The Effectiveness of Abamectin Insecticide in Suppressing the Population of Liriomyza spp (Diptera: Agromysidae) on Red Onions

The main problem of maintaining and increasing the red onion production in Indonesia is the pest attack (OPT) from leafminer flies (Liriomyza spp.) (Shahabuddin et al., 2015). These leafminer flies increase the damage level up to 60-70% and cause yield loss up to 20-80% (Rauf et al., 2000; Shahabuddin et al., 2013). So far the controlling method taken by farmers in order to minimize the yield loss by selecting and applying the insecticide (Barbosa et al., 2018; Mujica and Kroschel, 2013).
        
The farmers are apt to apply the insecticides unjudiciously and non-eco-friendly manners of 2-3 of spraying in a week (Jaya et al., 2015). It has been found that the intensive, broad-spectrum and unwise insecticide applications cause of disruption of ecosystem stability due to the death of some natural enemies (Kalaisekar et al., 2017; Leppla et al., 2018; Matthews, 2017; Shearer et al., 2016).
        
Type of insecticides that are commonly used by farmers contained Abamectin and Spinoteram active materials, working in contact, gastric and systemic that can cause cell malfunction in the insects’ digestive tract, especially in the midgut (Aljedani, 2017; Srinivasa et al., 2014). Therefore, there is a need for pest management by applying broad-spectrum insecticide applications (Salvo and Valladares, 2007).
        
This research was aimed to analyze the effect of insecticide application on the population abundance and fluctuation, the attack percentage and the production of local Lembah Palu red onion varieties and the effect of insecticide application on the abundance of parasitoids Liriomyza spp. on red onion planting.

Location and Time of Research
The research was conducted in the farmers’ fields in
Guntarano Village, Tanantovea Subdistrict, Donggala Regency, Central Sulawesi and at the Laboratory of Pest Science, Faculty of Agriculture Tadulako University from August 2016 to June 2017.
 
Materials
 
This research was done in a 500-m² field of local Palu red onion planting which were divided into two plots, measuring 250 m² respectively and the distance between plots was 300 m.

•  The first plot was treated with Abamectin insecticide @ 1 ml per litre water, with spraying volume of 500 litre per ha and the second plot was left in treatment.
•  Abamectin insecticide was applied in once-a-week schedule, started from the age of 1 week old planting and ended 7 days before the harvest time.
•  Each plot was divided into 18 sub-plots of 6 m x 1.25m respectively, the distance between each sub-plot was 35 cm and planting distance was 15x15 cm.
 
Variables
The Abundance of Liriomyza spp.
 
The observation and the collection of leaf miner fly population  was carried out at the beginning of the second week, one day before the application and then a week later i.e. the third week until 7 weeks after planting by setting up 18 cylindrical yellow traps (yellow sticky traps) on each plot with 15-25 cm of height position above ground level (Baliadi and Tengkano, 2008). The traps were replaced each week and then, counted and identified them at the Laboratory of Pest Science, Tadulako University.
 
Liriomyza spp. attack percentage
 
The observation of Liriomyza spp. population was done by counting the number of leaves that showed the symptom of white dots. This population was taken every week, from 2-7 old after planting. For each sub-plot, 32 plants were randomly selected for observation. Type of damage was observed by counting the attack percentage done by Liriomyza spp. by using Pedigo and Buntin equation (Pedigo and Buntin, 1994):

 

 
Where:
P = Percentage of Liriomyza spp. attack.
n = Number of red onion leaves showing the symptom of white dots.
N = Number of red onion (groups) observed.
 
 
The Abundance of Parasitoid Liriomyza spp.
 
To find out the diversity of parasitoids in the plots by collecting 24 leaves that showed the symptom of being attacked by leaf miner flies. Each leave sample was kept in a plastic container in 3 cm diameter and 7 cm height. The emerged adult parasitoids were counted.
 
Insecticide residue
 
The analysis of chemical insecticide residue on local Lembah Palu red onions spraying with Abamectin insecticide from the Carbamate group every week, since the age of 2 weeks after planting until 7 weeks by employing LCMS-MS method.
 
Data analysis
 
Observed data was analyzed by using T-test at significance level of 5% by comparing treated and non-treated population, damage level, the number of natural enemies in plant samples and yield of treated and non-treated data. Prior to the analysis by means of T-test at significance level of 5%, the data was first tabulated into Excel software and continued with the T-test by the help of MINITAB program.

Based on the observation data and laboratory identification, there were two types of Liriomyza spp. associated with the local Lembah Palu red onion varieties in Guntarano Village during the planting period from September  to November, 2016, namely Liriomyza chinensis and Liriomyza sativae. Whereas, planting period from March to May 2017, there were three species of Liriomyza namely L. chinensis, L. sativae and L. huidobrensis (Fig 1).
 

        
The observation data indicated that the abundance of adult Liriomyza spp. population during the planting period from September-November 2016 was lower as compared to the planting period of March-May 2017 (Table 1). Among the three Liriomyza species, the population of Liriomyza chinensis in red onion crops since the age of 7 days up to 4 weeks after planting, both in treated and non-treated plots and increase of population was observed. Whereas, the population of adult  Liriomyza sativae was very low at the age of 2-4 weeks after planting both for treated and non-treated plots (Fig 2).
 

        
Observed population of Liriomyza sativae, revealed that it tended to increase its population at the age of 4, 5 and 6 in coincidence with the decreasing population of  Liriomyza  chinensis during the observation of 5 and 6 weeks after planting for all treatments. It was observed that Liriomyza. sativae population increased in line with the increase in the plant age. The decreasing population of adult Liriomyza. chinensis could probably be influenced by the red onion leaf morphology which suffered from hardening in their tissues thus stylet were unable to support and perform the eating activities.
        
The research results revealed that attack intensity of Liriomyza spp. applied with Abamectin insecticide was lower (33.84%) compared with the non-treated one (62% on 6 weeks after planting). Fig 2a and 2b presented the population of Liriomyza chinensis and Liriomyza. sativae was dominant on the red onion plots location non-treated plots. For the next planting period of March-May 2017, a new species emerged, i.e. Liriomyza Huidobrensis as the phenomenon from farmers changed their planting pattern.




 
Liriomyza spp. attack percentage
 
In general, the attacks on red onions during September-November 2016 demonstrated that Liriomyza spp. attack percentage were lower than the planting period of March - May 2017. Based on T-test analysis results, the planting season of September-November 2016 indicated that Abamectin insecticide application had influenced on lower attack percentage than without insecticide application (Table 2), with average of 2.91-39.02% as compared with the non-treated one on an average of 11.91-54.12% attack percentage per observed plots.
 

        
Fig 3 shows the percentage of leaves attacked by leafminer flies up to the age of 6 weeks after planting was lower in comparison with the non-treated with Abamectin insecticide application. Therefore, it can be said that the application of Abamectin insecticide was effective in suppressing the leafminer flies despite the data of high population abundance on the Abamectin insecticide treatment. During the planting period of March-May 2017, adult Liriomyza spp. population increased, which causes high attack percentage above 50% in the second week, resulted in red onions non-treated with Abamectin insecticide application were severely damaged.
 

 
Abundance of parasitoids Liriomyza spp.
 
According to the morphological identification results done in the laboratory, there were two parasitoid species associated with Liriomyza i.e.Hemiptarsinus varicornis and Neochrysochaeres Formosa (Hymenoptera: Eulophidae) (Fig 4). Research results showed that the non-treated plots had more abundant population of H. Varicornis (67.17%) and N. Formosa (28.78%), in comparison with the -treated ones, the population abundance of parasitoids H. Varicornis was 4.04% (Table 3). The field observation results showed that Abamectin insecticide application had effect on the abundance of parasitoid species and lower number of individuals compared with the non-treated ones.
 



        
The abundance of H. varicornis and N. Formosa populations was influenced by their main abiotic factor, namely environment. Field observation results revealed that red onion cultivation practice by implementing high insecticide application had negative influence on the parasitoid species life sustainability and lower number of individuals compared with the one without Abamectin insecticide application. Decreased number of natural enemies found in the area treated with Abamectin insecticide application caused harmful effect on natural enemies of parasitoids.
        
Abamectin insecticide application had influence on red onion production per square meter. The average production of red onion during planting period of September-November 2016 applied with insecticide was 9.61 tons per hectare; it was higher in comparison with the non-treated red onion production (8.20 tons per hectare) (Table 4).
 

        
That may be influenced by the planting season of September-November 2016 when the attack percentage of parasitoids Liriomyza spp. is lower. Meanwhile, the planting season of March-May 2017 mean yield of red onion applied with Abamectin insecticide is 2.07 tons per hectare, higher than without insecticide application (0.27 tons per hectare).
        
During the planting period of March-May 2017, there was severe attack by parasitoids Liriomyza spp. that caused most of the plants severely damage. It was found that higher production was obtained from the area applied with Abamectin insecticide than the area without Abamectin insecticide application, even though the obtained yields were highly different with the planting period of September-November 2016. That low production during planting period of March-May 2017 was caused by high attack percentage of parasitoids Liriomyza spp., above 50% in the second week.
        
The application of Abamectin insecticide had positive impact on the production, yet on the contrary had negative impact on the existence of some natural enemies. For cultivation of local Lembah Palu red onion varieties, it requires an integrated pest management concept for handling the attack from parasitoids Liriomyza spp. By this time and the presence of OPT are two determinant factors in deciding the policy for cultivation local Lembah Palu red onion varieties in Guntarano Village. In addition, monitoring steps should be taken for use of insecticide, when approaches economic level.
 
Abamectin active residue
 
The results of Abamectin insecticide residue analysis of Carbamate group (Table 5) on local Lembah Palu red onion varieties by using LCMS-MS method with weekly spraying application since the age of 2 to 7 weeks after planting showed the presence of pesticide residue on red onions with very low LOD value of 0.005. An interesting thing from this study was despite the fact of weekly Abamectin insecticide application on those red onions, the insecticide residue was low and hence it was safe for consumption.
 

        
In accordance with the research results, the population of adult Liriomyza chinensis tended to be stable and dominant on red onions even since in the early age of 7 days to 4 weeks after planting and showed the tendency of increased population in line with the increased plant age. Liriomyza chinensis species attack red onion since the age of 2 weeks after planting, they belong to monophagous insects with limited hosts of shallots and onions usually grown on low-lands and highlands (Rauf, 2005; Saleh et al., 2014). At the age of 4-5 weeks after planting, the presence of adult Liriomyza chinensis tended to decrease in number and replaced by adult L. sativae. Another research result showed that the decreasing number of Liriomyza chinensis was influenced by the morphology of red onion leaves that suffered from hardening in their tissues thereby the style were unable to support and perform eating activities (Arfan et al., 2018).
        
The increased population of Liriomyza sativae was likely influenced by some environmental factors, in which there were insecticide spraying applications nearby the experiment location resulted in migration, Liriomyza entered the experiment areas due to insecticide application. There was a phenological compatibility of parasitoids Liriomyza spp., in which the crops in the experiment area had been harvested and in coincidence with the crop that turning into their fifth-week age.
        
Low Liriomyza spp. population in the treated plots was probably caused by the effectiveness of applied Abamectin insecticide, which was able and effective in suppressing the growth of Liriomyza, spp. larvae. Some other research results showed that Abamectin indeed was highly effective in suppressing the population of Liriomyza (Ramesh and Ukey, 2007; Saad et al., 2007). Abamectin insecticide has caused the malfunction of some cells in those insects’ digestion, more especially in the midgut (Aljedani, 2017). Abamectin application had decreased Liriomyza larvae significantly lower population of adult Liriomyza, spp. The treatment with abamectin 1.9 EC @ 0.4 ml/l (0.0007%) was found most effective in recording the least nymphal population of citrus psylla at 3^rd, 7^th and 14^th days after sprays over rest of the treatments (Wankhade et al., 2015).
        
The decreasing number of natural enemies found in the areas applied with Abamectin insecticide had caused the lessening role of parasitoid natural enemies. One of determinant factors that affected the life of natural enemies of parasitoids was mainly due to the spraying intensity and the application of broad-spectrum insecticide (Pratama et al., 2013). Insecticide application, particularly the organic synthetic one, is highly effective in controlling the pests and helping to maintain the production and quality of yields.

The application of Abamectin insecticide was effective in suppressing the growth of Liriomyza spp. population, there were two species that attacked red onion crops, i.e. Liriomyza chinensis and Liriomyza sativae, with population abundance of 33.2%, attack percentage of 39.02% and production of 9.61 tons per hectare. Abamectin insecticide application had real influence on the parasitoid species, with population abundance of 4.04% for H. varicornis. There are two parasitoid species associated with Liriomyza, namely Hemiptarsinus varicornis and Neochrysochaeres Formosa (Hymenoptera: Eulophidae).

The authors would like to thank the Directorate of Research and Community Service of the Directorate General for Strengthening Research and Development at the Ministry of Research, Technology and Higher Education.