Revista de la Facultad de Ciencias Agrarias. Universidad Nacional de Cuyo. En prensa. ISSN (en línea) 1853-8665.

Original article

Fungicide management of late leaf spot and peanut smut

Uso de fungicidas para el manejo de la viruela tardía y del carbón del maní

Damian Francisco Giordano¹ ^*^,²,

Agostina Del Canto¹,

Jessica Gabriela Erazo¹,

Nicolas Alejandro Pastor¹,

Ana Cecilia Crenna¹^,²,

Melina Rosso³,

Adriana Mabel Torres¹,

Claudio Marcelo Oddino¹^,²^,³

¹ Universidad Nacional de Río Cuarto (UNRC). Instituto de Investigación en Micología y Micotoxicología (IMICO). Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). 5800. Ruta Nacional 36 km 601. Río Cuarto. Cordoba. Argentina.

² Universidad Nacional de Río Cuarto (UNRC). Facultad de Agronomía y Veterinaria. Departamento de Biología Agrícola.

³ Criadero El Carmen. 5809. Av. Italia 871. General Cabrera. Córdoba. Argentina.

* dgiordano@exa.unrc.edu.ar

Abstract

Late leaf spot (LLS), caused by Nothopassalora personata, is the most devastating peanut disease in the world. In Argentina, peanut smut (Thecaphora frezii) has increased significantly in recent decades. LLS is mainly managed through chemical fungicides, however, peanut smut is not effectively controlled, except for some resistant peanut genotypes. This study evaluated the effects of widely used fungicides for LLS control on both diseases and crop yield. Field trials were conducted over three consecutive years in two locations, with different fungicide doses and number of applications. Disease intensities were significantly higher in General Cabrera (GC) than in Vicuña Mackenna (VM) resulting in higher yields in VM. This could be due to the longer history of peanut cultivation in GC, where fungicide applications reduced LLS intensity. Among fungicides, chlorothalonil showed the best performance. However, these treatments were ineffective against peanut smut, likely due to difficulties reaching the infection site. Considering fungicides are one major management tool, further study of different active ingredients against both diseases should also consider sustainable integrated management.

Keywords: Arachis hypogaea, chemical control, fungal diseases, Nothopassalora personata, Thecaphora frezii

Resumen

La viruela tardía (VT) ocasionada por Nothopassalora personata es la enfermedad del maní más desvastadora a nivel mundial, mientras que el carbón (Thecaphora frezii), es la enfermedad con mayor incremento en Argentina en las últimas décadas. VT es principalmente manejada a través de fungicidas químicos, mientras que, para el carbón del maní, no existen herramientas efectivas, salvo algunos genotipos resistentes. En este trabajo, se evaluó el efecto de fungicidas ampliamente utilizados para el control de VT, sobre ambas enfermedades y sobre el rendimiento del cultivo. Los ensayos de campo fueron realizados en dos localidades por tres años consecutivos, donde se probaron fungicidas en diferentes dosis y número de aplicaciones. La intensidad de ambas enfermedades fue más alta en General Cabrera (GC) que en Vicuña Mackenna (VM), resultando en mayores rendimientos en VM. Esto se debió posiblemente al mayor historial de producción de maní en GC, donde la aplicación de fungicidas redujo la intensidad de VT. Entre los fungicidas, clorotalonil demostró la mejor performance. Sin embargo, estos tratamientos no fueron efectivos frente al carbón del maní, posiblemente debido a no alcanzar el sitio de infección. Teniendo en cuenta que los fungicidas son una de las principales herramientas de manejo, se necesitan más estudios de diferentes ingredientes activos sobre ambas enfermedades, considerando un manejo integrado sustentable.

Palabras clave: Arachis hypogaea, control químico, enfermedades fúngicas, Nothopassalora personata, Thecaphora frezii

Originales: Recepción: 11/02/2024 - Aceptación: 16/10/2024

Introduction

Peanut (Arachis hypogaea L.) world production exceeds 49 million metric tons in pods. This oilseed is cultivated in over 100 countries, but approximately 80% of the production is concentrated in 10 countries, with China leading 18 million metric tons annually. Argentina is the tenth peanut producer with more than 950.000 metric tons, and the second exporter, with 16% of worldwide production. The province of Córdoba is the largest producer, accounting for 80% of the national output ⁽³²⁾.

Several diseases affect peanut production in Argentina and other countries. Early leaf spot (ELS) caused by Passalora arachidicola (Hori) and late leaf spot (LLS) caused by Nothopassalora personata (Berk. & Curtis) are the most important foliar diseases worldwide, being LLS the most frequent in some main producing regions ⁽^{14, 24}⁾. These diseases can generate important yield losses, and consequent economic imbalance ⁽²⁾. On the other hand, peanut smut by Thecaphora frezii (Carranza & Lindquist) has become the most important soil-borne disease in Argentina due to recent increasing prevalence and intensity ⁽³⁰⁾, causing significant yield losses ⁽²⁵⁾. LLS benefits from rainfall ⁽¹⁶⁾, while smut typically thrives under drought conditions, particularly during grain filling ⁽²⁸⁾.

Even though different tools aim to control LLS, its management relies mainly on chemical fungicides ⁽¹⁷⁾ like systemic single-site mode carboxamides, strobilurins and triazoles. Many studies have shown beneficial effects of using fungicide mixtures from different chemical groups, mainly with carboxamides ⁽^{10, 23}⁾. Among contact fungicides with multiple modes of action, the majorly used chlorothalonil presents consistent results ⁽⁹⁾. However, other options must be considered given that some active ingredients (a.i.) may soon be prohibited or useless against resistant strains.

Different management strategies have been tested against peanut smut, without successful effects on intensity. On the other hand, genetics have contributed resistant varieties ⁽⁵⁾: EC - 191 RC (AO), EC - 394 RC (AO) and EC - 420 RC (AO) ⁽²⁾, still grown only on a reduced area of the country. Meanwhile, biological control agents have proven useful regarding disease severity and grain weight at field scale ⁽¹⁵⁾, although still mostly preliminary. Regarding chemical control, many fungicide groups have shown variable results ⁽^{8, 22}⁾. Such variability in disease control may be due to low fungicide efficacy or the impossibility of accessing gynophores, the infection site for T. frezii ⁽²⁰⁾. Considering this, Paredes et al. (2021) tested 12 different a.i. in vitro, pots and field trials, using 1.5 times the recommended dose for the LLS control. Fungicides were applied at night directly to the plant base and pegs in pot trials and targeting the soil in field trials. These authors observed high disease control with azoxystrobin (strobilurin) in pots and a 2016 field trial, and with cyproconazole (triazole) in a 2015 field trial, while chlorothalonil did not control peanut smut, probably given its limited mobility in the plant compared to the other a.i. ⁽⁶⁾. The one product registered against peanut smut, composed of two triazole fungicides (triadimenol and myclobutanil), is ineffective against LLS ⁽¹⁹⁾.

Currently, chemical control of fungal pathogens can be achieved by different target site fungicides, depending on their mode of action. Fungicides with varying modes of action can be used mixed or in alternating regimes on the same crop. Before testing new a.i. against a given disease we should evaluate efficacy of currently registered fungicides. Another key aspect is to evaluate dose and number of applications with the lowest environmental impact. If some a.i. registered for LLS could impact smut, a simultaneous control of both diseases would be highly beneficial. Thus, we evaluated the effect of widely used fungicides against LLS in peanut crops, simultaneously considering LLS and smut intensities, and crop production.

Materials and methods

Field trials were conducted during three consecutive seasons, 2017/18, 2018/19 and 2019/2020, in General Cabrera (GC) and Vicuña Mackenna (VM), Córdoba, Argentina (table 1). GC is representative of the historical peanut-producing area, while in VM, peanut has been recently introduced. They have loam and sandy loam soil texture, respectively.

Table 1. Coordinates, sowing and harvest dates and accumulated rainfalls at both locations for three agricultural seasons.

Tabla 1. Coordenadas, fechas de siembra y cosecha y precipitaciones acumuladas para ambas localidades durante las tres campañas agrícolas.

GC: General Cabrera. VM: Vicuña Mackenna.

All trials followed a randomized complete block design with three replications, and four furrows 5 m long, spaced 0.70 m. Ten treatments were composed of different a.i. or mixtures, doses, and number of applications (table 2).

Table 2. Treatments at both locations during three agricultural seasons.

Tabla 2. Tratamientos en ambas localidades durante tres campañas agrícolas.

g a.i/ha: grams of active ingredient per hectare.

Gramos de ingrediente activo por hectárea.

All fungicides are registered in Argentina for LLS control ⁽⁷⁾. Applications were performed with a carbon dioxide pressurized backpack sprayer equipped with six hollow cone spray nozzles spaced 0.35 m apart, calibrated to 180 L/ha. Applications began upon the first symptoms of LLS. Seeds of cv. Granoleico (INASE Reg. N° 7907) were treated with 2.5 g (a.i.) of ipconazole + 2 g of metalaxyl and 30 g of carboxin + 30 g of thiram per 100 kg of seeds, preventing other soil pathogens and those carried by seeds.

Treatments 2, 3 and 4 implied using fungicides in the registered doses and number of applications, considering residual periods. Treatments 5, 6 and 7 maintained doses but reduced applications. Finally, treatments 8, 9 and 10, reduced a.i. dose to 60% of the recommended. Treatments 5, 6, 7, 8, 9 and 10 tested whether a different dose and application number was as efficient as the registered, representing a more interesting option for peanut producers. However, risks of generating resistance must be considered at reduced doses that should not be massively adopted (as in treatments 8 to 10) ⁽¹⁾. For all cases, the Environmental Impact Quotient (EIQ) was calculated according to Kovach et al. (1992), determining the environmental impact for each a.i. based on physicochemical and toxicological information. This widely used indicator evaluates pesticide risks and is useful for selecting less harmful molecules ⁽¹³⁾.

Before harvest, two cotyledonary branches per plot were collected (one branch per central furrow) and LLS intensity was calculated through incidence and severity. The first represents the percentage of diseased leaflets and the last considers the percentage of affected tissue. Incidence was calculated as the number of leaflets with LLS spots over the total number of leaflets. Severity (S) was calculated through the equation proposed by Plaut and Berger (1980): S = [(1-D) * Sx] + D, considering defoliation (D), and average severity (Sx) (calculated by a diagrammatic scale) ⁽³¹⁾.

At harvest maturity (150 days after planting), all plants in 1 m² per plot were collected. Pods were separated and allowed to dry until constant weight, in a dry and ventilated place. Once weighted and shelled, yield was estimated via total and confectionery quality weights, considering confectionary quality as those grains greater than 7,5 mm sieve size. Simultaneously, peanut smut incidence (percentage of affected pods) and severity (degree of symptoms in pods, through the disease severity index (DSI)) ⁽²⁷⁾ were evaluated. The DSI involves a five levels scale: 0 = healthy pod, 1 = normal pod with a small sorus in a single seed, 2 = deformed or normal pod with one seed half affected, 3 = deformed pod and a completely smutted seed, 4 = deformed pod, both seeds completely smutted. The DSI was calculated using the following equation:

where:

n = number of pods corresponding to each level (0-4)

N = total number.

For all parameters, ANOVA was performed, and means were compared using Tukey’s test (p ≤ 0.05) with InfoStat software ⁽¹²⁾.

Results and Discussion

According to a.i., concentration, dose and number of applications, EIQ values per treatment were: 1=0, 2=17.16, 3=21.80, 4=202.5, 5=8.58, 6=10.9, 7=121.23, 8=10.29, 9=13.08, and 10=121.5.

During the first year, LLS was not observed given environmental conditions, mainly precipitation ⁽²¹⁾. For the other campaigns, the disease appeared in both locations with higher intensity values in GC. In the GC 2018/19 trial (figure 1A), the lowest incidence levels were observed with chlorothalonil in five applications (treatments 4 and 10), while severity was higher only in the control (treatment 1). This agrees with Culbreath et al. (2018), who found chlorothalonil more efficient than almost all evaluated triazoles. Concerning the 2019/20 trial, treatment 4 had, once more, the best performance.

Treatments: 1) untreated control; 2) pyraclostrobin + epoxiconazole four times, 3) fluxapyroxad + epoxiconazole + pyraclostrobin four times; 4) chlorothalonil five times; 5) pyraclostrobin + epoxiconazole twice; 6) fluxapyroxad + epoxiconazole + pyraclostrobin twice; 7) chlorothalonil three times; 8) pyraclostrobin + epoxiconazole four times, reduced dose; 9) fluxapyroxad + epoxiconazole + pyraclostrobin four times, reduced dose; and 10) chlorothalonil five times, reduced dose. Different letters indicate significant differences (p<0.05).

Tratamientos: 1) control sin fungicida; 2) pyraclostrobin + epoxiconazole 4 aplicaciones; 3) fluxapyroxad + epoxiconazole + pyraclostrobin 4 aplicaciones; 4) clorotalonil 5 aplicaciones; 5) pyraclostrobin + epoxiconazole 2 aplicaciones; 6) fluxapyroxad + epoxiconazole + pyraclostrobin 2 aplicaciones; 7) clorotalonil 3 aplicaciones; 8) pyraclostrobin + epoxiconazole 4 aplicaciones, dosis reducida; 9) fluxapyroxad + epoxiconazole + pyraclostrobin 4 aplicaciones, dosis reducida; y 10) clorotalonil 5 aplicaciones, dosis reducida. Letras diferentes indican diferencias significativas (p<0,05).

Figure 1. Incidence and severity of late leaf spot in 2018/19 and 2019/20 on General Cabrera (A) and Vicuña Mackenna (B) field trials.

Figura 1. Incidencia y severidad de viruela tardía en 2018/19 y 2019/20 en los ensayos de campo de General Cabrera (A) y Vicuña Mackenna (B).

However, other treatments, like treatment 4, achieved lower incidence (5: pyraclostrobin + epoxiconazole in 2 moments, and 7: chlorothalonil in 3 moments), and severity (3 and 9: fluxapyroxad + epoxiconazole + pyraclostrobin in 4 moments) levels. These last results show effective disease management with mixes including carboxamides, and better behavior with shorter periods between applications, as previously found ⁽^{10, 23}⁾. Treatments 8 to 10, with a.i. in reduced doses, achieved effective LLS control. However, it should not constitute a strategy to be applied solely due to the possibility of creating fungal resistance ⁽¹⁾. Nevertheless, treatments with fewer applications and thus, lower EIQ, represent a good option considering environmental risk ⁽¹³⁾. Another interesting fact is that treatments 4 and 10, with chlorothalonil, led to better control than other a.i., but with higher EIQ values. However, this a.i. has significantly low selection pressure (Fungicide Resistance Action Committee, Code M5). On the other hand, no differences were evidenced among VM treatments (figure 1B), probably because of the low disease intensity registered in that location. However, the highest LLS incidence and severity were observed without fungicides (treatment 1).

Thecaphora frezii field inoculum was quantified before planting according to Marinelli et al. (2008), estimating 10000 and less than 2000 teliospores per gram of soil in GC and VM, respectively. Given this disease is less dependent on weather conditions than LLS, we could evaluate smut intensity during three seasons in both locations ⁽²⁷⁾. Intensity was high in GC and moderate in VM (figure 2A and 2B), incidence reached 72.08% and severity 2.34 in GC, while in VM, maximum values were 22.66% and 0.55, respectively. These results may depend on GC long history of peanut cultivation and processing, and thus, high inoculum ⁽²⁷⁾.

Figure 2. Incidence and severity of peanut smut in 2017/18, 2018/19 and 2019/20 in General Cabrera (A) and Vicuña Mackenna (B) field trials.

Figura 2. Incidencia y severidad de carbón del maní en 2017/18, 2018/19 y 2019/20 en los ensayos de campo de General Cabrera (A) y Vicuña Mackenna (B).

We did not observe fungicide effect on disease intensity when compared to the untreated control throughout all trials. Some authors ⁽^{3, 4, 33}⁾ cite the action of chlorothalonil, triazoles, strubilurins and carboxamides for controlling soil pathogens. However, for peanut smut, effects are variable probably because of low efficacy or inability to reach gynophores through spraying ⁽^{8,
20, 25}⁾. We evaluated fungicides with different mobility in plants: a non-penetrating a.i. (chlorothalonil) that cannot translocate through tissues and penetrant and mobile a.i. (epoxiconazole, pyraclostrobin and fluxapyroxad) transported through the xylem ⁽⁶⁾. These mobility differences could help these a.i reach gynophores and stop infections. Paredes et al. (2021) observed lower severity with azoxystrobin when compared to other fungicides and control pots. On the other hand, smut intensity in untreated control did not differ from treatments with chlorothalonil and pyraclostrobin. These outcomes align with our findings. Finally, in field trials, cyproconazole and azoxystrobin showed the best control efficiency among all treatments.

Since peanut smut intensity is directly related to crop production losses ⁽²⁵⁾, and no significant effect of fungicides was observed on the former, we expected no differences in yield (table 3).

Table 3. Peanut yield parameters (kg/ha) recorded in General Cabrera (GC) and Vicuña Mackenna (VM) for the three agricultural seasons.

Tabla 3. Parámetros de rendimiento de maní (kg/ha) medidos en General Cabera (GC) y Vicuña Mackenna (VM) para las tres campañas agrícolas.

Pod (P.), grain (G.) and confectionery quality grain (C.Q.) yields (kg/ha). Means ± standard deviation. Treatments: 1) untreated control; 2) pyraclostrobin + epoxiconazole four times; 3) fluxapyroxad + epoxiconazole + pyraclostrobin four times; 4) chlorothalonil five times; 5) pyraclostrobin + epoxiconazole twice; 6) fluxapyroxad + epoxiconazole + pyraclostrobin twice; 7) chlorothalonil three times; 8) pyraclostrobin + epoxiconazole four times, reduced dose; 9) fluxapyroxad + epoxiconazole + pyraclostrobin four times, reduced dose; and 10) chlorothalonil five times, reduced dose. Significant differences (p<0.05) per column are represented by *.

Rendimientos (kg/ha) de vainas, granos y granos calidad confitería. Medias ± error estándar. Tratamientos: 1) control sin fungicida; 2) pyraclostrobin + epoxiconazole 4 aplicaciones; 3) fluxapyroxad + epoxiconazole + pyraclostrobin 4 aplicaciones; 4) clorotalonil 5 aplicaciones; 5) pyraclostrobin + epoxiconazole 2 aplicaciones; 6) fluxapyroxad + epoxiconazole + pyraclostrobin 2 aplicaciones; 7) clorotalonil 3 aplicaciones; 8) pyraclostrobin + epoxiconazole 4 aplicaciones, dosis reducida; 9) fluxapyroxad + epoxiconazole + pyraclostrobin 4 aplicaciones, dosis reducida; y 10) clorotalonil 5 aplicaciones, dosis reducida. Las diferencias significativas (p<0,05) dentro de la misma columna, están representados con *.

In GC, differences in grain and confectionery quality grain yields were observed during the 2017-2018 season, where the untreated control presented higher production than other treatments. These results could be given by decreased yield when fungicides are applied to stressed plants ⁽¹¹⁾. Treatments 1 (untreated control), 2, 3 and 5 had the highest total grain yield (864, 892, 917 and 914 kg/ha, respectively), and confectionery quality grain yield (757, 804, 791 and 792 kg/ha, respectively).

On the other hand, during the 2018-2019 season, treatments 3 and 10 showed the highest grain yield (3354 and 3362 kg/ha, respectively) and confectionery quality yield (2860 and 2996 kg/ha, respectively). Both treatments achieved lower LLS intensity than control, as previously found ⁽^{9, 23}⁾. Finally, during the 2019-2020 season, no statistical differences were found for productivity parameters in GC. For VM trials, statistical differences for crop yield were only found in the 2019-2020 season. Treatment 1 had 22-49%, 25-50% and 40-58% lower values than the rest of the treatments for pod, grain and confectionery quality grain yields, respectively. In contrast, treatment 3 had 18-53% and 19-50% higher pod and grain yields than the other treatments. Finally, the difference between treatments 1 and 3 was approximately 100%, as found by Culbreath et al. (2018).

Considering each season, results were statistically different between locations. Table 4 shows markedly higher LLS and peanut smut incidence and severity in GC than in VM.

Table 4. LLS intensity, peanut smut intensity and crop yield, across trials.

Tabla 4. Intensidad de VT, carbón del maní y rendimiento del cultivo a lo largo de los años.

^a Late leaf spot. ^b Pod yield. ^c Grain yield. ^d Confectionery quality grains yield. Comparison between locations partitioned by year. Different letters represent significant differences (p<0.05).

^a Viruela tardía. ^b Rendimiento en vainas. ^c Rendimiento en granos. ^d Rendimiento en granos calidad confitería. Comparación entre localidades, particionadas por año. Letras diferentes representan diferencias significativas (p<0,05).

Although Paredes et al. (2024) report that peanut smut benefits from drought, we did not observe any correlation between the highest intensities and lowest rainfall, except for GC when comparing the first and second seasons. However, this behavior is not linear and depends on whether soil moisture falls below 30% of soil water-holding capacity and on which growth stage ⁽²⁸⁾. Regarding yield, all values were superior in VM for all years. Disease intensity and crop yield are possibly explained by cultivation history in each area.

Fungicide application leads peanut LLS management. Additionally, considering peanut smut is hard to control, having a fungicide against both diseases simultaneously would be significantly useful. Considering two different sites and three cropping seasons, this study showed how some majorly used fungicides for peanut crops in Argentina could control LLS even at lower doses and application frames than usual. However, these treatments proved no effects against peanut smut. Further testing should consider different a.i., their combinations, doses and application frames against LLS and peanut smut. Additionally, considering genetic resistance and biocontrol strategies with microorganisms is key for integrated management strategies.

Conclusions

Disease intensities of late leaf spot (LLS) and peanut smut are closely linked to the agricultural history of locations and weather conditions in a certain season. Chemical control of LLS has been effective, and certain options exhibit a lower environmental impact, particularly important for integrated management strategies. Conversely, fungicides demonstrated inefficacy against peanut smut in these field trials. We also demonstrated the importance of quantifying inoculum density given its direct relationship with disease levels to avoid certain locations or choose resistant varieties. Further studies on the biology of T. frezii and management of peanut smut should contribute to genetic resistance development.

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