford et al. 2017; Wise et al. 2019). Nevertheless, the partial returns in the current study are based on a deterministic model method and thus stochastic model methods could be use in the future to forecast the variations of prices in fungicide cost and grain and resulting returns in real-time and consider whether a conducive environment may lead to increases in tar spot.

    Our current results are the first economic analysis of net return and yield response of hybrid corn following foliar fungicide applications in Indiana under different tar spot severity conditions. The results of our analysis determined that fungicide application did not produce a yield benefit when applied in instances where limited tar spot occurred. Given that corn growers tend to apply fungicides based on perceived economic benefit (Rosburg and Menapace 2018), growers should use these current results to help guide fungicide application decisions and lean toward applications in situations when tar spot severity threatens yield. As a result of our research and the corresponding data analysis, it is evident that a two-fungicide application program may not be needed, but if growers decide to make two applications, the potential costs associated with the second application will greatly reduce the likelihood of a positive ROI. Nevertheless, it is important to note that these results may change with different fungicide products, locations, given cropping year, and the susceptibility of a given commercial hybrid to tar spot. Hence, additional research is needed to determine the efficacy of new products as they become commercially available, risk for resistance development within the pathogen population, and optimum timing of each fungicide product to help Indiana corn growers.

    Acknowledgments

    The authors thank J. Ravellette and D. M. Telenko at Purdue University for assistance with the field trial maintenance.

    The author(s) declare no conflict of interest.

    Literature Cited

    Funding: This research was supported by the Indiana Corn Marketing Council (ICMC); the Foundation for Food and Agricultural Research-Rapid Outcomes from Agricultural Research (FFAR-ROAR; award 18 #0000000017) grant with matching funds provided by Pioneer Hi-Bred, the National Corn Growers Board, the Illinois Corn Growers Association, and Purdue University; and the USDA National Institute of Food and Agriculture hatch project #IND00162952.

    The author(s) declare no conflict of interest.