Revista Mexicana Ciencias Agrícolas   volume 12   number 2   February 15 - March 31, 2021

DOI: https://doi.org/10.29312/remexca.v12i2.2551

Investigation note

Effectiveness of fungicides and Trichorderma spp. for the control of Lasiodiplodia spp. in ‘Persian’ lemon orchards in Veracruz

Santos Gerardo Leyva-Mir1

Marco Antonio Bautista-Cruz2

Gustavo Almaguer-Vargas2

María Teresa Colinas-León2

Juan Manuel Tovar-Pedraza3

Moisés Camacho-Tapia4§

1Department of Agricultural Parasitology-Chapingo Autonomous University. Highway México-Texcoco km 38.5, Texcoco, State of Mexico, Mexico. ZC. 56230. Tel. 5959521500, ext. 6179. (lsantos@correo.chapingo.mx). 2Postgraduate in Horticulture-Phytotechnics Department-Chapingo Autonomous University. Highway Mexico-Texcoco km 38.5. Texcoco, State of Mexico, Mexico. ZC. 56230. Tel. 595 9521500, ext. 6390. (bacma-74@hotmail.com; almaguervargas@hotmail.com; lozcol@gmail.com). 3Laboratory of Phytopathology, Culiacán Coordination, Center for Research in Food and Development. Highway El Dorado Campo El 10 km 5.5, Sinaloa, Mexico. ZC. 80110. Tel. 667 4806950 (juan.tovar@ciad.mx). 4National Laboratory for Agri-Food and Forestry Research and Service-Chapingo Autonomous University. Highway México-Texcoco km 38.5, Texcoco, State of Mexico, Mexico. ZC. 56230. Tel. 595 9521500, ext. 6450.

§Corresponding author: moises.camachotapia@gmail.com.

Abstract

The descending death of ‘Persian’ lemon (Citrus latifolia Tan.) caused by Lasiodiplodia spp., is a high-importance disease. The intensity of lemon pruning increases the susceptibility and annual loss of up to 35% of trees, resulting in 60% reduction in production. During 2016 and 2017, in the municipality of Papantla, Veracruz it was assessed the effectiveness of chemical and biological control against Lasiodiplodia spp., after pruning. A complete block design was performed at random; five treatments were applied: methyl thiophanate (1 g L-1), thiabendazole (2.5 g L-1), chlorothalonil (3 g L-1), mancozeb (4 g L-1), Trichoderma harzianum + Trichoderma viridae (20 ml L-1) and a witness (without application). Two sprays were made aimed at trunk, branches and foliage up to drip point. The incidence and severity of the disease was evaluated every seven days after the first application. With the data, epidemiological models were adjusted and descriptive parameters such as: initial intensity, rate of increase and area under the disease progress curve were calculated. Methyl thiophanate fungicide was most effective in disease control, followed by thiabendazole.

Keywords: Lasiodiplodia spp., descending death, disease control.

Reception date: January 2021

Acceptance date: February 2021

The lemon ‘Persian’ (Citrus latifolia Tan.) belongs to the family Rutaceae in Mexico the area with the highest production of this fruit is located in the Gulf (Mendoza-Tornez et al., 2016). Factors that reduce ‘Persian’ lemon production include various diseases, including sadness virus, exocortis, citrus greening disease, anthracnosis, descending death, gummosis among others. Gummosis damage in citrus fruits is caused by Phythopthora spp. For which the application of fungicides such as fosetyl-Al and metalaxyl is recommended (Jadeja et al., 2000; Raina, 2012; Acosta-Pérez et al., 2014).

However, in some cases, these applications do not have satisfactory results when controlling gummosis, because Lasiodiplodia spp., also induce gummosis in affected areas and are generally confused with Phytophthora spp. This situation occurs in the production areas of Veracruz, where production in ‘Persian’ lemon trees is reduced. In 2019 L. pseudotheobromae, L. theobromae, L. brasiliense, L. subglobosa, L. citricola and L. iraniensis were reported as the causal agents of descending death and canker in commercial ‘Persian’ lemon orchards in Puebla and Veracruz (Bautista-Cruz et al., 2019).

In 2019 in Morelos, it was reported to L. citricola, L. theobromae and L. pseudotheobromae affecting ‘Persian’ lemon (Valley- de la Paz et al., 2019a). Also, Polanco-Florian et al. (2019) reported to L. theobromae, Fomitopsis meliae and Eutrypella citricola as causing the descending death in sweet orange from Nuevo Leon and Tamaulipas.

Fungi of the genus Lasiodiplodia are nonspecific phytopathogens, can survive as endophytes and as saprophytes under abiotic stress conditions. They develop in subtropical and tropical regions where they affect more than 1 100 trees, causing diseases such as descending death, gummosis and peduncle rot (McDonald et al., 2011; Al-Sadi et al., 2013; Coutinho et al., 2017). Also, Lasiodiplodia spp., has been reported inducing symptoms of descending death, gummosis and canker in a wide range of citrus species (Al-Sadi et al., 2013; Coutinho et al., 2017).

Lasiodiplodia spp., causes descending death and gummosis, characterized by necrosis of tree bark and wood, as well as canker on stems in ‘Persian’ lemon orchards reported in the state of Veracruz, in the region of Martínez de la Torre, Tlapacoyan and Papantla and in the state of Puebla in Acateno and Hueytamalco (Bautista-Cruz et al., 2019). These phytopathogens fungi decrease citrus productivity 60% and annual loss of trees can reach up to 35%. Some studies reported the effectiveness of fungicides such as methyl thiophanate for the control of the descending death of mango orchards caused by Lasiodiplodia spp. (Khanzada et al., 2005; Shahbaz et al., 2009; Naqvi et al., 2015).

Other studies reported the effectiveness of Trichoderma for the control of fungal diseases in citrus fruits (García et al., 2011; El- Mohamedy et al., 2012). In the case of mango, it has been reported that the main access point of Lasiodiplodia spp., is through pruning wounds, damage caused by insects, branches broken by wind or oversupply of fruit (Sakadilis et al., 2011). In the crop of 'Persian' lemon intense pruning is carried out as part of the management of the crop, and this favors the incidence of gummosis, so it is necessary to protect the trees immediately after pruning. For this reason, the objective of this research was to evaluate the effectiveness of chemicals and biological products, after pruning, for the management of descending death in commercial ‘Persian’ lemon orchards.

It was selected a ‘Persian’ lemon orchard grafted in Citrus volkameriana, in the ejido of Insurgente Socialista, in the municipality of Papantla, state of Veracruz, Mexico and where previously six species of Lasiodiplodia were identified (Bautista-Cruz et al., 2019), lemon trees were eight years old and had planting distance of 5 x 5 m. In the selected orchard, during 2016 and 2017, the effectiveness of the products methyl thiophanate, thiabendazole, chlorothalonil, mancozeb was evaluated (Table 1), a product based on Trichoderma harzianum + Trichoderma viridae at a concentration of 8 x 108 conidia ml-1 and finally a control, where only water was applied, which gave a total of six treatments established in the field under a random full blocks design.

Table 1. Chemicals for the control of Lasiodiplodia spp. in ‘Persian’ lemon.

Each treatment had six trees and from each tree two branches were pruned with an average diameter of 3.5 cm, leaving a final length of 20 cm and that were located at each cardinal point, giving a total of 48 sampling units.

After pruning the branches, treatments with an SR 420 motorized sprinkler (Sthil, Mexico) were applied to each lemon tree up to drip point to ensure product coverage. A second application was made 20 days after the first application. Seven weekly evaluations were conducted, which began after seven days of the first application of the treatments.

The variable response was the length of lesions of Lasiodiplodia on pruned branches. The measures obtained were used to characterize the severity of the disease. The evaluation data made adjustments to epidemiological models that described the development of the disease over time. With the help of the SAS version 9.2 statistical package (SAS, 2008), epidemiological models (Exponential, Monomolecular, Logistics and Gompertz) were analyzed.

The selection of the disease descriptor model was with the coefficient of determination (R2). In addition, epidemic parameters such as initial severity of disease (Y0), disease increase rate (% day) and area under the disease progression curve (ABCPE) (%-day) were determined using the trapezoidal integration method (Campbell and Madden, 1990).

To determine the effect of the treatments and compare each of the epidemiological parameters, a variance analysis was performed (α= 0.05). In addition, a comparison of means was performed using the significant minimum difference test (Fisher, α= 0.05). The SAS version 9.2 statistical package was used for all analyses. The treatments used slowed the progression of symptoms of descending death, while the witness trees presented an obvious development of the disease. The model that best described the epidemic was logistics (y=1/ (1+ ((1-y0)/y0)*ex (-rL*t)) (Table 2).

Table 2. Effect of treatments on the descriptive parameters of the development of Lasiodiplodia spp. in ‘Persian’ lemon.

Y0= initial intensity of the disease; rL= rate of increase of the disease (% day); ABCPE= area under the disease progress curve (%-day).

It was observed that in all treatments the initial intensity of the disease (Y0) had some variations, indicating a lower initial intensity in the witness. This situation could have been due to the natural conditions under which the experiment was established, due in the field the variation of the inoculum could be due to the spatial distribution of the trees evaluated, in addition in this study there was no direct inoculation of  Lasiodiplodia spp., but was waited for the infection to occur due to natural conditions considering the principle of contagion through inoculum in the soil and surrounding branches that had symptoms and spores that increased the initial intensity of the disease. However, with treatment applications the initial intensity of inoculum may be reduced to generate less development of the epidemic.

By performing a second application at 20 days, the reduction of the inoculum generated after the start of the experiment can be guaranteed, and this has a direct effect on the rate of increase (rL). Considering this, it can be indicated that the best product to control Lasiodioplodia spp., it is methyl thiophanate, as it reduced rL (0.04536%-day) and was observed a lower ABCPE (514.90461%-day) compared to other treatments which, as an integrative parameter in the description of disease behavior, provided a better understanding of the importance of reducing the rate of increase and its effect on the development of a disease.

Thiabendazole had control after methyl thiophanate, so they could be considered as an alternative to disease control. In the same sense, thiabendazole could be considered for a second application, as it has an effect on reducing the rate of increase, in this study presented an rL of 0.049764, which is similar to that presented by methyl thiophanate. The witness exhibited an increase rate of 0.223954%, which resulted in an ABCPE of 336936.28%-day, which described an obvious development of the epidemic.

The contact fungicides chlorothalonil and mancozeb had a higher rate of increase, 0.164006 and 0.114338%-day respectively, which resulted in a higher ABCPE,  therefore, these fungicides should not be considered for the curative management of Lasiodiplodia  spp., Valle-de la Paz  et al. (2019b) report that isolated L. theobromae and L. citricola in 'Persian' lemon from Morelos, Mexico  and under in vitro conditions, are sensitive to methyl thiophanate and thiabendazole, which is consistent with this research in field,  while in vitro conditions they report good control with the use of Trichoderma but in field conditions there was no good control.

Similarly, Masood et al. (2014), reported high effectiveness for the control of descending death in mango crops in Pakistan, with the use of methyl thiophanate, by injection into xylem and foliar applications. On the other hand, Khanzada et al. (2005) found that carbendazim had a greater effect than methyl thiophanate, when evaluated in the same system. In the case of mango, injecting methyl thiophanate directly into xylem three months after starting treatment reduces defoliation in trees. However, injuries with the presence of gummosis cannot be eliminated.

Khanzada et al. (2005) when applying carbendazim, methyl thiophanate and fosetyl aluminum for the control of descending death of mango in Pakistan, they found acceptable effectiveness of methyl thiophanate in the control of this disease (only surpassed by carbendazim) and in addition to that, with this study, they managed to reduce fungal infection, suppressed the exudation of rubber, death and wilting of mango branches, in addition there was a significant increase in vegetative growth of the plants. In late orange was reported high effectiveness of thiabendazole for the control of Guinardia citricarpa (Yan et al., 2016).

On the other hand, in this sense, Tovar-Pedraza et al. (2013) managed to reduce 62% the incidence of descending death in the grafting phase in mamey sapote nurseries by treating immersion sticks with thiabendazole and mancozeb, they reported that thiabendazole showed greater effectiveness in disease control.

Likewise, Tovar-Pedraza et al. (2013) mention that the combination of fungicides and washing prevented L. theobromae infection during the mamey sapote grafting process. Shahbaz et al. (2009); Navqui et al. (2015) reported that under in vitro conditions methyl thiophanate has high effectiveness in the control of Lasiodiplodia. Wang et al. (2007) indicated that prochloraz, iprodione and tebuconazole were the most effective fungicides to inhibit the mycelial growth of L. theobromae in papaya, similarly Bester (2007) reported the use of prochloraz and tebuconazole for the control of Lasiodiplodia in grapes.

In this work Trichoderma did not have a good control, this may be because it was applied foliar form, compared to other researchers where they apply it in soil to control pathogens that affect root, in addition optimal conditions for the development of this control agent were not guaranteed (Harman et al., 2004; Infante et al., 2009; Martinez et al., 2013).  

Some studies in ‘Persian’ lemon and tangerine indicated that Trichoderma spp., may have a similar effect as methyl thiophanate to control root rot caused by Fusarium (El-Mohamedy et al., 2012; El-Mohamedy et al., 2013). In in vitro studies, Bhadra et al. (2015) reported high effectiveness of Trichoderma viridae in controlling Lasiodiplodia theobromae.

Considering the results obtained in this experiment, the use of Trichoderma for the control of Lasiodiplodia would not be recommended, because the infection is given in the branches and when the biological control agent is applied here, does not have all the necessary conditions to develop and be present for Lasiodiplodia control.

This research found that chlorothalonil had a better effect up to 28 days, because reduced the development of the disease more efficiently. After 28 days, this product loses its effectiveness, while methyl thiophanate has control throughout the evaluation time. Mancozeb was the least effective fungicide in this experiment. In trees treated with methyl thiophanate, increased scarring of these lesions was observed followed by thiabendazole, Trichoderma spp., chlorothalonil and mancozeb, compared to untreated trees. However, after 45 days of the first application (ddpa), some of the lesions that were already healing, began to have little rubber runoff. In untreated trees, the disease increased over time, until some of the stumps collapsed.

In the study region it is observed that some practices such as conserving lemon on the tree until it increases its value cause the increase in incidence of Lasiodiplodia and peduncle rot. In addition, the mummified fruits and pruning remains left on the ground are source of inoculum, impacting the initial intensity of the epidemic, in addition to the rate of increase in tree reinfection cycles, to avoid this, it is advisable to carry out the necessary fungicide applications, in addition to removing pruning residues and avoid leaving the fruit in the trees for an unnecessary time, since it also has an impact on the increase in the susceptibility of the trees to Lasiodiplodia infection.

It is usually associated with Phythopthora spp., as the causal agent of citrus gummosis, and for its control metalaxyl and fosetyl-Al treatments are carried out (Farih et al.,1981; Jadeja et al., 2000 and Raina et al., 2012). In the study area of Martínez de la Torre, Tlapacoyan, Papantla, fosetyl-Al and metalaxyl are regularly applied for the control of gummosis, but there are no favorable results, since the incidence of gummosis in the orchards exceeded 92.5% and economic losses increase considerably. In this research, methyl thiophanate was the best product to control Lasiodiplodia, followed by thiabendazole.

Conclusions

The fungicide that had the best effectiveness in controlling the descending death of ‘Persian’ lemon in field conditions, was methyl thiophanate, followed by thiabendazole. Performing two fungicide applications significantly reduces descending death; however, it is suggested that in an integrated management of the ‘Persian’ lemon, to consider the climatic conditions in which pruning is carried out and the application to decrease the source of inoculum and the rate of increase, since in rainy season would increase incidence and severity of Lasiodiplodia spp.

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