Study area

The experiment was established during the years 2015 to 2018 in three regional control areas (ARCOs) located in the municipality of Padilla, El Barretal, El Carmen, Estación Santa Engracia, Güémez and Victoria, Tamaulipas (Figure 1).

Figure 1 Geographical location of the regional control areas (ARCOs) in Tamaulipas, Mexico. 

ARCO 1 was made up of 5 402.38 ha, 65 commercial orchards (Table 1) sown with Valencia orange trees. The average age of the trees was 15 years, the separation between the trees and lines was four and seven meters. The trees were watered with a furrow irrigation system.

ARCO 2 was made up of 3 491.23 ha, 49 commercial orchards (Table 2) sown with Valencia orange. The average age of the trees was 15 years, the separation between the trees and rows was four and seven meters. The trees were watered with a furrow irrigation system.

ARCO 3 consisted of 1 575.75 ha; 18 commercial orchards (Table 3) sown with Italian lemon trees. The average age of the trees was five years, the separation between the trees and rows was four and seven meters. The trees were watered with a micro-sprinkler irrigation system.

Record of the phenology of citrus trees

The record of the phenology of the Valencia orange and Italian lemon crops was carried out every eight days taking as a reference what was published by ^{Robles and Delgadillo (2010)}; ^{Lozano and Jasso (2012)}.

Monitoring of D. citri adults in the ARCOs

The adults were captured with yellow traps of 7.5 cm by 12.5 cm, stamped with a black grid of 1.5 cm and accompanied by a base covered with the adherent Stick Bug 50%^®. In the orchards, the traps were placed based on the HLB campaign operating manual. Ten traps were placed on the periphery (South-East) and 10 traps in a transverse line to it, at a distance between traps of 12 m and 1.20 m from ground level. The traps were replaced every eight days and the number of adults was quantified in the laboratory. In ARCO 1, ARCO 2 and ARCO 3, 1 300, 980 and 360 traps were installed.

Statistical analysis

The number of D. citri individuals were grouped into six categories with ranges from 0 to 100 individuals, taking as a reference that the lowest number of adults captured per month is 20 and the largest is 134 (^{Flores et al., 2017}). The categories of the population densities of the insect were: pest 1 (0 individuals), pest 2 (1 to 100 individuals), pest 3 (100 to 200 individuals), pest 4 (200 to 300 individuals), pest 5 (300 to 400 individuals) and pest 6 (400 to 500 individuals). The categories were associated with the phases of shooting, shooting-fruiting, shooting-flowering, shooting-development and dormancy of commercial orchards of Valencia orange (ARCO 1 and 2) and Italian lemon (ARCO 3).

Finally, the categories were subjected to a multivariate analysis of multiple correspondence (^{Benzécri, 1973}; ^{Greenacre, 1983}). The analysis considers the percentage of inertia of the X and Y axes, interpreting the one with the highest percentage of inertia. The interpretation of the results consists of associating the categories with greater proximity considering frequency data without losing the identity or origin of the sampled sites (^{Rencher, 2002}).

Phenology of the Valencia orange and Italian lemon crops

The Valencia orange trees presented the following phenology: shoot production, flowering, fruit development, dormancy and fruiting. The production of shoots occurred from January to July and from October to December, fruiting occurred in January and December. Flowering began in late March and ended in the third week of April, the development phase began in late April and ended in July and the dormancy phase occurred in late July and ended in the first week of October. On the other hand, the Italian lemon trees presented the following phenology: shoot production, flowering, fruit development and fruiting. The production of shoots occurred all year round, fruiting occurred in January and December, flowering began at the end of March and ended in the third week of April and the development phase began at the end of April and ended in July.

Seasonal abundance of D. citri associated with the phenological phases of citrus fruits in the ARCOs

In 2015, the D. citri population presented two significant associations with the phenological phases in the three ARCOs X²= 1664.78, d.f.= 121 (Figure 2). Populations of 1 to 100 individuals were associated with the shooting-development phase in ARCO 1 (A1). Whereas populations of 1 to 100 individuals were associated with the shooting-development, shooting-flowering and dormancy phases in ARCO 2 (A2) and population densities of 100 to 200 individuals were associated with the shooting phase in ARCO 3 (A3).

Figure 2 Analysis of the association of seasonal abundance of Diaphorina citri in the phenological phases of the Valencia orange and Italian lemon crops in three regional control areas in 2015. The categories of population densities of the insect were pest 1 (plaga 1) (0 individuals), pest 2 (plaga 2) (1 to 100 individuals), pest 3 (plaga 3) (100 to 200 individuals), pest 4 (plaga 4) (200 to 300 individuals), pest 5 (plaga 5) (300 to 400 individuals) and pest 6 (plaga 6) (400 to 500 individuals). 

In 2016, D. citri adults showed a significant association with the phenological phases in the three ARCOs X²= 1998.24, d.f.= 169 (Figure 3). Populations of 100 to 200 individuals were associated with the shooting-development phase in ARCO 1 (A1). Whereas populations of 400 to 500 individuals were associated with the shooting-development phase in ARCO 2 (A2). Similarly, densities of 400 to 500 individuals were associated with the shooting phase in ARCO 3 (A3).

Figure 3 Analysis of the association of the seasonal abundance of Diaphorina citri in the phenological phases of the Valencia orange and Italian lemon crops in three regional control areas in 2016. The categories of population densities of the insect were pest 1 (plaga 1) (0 individuals), pest 2 (plaga 2) (1 to 100 individuals), pest 3 (plaga 3) (100 to 200 individuals), pest 4 (plaga 4) (200 to 300 individuals), pest 5 (plaga 5) (300 to 400 individuals) and pest 6 (plaga 6) (400 to 500 individuals). 

In 2017, two associations occurred between the number of D. citri individuals with the phenological phases in the three ARCOs (X²= 2087.39, df= 169) (Figure 4). The first association was carried out with population densities of 1 to 200 individuals in the shooting phase in ARCO 3 (A3). For the second association, populations of 200 to 300 individuals were associated with the shooting-flowering and shooting-development phases in ARCOs 1 and 2 (A1, A2).

Figure 4 Analysis of the association of seasonal abundance of Diaphorina citri in the phenological phases of the Valencia orange and Italian lemon crops in three regional control areas in 2017. The categories of population densities of the insect were pest 1 (plaga 1) (0 individuals), pest 2 (plaga 2) (1 to 100 individuals), pest 3 (plaga 3) (100 to 200 individuals), pest 4 (plaga 4) (200 to 300 individuals), pest 5 (plaga 5) (300 to 400 individuals) and pest 6 (plaga 6) (400 to 500 individuals). 

In 2018, the population of D. citri presented significant associations with the phenological phases in the three ARCOs (X²=2313.21, df= 196) (Figure 5). Population densities of 1 to 100 individuals were associated with the shooting, shooting-flowering, shooting-fruiting and dormancy phases in ARCO 1 (A1). Population densities of 100 to 200 individuals were associated with the shooting-development phase in ARCO 2 (A2). Finally, densities of 200 to 300 individuals were associated with the shooting phase in ARCO 3 (A3).

Figure 5 Analysis of the association of the seasonal abundance of Diaphorina citri in the phenological phases of the Valencia orange and Italian lemon crops in three regional control areas in 2018. The categories of population densities of the insect were pest 1 (plaga 1) (0 individuals), pest 2 (plaga 2) (1 to 100 individuals), pest 3 (plaga 3) (100 to 200 individuals), pest 4 (plaga 4) (200 to 300 individuals), pest 5 (plaga 5) (300 to 400 individuals) and pest 6 (plaga 6) (400 to 500 individuals). 

The abundance of D. citri was different in the ARCOs and in the years of study. According to ^{Razeto (2005)}, the variety of the cultivar and the production of shoots in citrus trees influences the abundance of D. citri. In the present work, the difference in the abundance of D. citri was possibly due to the amount and period of production of shoots in the Valencia orange and Italian lemon crops, since the orange crop produces fewer shoots (38.70 shoots/month) per year than the lemon crop (673.5 shoots/month) (^{Medina et al., 2007}; ^{Chávez et al., 2016}).

In the ARCOs, the Valencia orange trees produced shoots from January to July and from October to December. Whereas the Italian lemon trees presented shoots all year round, possibly due to the micro-sprinkler irrigation system, use of fertilizers, pruning of the trees and because the lemon trees are younger (five years) than the orange trees (^{Pluke et al., 2008}). While orange orchards do not have an irrigation system, fertilizer use is limited, and trees are on average 15 years old.

In the three years, the highest abundance of D. citri recorded in ARCO 3 was associated with the shooting phase of the Italian lemon crop. Whereas the greatest abundance recorded in ARCO 1 and ARCO 2 was associated with the shooting and shooting-development phases of the Valencia orange crop. In both crops, D. citri occurs in the phase of production and development of shoots, because adults and nymphs feed on them to mature their eggs and complete development (^{Ortega et al., 2013}). Although adults also feed and survive for several months on fully developed leaves (^{Tsai et al., 2002}; ^{Fernández and Miranda, 2005}; ^{Stansly and Qureshi, 2007}; ^{Qureshi and Stansly, 2008}). ^{Hall et al. (2008)} indicated that population peaks of D. citri occur when there are favorable environmental conditions and shoots availability.

In this regard, the Italian lemon crop produced shoots all year round (the greatest abundance of shoots was observed from December to March) and D. citri was present in the trees. Similarly, this has occurred in the Mexican lemon crop in the municipality of Apatzingán, Michoacán (^{Luna et al., 2018}). D. citri is present throughout the year because the crop produces shoots constantly. However, the maximum population peak occurs in August because of the favorable environmental conditions for the insect. A similar result was determined in the Persian lemon (C. latifolia) in the municipality of Huimanguillo, Tabasco (^{García et al., 2013}).

As in Mexican lemon orchards, this crop produces shoots constantly and the greatest abundance of D. citri occurs from March to July. Conversely, in the Mexican lemon in Acapulco, Guerrero, the smallest adult population of D. citri occurred in February, when the trees were in the shoot production stage. Whereas the greatest abundance occurred in April and November, in the stage of fruit set and fruit development, respectively. In this case, low rainfall (^{Botero et al., 2014}) and optimal temperature played an important role in the occurrence of high population peaks of D. citri in trees (25 to 28 °C) (^{Liu and Tsai, 2000}; ^{Paris et al., 2017}).

Contrary to the Italian lemon crop, the Valencia orange trees did not produce shoots all year round. However, the greatest abundance of D. citri occurred in the phase of production of shoots and in the development of these. A similar result was reported by ^{Ortega et al. (2013)} in Cazones, Veracruz. The authors recorded the periods of greatest abundance of D. citri in orange trees (C. sinensis cv Mars, C. sinensis cv Valencia) and sweet lime (C. limetta) from February to April and in July, which coincide with the phase of production and development of shoots.

Conclusions

During the years 2015 to 2018, the population size of D. citri was different in all three ARCOs. In this result, the phenology of the crop played an important role. Because the greatest abundance of the insect was recorded in the phase of production of vegetative shoots.