*Corresponding author: acervantes@utmachala.edu.ec

Keywords:

Severity

Chemical control

Musaceae

Streaks

Leaf spot

Evaluation of fungicides used in the management of black Sigatoka in banana cultivation

Evaluación de fungicidas utilizados en el manejo de Sigatoka negra en el cultivo de banano

Avaliação de fungicidas utilizados no manejo da Sigatoka negra na bananicultura

Abrahan Rodolfo Cervantes-Álava

Adriana Beatriz Sánchez-Urdaneta

2,3

Ciolys Beatriz Colmenares de Ortega

José Nicasio Quevedo-Guerrero

Rev. Fac. Agron. (LUZ). 2023, 40(2): e234016

ISSN 2477-9407

DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v40.n2.06

Crop Production

Associate editor: Dra. Lilia Urdaneta

University of Zulia, Faculty of Agronomy

Bolivarian Republic of Venezuela

Agronomy Degree, Department of Plant Health, Faculty

of Agricultural Sciences, Technical University of Machala.

Machala, Ecuador.

Institute of Scientic Research, Faculties of Agronomic

Engineering and Health Sciences, Research Group on Crop

Management, Nutrition and Ecophysiology, Technical

University of Manabí, Ecuador.

Departments of Botany and Statistics, Faculty of Agronomy,

University of Zulia. Maracaibo, Venezuela.

Received: 20-12-2022

Accepted: 13-04-2023

Published: 23-05-2023

Abstract

The main phytosanitary problem of commercial bananas is black Sigatoka

(BS; Mycosphaerella jiensis), which causes damage to leaf area, loss of

exportable quality, and low yields. The management of BS with mixtures of

four systemic fungicides in dierent combinations in the border and central

area of three banana plantations, and its eect on the severity of this disease

were evaluated. The study was carried out in Ecuador, province of El Oro,

Pasaje canton, at the ‘‘El Playón’’, ‘‘Mega Impulso’’ and ‘‘Lolita’’ farms; in

an area of 5 hectares of the Williams cultivar with 10 years of production,

50 plants were selected in the vegetative phase in the borders and center

of the plantation, four treatments were evaluated: T1 (Triazole+Amine),

T2 (Pyrimethanil+Spiroxamine), T3 (Difenoconazole+Amine) and T4

(Amine+Pyrimethanil) and three replicates, with four applications every

14 days. Severity was assessed for 10 weeks using the Stover scale. The

experimental design was a randomized block design and the data were

analyzed by two-way ANOVA. The greatest fungicidal eect was achieved

in ‘‘El Playón’’, the severity for leaf 4 in the border area was 37.5 % and

38 % in the center. On leaf 5, ‘‘El Playón’’ 55 %, ‘‘Mega Impulso’’ 60 %,

and ‘‘Lolita’’ 72.5 % reached a severe value. The highest average number of

functional leaves was obtained in ‘‘Mega Impulso’’ and the highest average

number of old leaves free of streaks in ‘‘Lolita’’. The fungicides applied

controlled BS, due to the low percentages of disease severity.

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Rev. Fac. Agron. (LUZ). 2023, 40(2): e234016. Abril-Junio. ISSN 2477-9407.

2-6 |

Resumen

El principal problema tosanitario de los bananos comerciales

es Sigatoka negra (SN; Mycosphaerella jiensis), causa daño al

área foliar, pérdida de calidad exportable y bajos rendimientos. Se

evaluó el manejo de SN con mezclas de cuatro fungicidas sistémicos

en diferentes combinaciones en la zona de linderos y centro de tres

bananeras y su efecto sobre la severidad de esa enfermedad. Se realizó

en Ecuador, provincia de El Oro, cantón Pasaje, en las haciendas "El

Playón", "Mega Impulso" y "Lolita"; en una supercie de 5 hectáreas

del cultivar Williams con 10 años de producción, se seleccionaron

50 plantas en la fase vegetativa en los linderos y centro de la

plantación, se evaluaron cuatro tratamientos: T1 (Triazol+Amina),

T2 (Piremetanil+Espiroxamina), T3 (Difeconazol+Amina) y T4

(Amina+Piremetanil) y tres repeticiones, con cuatro aplicaciones

cada 14 días. La severidad se evaluó durante 10 semanas utilizando

la escala de Stover. El diseño experimental fue de bloques al azar y

los datos fueron analizados mediante ANOVA de dos vías. El mayor

efecto de fungicidas se logró en "El Playón", la severidad para la hoja

4, en zona de linderos fue 37,5 % y el centro 38 %. En la hoja 5, "El

Playón" 55 %, "Mega Impulso" 60 % y "Lolita" 72,5 % alcanzaron

un valor severo. El mayor número promedio de hojas funcionales

se obtuvo en "Mega Impulso" y el mayor promedio de hojas viejas

libres de estría en "Lolita". Los fungicidas aplicados controlaron a

SN, debido a los bajos porcentajes de severidad de la enfermedad.

Palabras clave: severidad, control químico, musáceas, estrías y

manchas foliares.

Resumo

O principal problema tossanitário das bananas comerciais é a

Sigatoka preta (SP; Mycosphaerella jiensis), que causa danos na

área foliar, perda de qualidade exportável e baixos rendimentos.

A gestão do SP com misturas de quatro fungicidas sistémicos em

diferentes combinações foi avaliada na zona fronteiriça e central de

três plantações de banana e o seu efeito na gravidade desta doença.

Foi realizada no Equador, província de El Oro, cantão de Pasaje,

nas fazendas "El Playón", "Mega Impulso" e "Lolita"; numa área

de 5 hectares da cultivar Williams com 10 anos de produção, foram

seleccionadas 50 plantas na fase vegetativa nas fronteiras e no centro da

plantação, foram avaliados quatro tratamentos: T1 (Triazol+Amina),

T2 (Pireometanil+Espiroxamina), T3 (Difeconazol+Amina) e T4

(Amina+Pireometanil) e três réplicas, com quatro aplicações de 14

em 14 dias. A severidade foi avaliada durante 10 semanas utilizando

a escala de Stover. O desenho experimental foi um desenho de bloco

aleatório e os dados foram analisados por ANOVA bidireccional. O

maior efeito fungicida foi alcançado em "El Playón", a severidade

para a folha 4, na zona fronteiriça foi de 37,5 % e o centro de 38

%. Na folha 5, "El Playón" 55 %, "Mega Impulso" 60 % e "Lolita"

72,5 % atingiram um valor severo. O maior número médio de folhas

funcionais foi obtido em "Mega Impulso" e o maior número médio de

folhas velhas livres de estrias em "Lolita". Os fungicidas aplicados

controlaram SP, devido às baixas percentagens de gravidade da

doença.

Palavras-chave: severidade, controlo químico, musaceae, estrias e

manchas de folhas.

Introduction

Bananas are a crop of economic and food importance to the

world. In Ecuador, in the commercial and social sphere, it represents

2 % of the gross domestic product (GDP). The banana industry

generates approximately 1 million families and benets 2.5 million

people, representing 6 % of the country’s total population (García et

al., 2019).

According to Yánez et al. (2020), 60 % of the area planted with

bananas in Ecuador corresponds to the Williams cultivar and describe

it as a medium-sized plant (between 3.5 and 4.0 m), of high production

and susceptible to Black Sigatoka (Mycosphaerella jiensis Morelet).

Cedeño et al. (2017) reported that black Sigatoka is the most

destructive disease in banana crops because the fungus destroys the

leaf area due to the excretion of the phytotoxin “Juglone”, which

interrupts the transport of electrons in the membranes of chloroplasts,

causing necrosis and death of leaf tissue in the plant.

To prevent black Sigatoka from causing the loss of leaves of

banana plants, it is necessary to monitor weekly the phytosanitary

status of the crop and the application of fungicides to obtain an

acceptable commercial production; however, this raises costs and

producers see their incomes aected (Ramírez et al., 2014).

In Ecuador, the most commonly used systemic fungicides are:

amines (fenpropimorph), triazoles (epoxiconazoles), strobilurins,

anilinopyrimidines, carboxamides, and guanidines, and the

application cycles depend on the degree of infection, the frequency is

7 to 14 days in the rainy season and 28 days in the dry season.

This chemical control of the disease increasingly requires the

application of more fungicides in mixtures and at low frequencies

due to the resistance that the fungus has developed, which increases

production costs by more than 30 % (Sepúlveda, 2015). In this sense,

Cervantes-Alava et al. (2020) and Sánchez et al. (2021) highlighted

that applications should be made taking into consideration the rotation

indicated by the FRAC (Fungicide Resistance Action Committee) for

the dierent chemical groups.

Regarding the systemic mode of action of the fungicides applied,

Pérez (2006) pointed out that it allows them to enter at the level of the

waxy layers and the cuticle in the leaf, highlighting that the chemical

groups presented dierent solubility values: spiroketalamines

and pyrimethanil (2.8); epoxiconazole (3.4); tridemorph (4.2);

difenoconazole (4.3) and fenpropimorph (4.7).

Likewise, Murillo (2015) pointed out that the absorption and

translocation of systemic fungicides depend on their lipophilicity,

a characteristic that allows penetration at the level of the waxy

layers and the cuticle of the leaf, and solubility in water, factors that

substantially aect their systemic action.

The aerial spraying reaches to fumigate the entire area planted

with bananas and especially in the borders, an area that receives twice

as many products; however, in general, at this site, there is always

high infection all year round.

Therefore, the objective of the research was to evaluate the

management of black Sigatoka through the application in mixture

of four systemic fungicides in dierent combinations in the border

and central areas of the banana plantations ‘‘El Playón’’, ‘‘Mega

Impulso’’, and ‘‘Lolita’’ and its eect on the severity of this disease.

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Cervantes-Álava et al. Rev. Fac. Agron. (LUZ). 2023 40(2): e234016

3-6 |

Materials and methods

The study was conducted in the southern region of Ecuador,

in the province of "El Oro" Pasaje canton in banana plantations

"El Playón", "Mega Impulso" and "Lolita". The study area has a

humid tropical climate, with an average temperature of 24 °C, annual

rainfall of 550 mm, and relative humidity of 80 %, with clay

loam soils (Yánez et al., 2020).

The banana plantations had been established for 10 years with

the Williams cultivar and with a subfoliar irrigation system. For the

collection of data in the eld, from the zones (center and border) 50

plants of more than 3 meters in height were selected in the vegetative

phase, distributed in an area of 5 hectares, in each of the farms. Two

evaluation sites were considered, a first zone subjected to normal

frequency cycles called "center" that received a chemical load of

fungicides respecting the FRAC guidelines, and a second zone of

“borders” that received a greater chemical load due to the drift of the

adjacent applications.

Of the 50 plants selected, the variables severity, old leaf free of

streaks (OLFS), and number of total leaves (TL) were evaluated in

plants, 7 days after the application of fungicide mixtures for 10

weeks.

For the quantication of the severity, 40 cm from the apex

towards the center of leaves 3, 4, and 5 were cut using a billhook.

The percentage of severity was evaluated according to the Stover

scale modied by Gauhl, which measures physiological parameters

visible in the young leaves of plants ready for owering, in which

the evolutionary stages of the fungus and levels of infection were

determined according to the degrees established by Gauhl (Quevedo

et al., 2018). The values for the variable OLFS were considered

according to the last leaf with streaks whose percentages were less

than 5 % in plants with the presence of inorescences (newly emerged

acorn), in both zones within the test area, and the TL was calculated

by counting the rst leaf from the top to the base of the plant.

The applications of the mixtures of the systemic fungicides

evaluated were made by aerial spraying (table 1), the products were

prepared in emulsion at a volume of 3 gallons of water and 2 gallons of

oil (Banole®) per hectare, the dose of the fungicides was as indicated

Table 1. Rotations of fungicides used in the management of black Sigatoka in the three banana plantations of the Pasaje canton, Ecuador.

Farms Fungicides (systemic)

Principal Chemical group Dose (L.ha

-1

) Mixer Dose (L.ha

-1

) Chemical group

"El Playon"

T1. Epoxiconazole Triazole 1.25 Tridemorph 0.5 Amine

T2. Spiroxamine Spiroketalamines 0.4 Pyrimethanil 0.5 Anilinopyrimidines

T3. Difenoconazole Triazole 0.4 Tridemorph 0.5 Amine

T4. Fenpropimorph Amine 1.0 Pyrimethanil 0.5 Anilinopyrimidines

"Mega Impulso"

T3. Difenoconazole Triazole 0.4 Tridemorph 0.5 Amine

T4. Fenpropimorph Amine 1.0 Pyrimethanil 0.5 Anilinopyrimidines

T1. Epoxiconazole Triazole 1.25 Tridemorph 0.5 Amine

T2. Spiroxamine Spiroketalamines 0.4 Pyrimethanil 0.5 Anilinopyrimidines

"Lolita"

T2. Spiroxamine Spiroketalamines 0.4 Pyrimethanil 0.5 Anilinopyrimidines

T1. Epoxiconazole Triazole 1.25 Tridemorph 0.5 Amine

T4. Fenpropimorph Amine 1.0 Pyrimethanil 0.5 Anilinopyrimidines

T3. Difenoconazole Triazole 0.4 Tridemorph 0.5 Amine

on the label by the manufacturer and the frequency of rotation was 14

calendar days.

Using the SPSS statistical program, the data obtained were

subjected to two-way analysis of variance according to the randomized

block design with three replications. The separation of means was

carried out by Tukey’s test.

Results and discussion

Severity of Black Sigatoka

In the estimation of the eect of the severity of black Sigatoka,

considering the border and central areas within the farms, in leaves

4 there were no statistical dierences, only in the ‘‘Mega Impulso’’

farm there were statistical dierences in leaf 5 between the two areas

of application (table 2).

Table 2. Eect of the fungicides evaluated on the severity of black

Sigatoka on leaves 4 and 5, in plants of the central and

border areas in three banana plantations of the Pasaje

canton, Ecuador.

Farms

Severity (%)

Leaf 4 Leaf 5

"El Playon" L 37.5aA 55.0aA

"El Playon" C 38.0a 55.5a

"Mega Impulso" L 42.5bB 60.0bB

"Mega Impulso" C 43.0b 62.7c

"Lolita" L 45.0cC 72.5dC

"Lolita" C 45.0c 73.0d

Note: The values with the same lowercase letter indicate that the means did

not present signicant dierences within the farms, and the values with

dierent capital letters indicate that there were dierences between the farms.

Abbreviations: L=Border; C=Center.

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Rev. Fac. Agron. (LUZ). 2023, 40(2): e234016. Abril-Junio. ISSN 2477-9407.

4-6 |

Signicant dierences were found among the farms, the

ANOVA allowed to differentiate the

three subsets that were formed

in "El Playón", "Mega Impulso" and "Lolita", in the border (L)

and the center (C), which indicated that the fungicides and the

application area had a dierent behavior (table 2). All systemic

fungicides applied at a frequency of 14 calendar days exerted a

satisfactory control (37.5 to 45 % severity) of the disease on leaf 4

in general, showing that the dierent treatments of fungicides acted

independently in the dierent farms.

When the subsets between the border and central areas were

analyzed (table 2), in the Mega Impulso farm, signicant dierences,

in leaf 5, between the two zones (p = 0.001) were found. In relation

to leaf 4 in the production units, "El Playón", in the border and

central areas, the lowest percentages of severity were 37.5 and

38 %, respectively; values considered high according to the scale

used by Cedeño-Zambrano et al. (2021), Sánchez et al. (2021) and

Sánchez-Urdaneta et al. (2021).

In the border areas of the "Mega Impulso" and "Lolita" farms,

the percentages of severity were also within the range considered

high 42.5 and 45 %, respectively; which implied a greater risk of

burning for these farms, highlighting that in the "Lolita" farm the

severity in leaf 4 was the highest with 45 % in border area and 45.5

% in central area.

The lowest percentage of severity of the disease in leaf 5 was

presented by "El Playón" farm, both for the central and border areas

with 55.0 and 55.5 % (severe), respectively; the "Mega Impulso"

farm showed an average of 60.0 % for the border and 62.7 % for

the center (severe); which was statistically different. ‘‘Lolita’’ had a

severity percentage of 72.5 % and 73.0 % (severe) for the border

and central areas, respectively (table 2). The results showed that

the systemic fungicides used in the research had dierent behaviors

when evaluating the severity between farms (p = 0.001) for each

application site in the treated leaves, which coincided with what

was reported by Quevedo et al. (2018) who mentioned that when

rotating systemic and protective fungicides, the analysis of variance

of the evolutionary states (severity) showed statistical dierences

between farms.

The banana plantations of "El Playón", "Mega Impulso" and

"Lolita" were areas planted with the Williams cultivar, and the

treatments were applied according to the mixtures of systemic

fungicides most used in La Peaña parish; triazole + amine, amine

+ anilinopyrimidines, difenoconazole + amine and spiroxamine +

anilinopyrimidines (table 1). The results obtained in the control

of black Sigatoka, conrmed that the rotation of the molecules is

important for the timely control of the disease (Cedeño et al., 2017).

Old leaves free of streaks (OLFS)

The range of old leaves free of streaks ranged from 7 to 7.3

(gure 1). In "El Playón" farm the results of OLFS in both areas

were the same in the treatments T3 = difenoconazole + tridemorph

and T4 = fenpropimorph + pyrimethanil (gure 1 ), t he highest

values were obtained at the "Lolita" farm for T1 = epoxiconazole +

tridemorph and T4 = fenpropimorph + pyrimethanil. What has been

observed for OLFS in T4 can be justied since fenpropimorph is a

systemic fungicide of triple action that has preventive and curative

activity, and acts as a protectant, in addition its absorption medium

is foliar and its mechanism of action lies in the inhibition of the

germination of the spores of the fungus (Agroactivo, 2023).

7,2

7,25

6,90

7,00

7,10

7,20

7,30

Center Border

Old leaves free of streaks by treatment

Application areas

7,2

7,3

6,95

7,00

7,05

7,10

7,15

7,20

7,25

7,30

7,35

El Playón Mega Impulso Lolita

Number of old leaves free of streaks

Farms

Figure 1. Old leaves free of streaks (average) by treatment of

fungicides applied at "El Playón", "Mega Impulso"

and "Lolita" farms. Abbreviations: T1= fungicide

epoxiconazole + tridemorph, T2= spiroxamine +

pyrimethanil, T3= difenoconazole + tridemorph and T4=

fenpropimorph + pyrimethanil.

Figure 2 shows that the old leaves free of streaks in the central

area, T1 = epoxiconaxole + tridemorph presented a higher value,

and T2 = spiroxamine + pyrimethanil (6.95) presented lower values.

This result was due to the fact that, at the time of the aerial spraying,

the ight height was more ecient in the center of the plantation,

because there was greater ease for the plane to pass closer to

the foliage and its coverage was greater. For the border area, T2

spiroxamine + pyrimethanil was equal to T4 = fenpropimorph +

pyrimethanil, with the lowest means for this variable being attributed

to the diculty of the plane to y and avoid losses due to drifts

(Arriaga-García et al., 2022).

by ar

eas of application and by treatment of

fungicides evaluated at "El Playón", "Mega

Impulso", and "Lolita" farms. Abbreviations:

T1= fungicide epoxiconazole + tridemorph, T2=

spiroxamine + pyrimethanil, T3= difenoconazole +

tridemorph, and T4= fenpropimorph + pyrimethanil.

Figure 2. Old leaves free of streaks (average) by areas of (average)

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Cervantes-Álava et al. Rev. Fac. Agron. (LUZ). 2023 40(2): e234016

5-6 |

Functional leaves

Figure 3 shows that at "El Playón" farm for treatments (T3 and T4)

12.3 functional leaves were quantified, while for T3 and T4 at the

"Mega Impulso" farm there were 12.0 and 12.7 total functional leaves

on average, respectively, showing a difference of 0.7 leaves for

this particular mixture. At the "Lolita" farm, 12.3 and 12 total

functional leaves were reported for T3 and T4, respectively.

Likewise, T1 (epoxiconazole + tridemorph) and T2 (spiroxamine

+ pyrimethanil) had similar behavior, only to a greater extent in T1.

Figure 3. Functional leaves (average) by treatment of fungicides

applied at "El Playón", "Mega Impulso", and "Lolita"

farms. Abbreviations: T1= epoxiconazole fungicide

+ tridemorph, T2 = spiroxamine + pyrimethanil, T3 =

difenoconazole + tridemorph and T4 = fenpropimorph +

pyrimethanil.

Hernández et al. (2016) pointed out that M. jiensis, caused

necrosis in the leaves and that this disease is endemic in the Musaceae

and with recurrence both in dry and rainy season, they also mentioned

that all phytosanitary programs should be reinforced with good

defoliation management, eliminating the necrotic parts and with this,

the frequencies of application decreased.

T1 = spiroxamine + pyrimethanil and T3 = difenoconazole +

tridemorph, were the best treatments and presented equal values

12.45 of functional leaves for both the central and border areas (gure

4). The application of spiroxamine + pyrimethanil (T2) the average

of the total leaves was 12.05 both in the area of application of the

center and the border; with the use of fenpropimorph + pyrimethanil

(T4) the average was 12.35 HF, which was 0.35 times higher than T4,

with respect to T2, which shows that the mixtures fenpropimorph +

pyrimethanil, acted in a preventive and curative way against black

Sigatoka, guaranteeing 35 % more leaf area.

For the management of M. jiensis, the most used fungicides

have been of systemic action such as triazoles, strobirulins and

anilinopyrimidines, which coincided with what was indicated by

Martínez-Bolaños et al. (2012). Also highlighting what was reported

by Mena-Espino and Couoh-Uicab (2015) who mentioned that 10 to

45 applications of fungicides per year were required for the chemical

management of black Sigatoka, which agreed with the results of this

study. It should be noted that authors such as Archicanoy (2001),

and Barrera et al. (2016) indicated that applications in mixture of

fungicides at the time of higher pressure of the disease should be

preventive at short frequency, which allows ecient management

of the disease. Where in addition, they suggested managing the crop

using dierent levels of shade in order to reduce the eects of the

disease, this could also be seen in the results obtained in this research

in relation to the period of application of fungicides.

Conclusions

It is necessary to use systemic fungicides for good management

of black Sigatoka in banana cultivation, especially at the beginning

of the rains, demonstrated through the fact that the fungicides used

exerted a satisfactory control of black Sigatoka, in reference to the

low percentages of severity of the disease presented in banana plants

and the amount in general of functional leaves at the time of emission

of the inorescence (inorescence-raceme) both for the central and

border areas, particularly at "El Playón" and "Mega Impulso" farms.

The fungicides were applied in mixtures at a short frequency of 14

days of rotation, completing a total program of 28 cycles per year. In

general, the phytosanitary control for the parameters total leaves, and

old leaves free of streaks was within the normal ranges of a plantation

with conventional management (chemical controls).

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servlet/articulo?codigo= 7266829

12,3

12,7

11,80

12,00

12,20

12,40

12,60

12,80

El Playón Mega Impulso Lolita

Functional leaves by treatment

Farms

12,45 12,45

11,90

12,10

12,30

12,50

Center Boundary

otal functional Leaves per treatment

and application zone

AREAS OF APPLICATION

Figure 4. Functional leaves (average) by application areas

and by fungicide treatment evaluated at "El

Playón", "Mega Impulso", and "Lolita" farms.

Abbreviations: T1= fungicide epoxiconazole +

tridemorph, T2= spiroxamine + pyrimethanil, T3=

difenoconazole + tridemorph and T4= fenpropimorph +

pyrimethanil.

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Rev. Fac. Agron. (LUZ). 2023, 40(2): e234016. Abril-Junio. ISSN 2477-9407.

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