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Revista mexicana de ciencias agrícolas

versão impressa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.8 no.5 Texcoco Jun./Ago. 2017

https://doi.org/10.29312/remexca.v8i5.111 

Articles

Effect of HLB on Mexican key lime yield in Colima, Mexico

Marciano Manuel Robles-González§ 

Mario Orozco-Santos1 

Miguel Ángel Manzanilla-Ramírez1 

José Joaquín Velázquez-Monreal1 

Silvia Heréndira Carrillo-Medrano1 

1Campo Experimental Tecomán-INIFAP. Carretera Colima-Manzanillo km. 35. Tecomán, Colima, México. CP. 28930. Tel. 01 (800) 0882222, ext. 84332. (orozco.mario@inifap.gob.mx; manzanilla.miguel@inifap.gob.mx; velazquez.joaquin@inifap.gob.mx; carrillo.silvia@inifap.gob.mx.


Abstract

Huanglongbing disease (HLB) associated with the bacterium Candidatus Liberibacter asiaticus’ is the most serious threat faced by the Mexican key lime crop [Citrus aurantifolia (Christm) Swingle] in Colima, México. It was detected in April 2010 and soon it spread to all producing areas, causing heavy production losses. In order to characterize yield losses, due to HLB, 700 trees with different percentages of treetop affected were sampled. Using a metal ring of 0.75 m2, divided into quadrants, the number of fruits per square meter of treetop (fr m-2) was quantified. In HLB trees a tend to reduce the fr m-2 was observed as the percentage of affected treetop increases, both in symptomatic (y= 4.6953x + 53.731; R2 0.8072) and asymptomatic sectors (y= 7.1643x + 67.781; R2 0.9146). Trees without HLB symptoms, averaged 60.3 fr m-2. In contrast trees with HLB symptoms covering the entire treetop averaged 27.6 fr m-2, representing a reduction of 45.8%. This paper provides information on how HLB affects yield of Mexican key lime trees from the early stages of infection until when the entire treetop display the symptoms of the disease and helps to explain the yield fall in the production of this citrus in the region.

Keywords: Citrus aurantifolia; Candidatus Liberibacter; asiaticus; symptomatic sector; yield

Resumen

La enfermedad del Huanglongbing (HLB) asociada a la bacteria ‘Candidatus Liberibacter asiaticus’ es la amenaza más grave que ha enfrentado el cultivo de limón mexicano [Citrus aurantifolia (Christm) Swingle] en Colima, México. Se detectó en abril de 2010 y en poco tiempo se extendió por todas las zonas productoras, causando fuertes pérdidas de producción. Con la finalidad de caracterizar las pérdidas de rendimiento, debido al HLB, se muestrearon 700 árboles con distintos porcentajes de copa afectada por la enfermedad. Con ayuda de un aro metálico de 0.75 m2, dividido en cuadrantes, se cuantificó el número de frutos por metro cuadrado de copa (fr m-2). En los árboles con HLB se observó una tendencia a reducir el fr m-2 conforme aumenta el porcentaje de copa afectada, tanto en los sectores sintomáticos (y= 4.6953x + 53.731; R2 0.8072) como en los sectores asintomáticos (y= 7.1643x + 67.781; R2 0.9146). Los árboles sin síntomas de HLB promediaron 60.3 fr m-2. En contraste los árboles con síntomas de HLB cubriendo toda la copa promediaron 27.6 fr m-2, lo que representa una reducción de 45.8%. Este trabajo proporciona información de cómo el HLB afecta la productividad de los árboles de limón mexicano desde etapas tempranas de la infección hasta que toda la copa presenta los síntomas de la enfermedad, y ayuda a explicar la caída de producción de este cítrico en la región.

Palabras clave: Citrus aurantifolia; Candidatus Liberibacter; asiaticus; productividad; sector sintomático

Introduction

According to data from the Agri-Food and Fisheries Information Service (SIAP-SAGARPA, 2016), during 2015, 78 934.6 ha dedicated to the cultivation of Mexican lime were recorded, mainly distributed in the states of Michoacán, Colima, Oaxaca and Guerrero. The annual fruit production exceeded one million tons, with a value exceeding 3 829 million pesos. This agribusiness generates a large number of jobs for day laborers and field professionals, packaging, industry, transportation and marketing. In addition, a considerable number of plant nurseries producers as well as inputs suppliers benefit from this crop (Robles-González et al., 2014).

Huanglongbing disease (HLB) is the most serious threat faced by Mexican lime in Colima. The symptoms of this disease are associated with the presence of an α-proteobacteria ‘Candidatus Liberibacter asiaticus’ of Gram-negative type, restricted to phloem of host plants and spreaded by the Asian citrus psyllid (Diaphorina citri). It is now considered as the most destructive citrus disease (Wang et al., 2016) and has become the most serious threat to citrus production worldwide (McCollum et al., 2016). No cure for infected trees is known (Gottwald et al., 2007), which soon become decadent and unproductive, and in some cases die.

For some citrus species, there has been determined that the HLB strongly affects the phloem tissues (Folimonova et al., 2009; Achor et al., 2010; Fan et al., 2013), causing problems for translocation of assimilates in host plants. Moreover, studies at the genomic level have been ascertained that HLB can alter the expression of a large number of genes in various organs of infected plants (Kim et al., 2009; Liao and Burns, 2012; Mafra et al., 2013; Zheng and Zhao, 2013; Aritua et al., 2013; Zhong et al., 2015; Wang et al., 2016). Some genes are overexpressed, but others reduce its expression. Genes whose expression is altered are mainly related to the plant’s defense systems (Kim et al., 2009; Rawat et al., 2015; Wang et al., 2016), the sucrose and starch metabolism (Xu et al., 2015; Rawat et al., 2015; Wang et al., 2016), synthesis and signaling hormones (Martinelli et al., 2012), nutrients absorption and transport (Zhang et al., 2015; Rawat et al., 2015; Zhong et al., 2015).

Until early 2004, the American continent was considered free from HLB, but in March of that year the disease was detected in the state of São Paulo, Brazil. In the United States of America it was first detected in August 2005, in the state of Florida, later in Louisiana during 2008, Georgia in 2009, Texas and California in 2012. It has been reported in Cuba, Belize, Jamaica, and others Countries of the Caribbean basin, where it is causing severe damage to citrus agriculture (Wang and Trivedi, 2013).

In México the disease was detected for the first time in July 2009, in Mexican backyard lime trees in Tizimín, Yucatán (Trujillo, 2010). That same year it was also found in the states of Quintana Roo, Nayarit and Jalisco in Mexican and Persian lime trees (C. latifolia Tanaka). During 2010, new detections were made that included Campeche, Colima, Sinaloa and Michoacán. Currently HLB has been detected in 391 municipalities of 22 states of the Mexican Republic (SENASICA, 2016). It has become endemic in the producing areas of Mexican and Persian lime in the states of Colima, Michoacán, Jalisco and Nayarit, where it has caused a very important economic and social impact. Only in Colima, from 2010 to 2012, a drop in the demand for labor for field and harvest work was estimated for 2 435 full-time jobs (Avalos and González, 2013).

In Colima, the first trees with symptoms and positive diagnosis for HLB were detected in April 2010 on a four-year-old Mexican lemon plantation, very close to the Pacific coast. The spread of the disease was very rapid and in only seven months HLB-positive trees had already been detected in all Mexican lemon producing areas in the state (CESAVECOL, 2011). In a systematic sampling conducted in July 2013, it was determined that HLB was affecting 100% of trees in all producing areas. To this date, the trees had symptoms on 50% of their treetops on average and had already been highly affected in fruit yield (Robles-González et al., 2013b).

In Mexican lime the HLB symptoms are very evident and easy to detect in the field. At first, the trees show one or two small sections of its top with yellowish speckles, giving a sectorized aspect of the disease, as described by Bové (2006) for other citrus fruits. In the next four to five months, the number and size of the symptomatic sectors in these trees, increases significantly, covering the entire treetop with symptoms. The speed with which the disease covers treetops is closely related to the amount of infective psyllids generated in the plantation or in neighboring plantations (Robles-González et al., 2013a).

Magomere et al. (2009) points out that it is not easy to collect precise experimental information on yield losses caused by HLB disease. The authors note that in Kenya citrus the Candidatus Liberibacter africanus infected branches yield little or no commercial fruit and in some cases yield losses of 100% were recorded. Being a relatively new disease in México, there is no information about the impacts it has on fruit yield in Mexican lime trees. This paper aims to characterize the yield losses caused by HLB in Mexican lime trees.

This is the first paper that shows information about the effect of HLB on the yield capacity of Mexican lime trees, since the first symptoms appeared in one section of the tree, until the whole treetop is affected by the disease. These results help to explain the yield fall of this citrus in the state of Colima.

Materials and methods

The research was carried out from February to June 2012 in the Mexican lime producing area of Tecomán, Colima, México, characterized by dry and semi-dry tropical climate, with an average temperature of 26 °C and a mean precipitation of 750 mm. For this year, the number of affected orchards by HLB was very high and most trees showed symptoms of the disease, in varying proportions ranging from a few twigs, to the whole of its treetop. However, apparently healthy trees could still be found, as they did not show symptoms of the disease, which gave an opportunity to estimate the yield losses of the trees related to the percentage of treetop affected by the disease. Two methods were used.

Number of fruits per square meter of treetop

Seven orchards were chosen with good agronomic management, especially regarding irrigation and fertilization. Trees grafted on C. macrophylla, were four to six years old, according to the orchard, and were planted in density of 312 trees ha-1.

Sampling was carried out on a different date, beginning in February for the first orchard and ending in June with the last one. In each orchard, 20 trees were selected for each of the treatments, which were determined based on the percentage of treetop that showed symptoms of the disease at the time of sampling: (T1; trees without symptoms, T2; 10-25%, T3; 25-50%, T4; 50-75% and T5; 75-100% treetop area with symptoms). This procedure was designed in 2010, tested in 2011 (Robles-González et al., 2013a). A ring of 0.75 m2 was used, divided into quadrants. The ring was placed in front of the treetop, at a height of 1.5 m from the ground and in four positions, which coincided with the four cardinal points. The number of fruits at harvest maturity (light green, spheroid shape and minimum equatorial diameter of 35 mm) were recorded within each quadrant. It was also recorded whether the location of the ring corresponded to a sector with or without HLB symptoms. With these data the number of fruit m-2 treetop was estimated. Data from each orchard were used as replicate and analyzed in a randomized block design with the statistical package Statistix 9 (2008).

Yield kg tree -1 year -1 before and after infection with HLB

An experimental plot was used in which, since 2006, the yield behavior of the Mexican lime varieties ‘Lise’ and ‘Colimex’ was evaluated. Trees grafted on C. macrophylla, were planted in sandy loam clay soil, with high content of CaCO3 (40 000 ppm) in lands of the INIFAP experimental field, Tecomán Campus with a density of 312 trees ha-1. Five trees were used as experimental unit, taking the three central trees as a useful plot, with five replicates. Yield data (kg tree-1) were recorded for each crop, with which the annualized yields were calculated in t ha-1. Statistical analysis was done in a randomized block design with the statistical package Statistix 9 (2008).

Results and discussion

In Colima, from the first HLB detections in April 2010, a quick spread within and between productive zones of the State was observed (Robles-González et al., 2010). As pointed out by Bove (2006) for other citrus fruits, the disease was shown by sectors in the treetops. At first, one or two small sectors are detected in the crown of the tree whose leaves show characteristic symptoms of the disease, but in a short time the number and size of sectors with symptoms increases until 100% of the tree crown is covered. By 2012, the number of orchards affected by HLB was high and most trees showed symptoms of the disease. The affected crown percentages in the trees ranged from a small sector to the entire treetop. However, asymptomatic trees could still be found, which provided an opportunity to estimate tree yield losses related to the HLB-affected crown ratio and to compare them with the yield of asymptomatic trees under the same management conditions.

Number of fruits per square meter of treetop

Fruit production in sectors with and without symptoms. In the seven orchards used for the study, HLB was widely disseminated. Symptomatic trees showed wide diversity in the proportion of the crown affected by the disease. In these trees, the branches located in the sectors without symptoms had green foliage and fruit production apparently similar to that observed in the branches of asymptomatic trees. In contrast, the branches located in symptomatic sectors had yellowish foliage and less fruit. Of the 2 800 positions sampled with the ring, 1 505 were located in asymptomatic sectors and 1 295 in sectors with symptoms. Positions located in asymptomatic sectors recorded an average of 45.46 fr m-2 of treetop, while the positions corresponding to sectors with symptoms averaged 37.29 fr m-2 of treetop, which represents a reduction of 18% compared to that observed in sectors without symptoms (Table 1).

Table 1 Number of fruits per m2 of cup in sectors with and without symptoms in Mexican lime trees with different proportion of treetop affected by HLB. 

The above is explained because in the sectors of the tree showing HLB symptoms, most of the leaves show irregularly yellow spots (Robles-González et al., 2010) largely on its surface and is encouraged by the loss of green pigments. This can cause a sharp reduction of the photosyntates production in those leaves as pointed by (Nwugo et al., 2013; Xu et al., 2015). In some cases there is also a premature leaf drop (Robles-González et al., 2010). All this causes the sectors affected by the HLB to reduce its fruit production capacity, as estimated by Bassanezi et al. (2011) for different varieties of sweet orange.

Fruit production in trees with different percentage of treetop affected by HLB. When analyzing data of fr m-2 of treetop of sectors with and without symptoms and relate them to the different proportions of treetop showing HLB symptoms, it was determined that the production of fruit, is not only affected in those branches located in sectors with disease symptoms. As can be seen in Figure 1, both the symptomatic and the asymptomatic sectors show a clear tendency to reduce the number of fruits per square meter of treetop, as the treetop percentage increases in the trees manifesting HLB symptoms. With these data, the equation y= -7.0962 68.079 was generated with a value of R2= 0.91 for sectors without symptoms. Symptomatic sectors showed a similar trend and generated the equation y= -4.7304x + 53 864 and R2= 0.81. The above shows that, although the disease occurs in a sectorized way in the treetop and clearly reduces fruit production in sectors with symptoms, it also causes a generalized loss of vigor in the whole tree, which translates in reduced capacity of fruit production also in the sectors without symptoms.

Figure 1 Fruits per square meter in sectors with and without HLB symptoms in Mexican lime trees with different percentage of treetop affected by the disease. 

Such production losses are accentuated as the percentage of treetop area affected by the HLB increases. This result differs from the indicated by Bassanezi et al., 2011 who concluded that the HLB is restricted to the branches with symptoms of the disease. In other studies with Mexican lime, it could also be determined that trees affected by HLB tend to produce more vegetative buds, but reduce the emission of shoots with inflorescences (Robles-González et al., 2013b) which may explain a part of yield reduction.

It seems that the loss of green pigments in the leaves with HLB symptoms, which leads to the reduction in the photosynthetic activity and consequently less production of photoasimilates, not only impacts the branches affected by the disease. The lower production of photosyntates, together with the reduction of its transport to other organs, especially the root, is likely to affect the overall vigor of the tree. Although the effect of disease in root density has not been studied, it is presumed that the amount of tree roots decreases in tres affected by the disease, as suggested by Graham et al. (2013).

Fruit production in trees with different level of affectation in the treetop.

When analyzing data of fr m-2 of treetop and relate them with the percentage of treetop affected by HLB, it can be seen that asymptomatic trees which served as control showed the highest amount of fruits, with significantly different average to that recorded in the trees that showed symptoms of the disease. As shown in Table 2, trees with 10 to 25% and 50 to 75% of its HLB-affected treetop produced 80% and 75% of fruit respectively, compared to the control. When the trees had between 50 and 75% of affected treetop, its yield was hardly of 65.7% with respect to the control. However, when the cup proportion affected by HLB reaches 75 to 100%, fruit yield barely reaches 45.6% with respect to the control. With these results it is clear that the production capacity of Mexican lime trees with HLB decreases as the percentage of treetop affected by the disease increases until reaching its minimum when the whole treetop shows the symptoms. This result has resemblance to what points Bassanezi et al. (2011) for different varieties of sweet orange.

Table 2 Number of fruits per m2 in Mexican lime trees with different percentage of treetop affected by HLB. 

This behavior in fruit production occurs in plantations with good agronomic management, especially irrigation and fertilization. In these orchards, when all trees reach 100% of HLB affected treetops, their yields can fall between 40 and 60% with respect to that determined in trees without HLB symptoms. However, in plantations with inadequate irrigation and fertilization, trees affected by HLB become practically unproductive.

Yield kg tree -1 year -1 before and after infection with HLB

Production losses of trees affected by HLB were also estimated in an experimental batch of INIFAP in which two Mexican lime varieties grafted on C. macrophylla were evaluated. In this experiment, the fruit yield had been recorded since 2008, when the plantation was two years old. In this plantation the HLB was detected since 2011. In that year, the two varieties under study registered annualized yields higher than 40 t ha-1. By 2013, 100% of the trees had HLB symptoms with affected treetop percentages exceeding 50%, which led to a slight reduction in yield in both varieties. However, by 2014 yields fell to 23.4 and 22.9 t ha-1 for ‘Colimex’ and ‘Lise’ respectively (Table 3).

Table 3 Annualized yields in two varieties of Mexican lime from 2010 to 2014. 

The results of both experiments help to explain the fall in the production of Mexican lime in the state of Colima, where the disease is affecting 100% of the trees in all producing areas. In this state, until 2011 the average yield per year in the state exceeded 20 t ha-1; however, from 2012 production showed a downward trend, reaching an average of only 9.3 t ha-1 2014 (SIAP-SAGARPA, 2015). It is important to note that the HLB disease has caused producers to start improving their orchards, leading to improve fruit yields and by 2015 and a state average of 10.55 t ha-1 (SIAP-SAGARPA, 2016) was recorded.

Conclusions

It was possible to determine that HLB causes a generalized loss of vigor in Mexican lime trees, which is aggravated as the percentage of treetop affected by the disease increases and results in a reduction in fruit production capacity, both in the symptomatic sectors as in the sectors without symptoms of the trees affected by the disease. This reduction in fruit production is directly related to the treetop percentage showing symptoms of the disease. When HLB manifests itself in 100% of the treetop, it causes losses of production near to 50% compared to the trees without symptoms. This occurs in plantations with good agronomic management, especially in irrigation and fertilization. However, in plantations with poor irrigation and fertilization, trees become practically unproductive. Good management of nutrition and the use of higher planting densities can help to recover the yield of plantations and to reduce the impact of HLB on this citrus.

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Received: March 2017; Accepted: May 2017

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