Population of Bemisia tabaci and Incidence of Yellow Disease in Chili Intercropped with Corn

Bemisia tabaci is one of the limiting factors in chili farming, because it can cause damage both directly and indirectly as a vector for the Pepper yellow leaf curl virus (PepYLCV). Intercropping chili with corn is one of the efforts to control B. tabaci . Physically, corn plants are able to withstand the presence of B. tabaci , in addition to producing volatile compounds that are repellent to B. tabaci . This research was conducted to determine the optimal age of corn plants to be intercropped with chili plants. The research was conducted in Pleret District, Bantul Regency by testing five different ages of corn: 2 weeks after planting, 6 weeks after planting, 8 weeks after planting, 10 weeks after planting and control (without intercropping with corn). Weeks after planting are counted from the first day the corn seeds were planted. Yellow sticky trap was used to determine the presence of B. tabaci population in each treatment plot. Yellow sticky trap was tied to bamboo sticks and placed on treatment beds with as many as 2 (two) traps per treatment plot. The distance between the yellow sticky trap and the plant was 30 cm, so the height of the trap was always adjusted according to the height of the plant. Observation of B. tabaci population was carried out every 5 days by counting the number of B. tabaci caught in yellow sticky traps. The results showed that the population of B. tabaci in the chili plots intercropped with corn was lower than that in the control plot, especially at the age of 6 weeks after planting (WAP). However, the intercropping of chilies and corn had no significant effect on the incidence of yellow disease in chilies


INTRODUCTION
Chili is one of the leading horticultural commodities that is widely cultivated and has the highest price fluctuations in Indonesia (Adriani et al., 2019).The harvested area for red chilies in 2019 ranks at the top compared to other vegetable commodities (Centre for Agricultural Data and Information Systems, 2020).Chili productivity in Indonesia is still relatively low compared to other countries in Asia.Several factors have contributed to the low productivity of Indonesian chilies, including the use of inferior seeds, inefficient cultivation techniques and pest and disease attacks (Soelaiman & Ernawati, 2013).One of the pests that attack red chili plants is the whitefly, Bemisia tabaci Gennadius.
Damage caused by B. tabaci attack on chilies can occur directly or indirectly.Direct damage occurs when whitefly causes leaves to become chlorosis and drop, or plants become stunted due to feeding activity.Meanwhile, indirect damage occurs when the honeydew released by whitefly grows sooty fungi which can reduce the rate of the photosynthesis process thereby reducing fruit quality (McAuslane & Smith, 2015).In addition, the whitefly B. tabaci is a vector that can transmit Pepper yellow leaf curl virus in chilies (PepYLCV) and the distribution of Pep YLCV increases respectively to B. tabaci populations.Whiteflies can persistently spread the virus, which means once it feeds on a viral-loaded plant, it will persist in the insect's body throughout its life.
Thus, the virus can be transmitted even after the vector is shed (Nigam, 2021).This virus can cause significant yield loss (Ashwathappa et al., 2020), especially in chili pepper (Zaidi et al., 2017) that can even reach 100% of yield loss (Kenyon et al., 2014).
One strategy to suppress B. tabaci populations is to use border plants.Friarini et al. (2016) proved that corn was quite effective in reducing the spread of B. tabaci in red chili planting plots, which in turn was also able to inhibit the spread of the yellow virus in red chilies.Meanwhile, Udiarto et al. (2023) also proved that cultivating corn as a limiter and in combination with sunn-hem can reduce the incidence of chili yellow disease by up to 49.94 -50.80%.
Corn have been known to produce volatile organic compounds that were not favored by B. tabaci (Tyasningsiwi et al., 2019).Corn leaves are known to contain volatile compounds with carbon groups, namely (Ζ)-3-hexenol (2-7%), (Ζ)-3-hexenyl acetate (3-14%), (Ζ)-4-hepten-2-one (2-8%) and (Ζ)-4-hepten-2-ol (2-4%) (Buttery & Ling, 1984).Konstantopoulou et al. (2004) showed that the volatile compounds of corn plants quantitatively affect the oviposition behaviour of female Sesamia nonagrioides where filter papers containing volatile compounds with higher aldehyde groups has fewer eggs than those with lower aldehyde groups.In addition, corn silk also contains a wide range of bioactive compounds in the form of volatile oils, steroids, and other natural antioxidants, such as polyphenols and flavonoids (Bhuvaneshwari & Sivakami, 2017;Singh et al., 2022;Žilić et al., 2016).Tyasningsiwi et al. (2019) reported that corn grown in a greenhouse produces different volatile compounds at each age stage.The most optimal age of corn in producing repellent compounds is 12 weeks after planting (WAP), with a rejection rate of B. tabaci of 83.72%.However, information on the ability of corn plants to resist B. tabaci at the field settings are still limited.Therefore, this study aims to examine the ability of corn plants to resist B. tabaci in the field.

MATERIALS AND METHODS
The research was conducted at a chili plantation field in Pleret District, Bantul Regency, Yogyakarta and The Laboratory of Pest Science, Department of Plant Pests and Diseases, Faculty of Agriculture, Universitas Gadjah Mada from August 2022 to August 2023.

Field Experiment
The corn variety used in this study was BISI-2, while the chili variety used in this study was LABA.The study was conducted to test the ability of corn to resist B. tabaci.The treatment used was the age of the corn plant.Corn plants at the age of two, six, eight, and ten weeks after planting (WAP) compared to controls (no corn plants at a radius of 30 meters).Weeks after planting (WAP) are counted from the first day the seeds were planted.Each treatment was repeated five times.Chili and corn plants were planted in beds measuring 100 cm 500 cm with a distance of 40 cm between the beds.Two beds of chili plants are flanked by one bed of corn plants according to the treatment used.To prevent the influence of corn plants on other plots, each treatment plot was spaced 10 meters apart (Figure 1).Corns were planted earlier than chilies according to the treatment used.Transplanting chilies were carried out when the chilies were 4 weeks old with a planting distance of 40 cm × 50 cm.
Yellow sticky trap (YST) was used to determine the presence of B. tabaci population in each treatment plot.YST was tied to bamboo sticks and placed on treatment beds with as many as 2 (two) traps per treatment plot.The distance between the yellow sticky trap and the plant was 30 cm, so the height of the trap was always adjusted according to the height of the plant.
The parameters observed in this test were the number of B. tabaci caught in the yellow sticky trap and the incidence of yellow diseases.Observation of the number B. tabaci was conducted during dry season of September -October 2022 and carried out every five days until the chili plants are 60 days old.Observation of the incidence of yellow diseases was carried out every 15 days since the age of chili 30 days after planting to 75 days after planting (DAP).Disease incidence was calculated using the formula (Masnilah et al., 2020): DI= percentage of yellow disease incidence; n= number of plants affected; N= the number of plants observed ISSN 1410ISSN -1637 (print) (print), ISSN 2548-4788 (online)

DI = n × 100% N
The data obtained were analyzed by analysis of variance (ANOVA) and the differences between treatments were determined using the Tukey test at the 5% level.

Mass Rearing of B. tabaci
Mass rearing of B. tabaci was carried out based on the method of Rinaldi et al. (2016) with modification by researchers.The imago of B. tabaci were caught from eggplant, chili and tomato plantations.The imago of B. tabaci obtained from the field were placed in cages made of wood covered with gauze measuring 150 cm × 150 cm × 150 cm and filled with eggplant plants as host plants.Twenty (20) polybags of host plants aged ± 4 WAP were placed in cages.An infected plant was replaced with a new healthy plant.The imago of B. tabaci used in this test were 10 females starting from the second generation (F2) after collection from the field for each treatment in each replication.The use of B. tabaci females, based on Hasyim et al. (2016) where female whiteflies have a higher level of virus transmission efficiency compared to male insects.

Test of Corn Volatile Compounds as a Repellent for B. tabaci Using Olfactometer
This test was carried out using corn plant which give best repellency result in field test.Corn plants were placed in plastic boxs sizing 40 cm × 40 cm × 150 cm for about 24 hours to collect the volatiles produce by the plant.Collected volatile compounds in the plastic box then be transferred to olfactometer using aerator.Volatile compounds were drained from inside the plant cover using an aerator and connected to an olfactometer.The olfactometer test used a Y-shaped glass tube with a diameter of 1.3 cm, with a long base and two hands of 10 cm each.Each end of the Y-tube was covered using gauze.One of the tube hands was perforated to be connected to the aerator hose so that gas from inside the hood can be channeled into the olfacto-meter tube.Then faced with a small fan to blow air slowly so that it directs B. tabaci towards the two hands of the tube.This test was carried out in a closed room with even lighting between the right and left Y-tube hands.This is to prevent B.

Population of B. tabaci
The field test results for the repellency of B. tabaci in corn showed that the corn crop caused a decrease in the population of B. tabaci in chili plants.The population of B. tabaci on chili crops accompanied by corn crops was significantly different from the control, namely chili crops which were not accompanied by corn crops.The age of the corn crops used to accompany the chili crops also had influences on B. tabaci populations which were trapped in the yellow sticky traps.The most optimal age of corn crops used to accompany chili crops was corn aged 6 WAP, because the population of B. tabaci was significantly lower (P <0.05) than the treatment at corn ages 2, 8, and 10 WAP (Figure 2).
The high population of B. tabaci in the 2 WAP corn treatment could be due to the fact that the corn crops were still too young so that they had not been able to provide optimal assistance effects both physically and in terms of the production of volatile compounds repelling B. tabaci.According to Arimura et al. (2004), in general, vegetative tissues release volatile compounds in small quantities, which can be caused by mechanical damage and infection by herbivores or pathogens.The most optimal repellent ability was found in the treatment of corn aged 6 WAP.At this age, corn crops had entered the tasselling and silking phase, where physically, the leaves of the corn plant are fully opened and produce male and female flowers.The results of the study by Knudsen et al. (2006) stated that the most diverse mixtures with the highest abundance of volatile compounds were released mainly from flowers in most flowering plants.This is in accordance with the research of Tyasningsiwi et al. (2019), which showed that the composition of volatile compounds was higher as the age of the corn crops get older.The repellent ability of corn plants at the age of 8 WAP and 10 WAP were not high even though at these ages they had also entered the tasselling and silking phases.Corn plants aged 8 and 10 WAP could not optimally accompany chili plants because the time period was narrower than corn plants 6 WAP.The harvesting age of corn crops was 15 WAP so that when chilies reach the optimal age for the development of B. tabaci, they are no longer accompanied by corn crops.According to Yuliani et al. (2006) stated that the B. tabaci populations increase and reaches its peak when the chili plants are between 63-77 DAP, then the population of B. tabaci will decrease again.The population decline was due to the chili plants at that age no longer having young leaves or their vegetative growth had stopped making them less suitable to be used as hosts for B. tabaci again.
The ability of corn crops to produce volatile compounds that were repellent to B. tabaci is strengthened by B. tabaci trap data before and after corn ISSN 1410-1637 (print), ISSN 2548-4788 (online) plants were harvested.Based on the observations, it was known that there was an increase in the population of B. tabaci after the corn plants were harvested at the age of 6, 8, and 10 WAP treatments, on the contrary there was a decrease in the B. tabaci population after the corn plants were harvested in the 2 WAP treatment (Figure 3).There was no significant difference in the population of B. tabaci before and after the corns were harvested at the age of 2 and 6 WAP.This could be due to the corn harvest time in the two treatments which had entered the rainy season.Corn harvest for treatments aged 2 WAP and 6 WAP were carried out in October and November where the rainfall was higher than in September (harvest time for treatments 8 WAP and 10 WAP).Based on data from the Yogyakarta Climatology Station, in October and November, rainfall in Pleret District reached 380.4 mm and 666.6 mm (Meteorological, Climatological, and Geophysical Agency, 2023).This rainfall is much higher than when harvesting corn treatment aged 8 and 10 WAP which was carried out in September, namely 19.5 mm.According to Sudiono and Purnomo (2009), rainfall affects the population of B. tabaci, the higher the rainfall, the whitefly population decreases.The high intensity of rain causes the population of B. tabaci to naturally stress, drives insects away from the plants and can also affect microclimatic conditions through cooling (Dobkin et al., 1987;Kamata & Igarashi, 1994).

Incidence of Yellow Disease
The observation results showed that the incidence of yellow disease increased at each observation interval.The results of the analysis showed that the incidence of yellow disease in chili aged 30 and 60 DAP was not significantly different between the four treatments but significantly different from the controls.The incidence of yellow disease increased at the age of 45 DAP and there was no significantly difference between the corn treatment and the control.The incidence of yellow disease at the end of the observation (75 DAP) was not significantly different between the four treatments, but was significantly different between the 2 and 6 WAP corn treatments and the control (Table 1).
The incidence of chili yellow disease increased with the age of chili in all treatments and controls.Age treatment of corn crops did not affect the incidence of yellow disease.Based on statistical analysis, the incidence of yellow disease was significantly different in treatments 2 and 6 WAP compared to the control (without corn).The lowest incidence of yellow disease occurred in the chili plants accompanied by corn age 6 WAP.According to Jeger (2020), the occurrence of disease incidents in plants is influenced by several things such as virus virulence or the ability of viruses to cause disease, the influence of plant genotypes or varieties, and most importantly the influence of the abundance of insect vectors supported by environmental conditions.One of the factors that play a very important role in the spread of yellow disease caused by this virus is the presence of the insect vector of the virus, namely the whitefly (B.tabaci).The higher the population of B. tabaci, the higher the incidence of yellow disease (Narendra et al., 2017;Taufik et al., 2023;Temaja et al., 2022).Bemisia tabaci transmits the yellow virus persistently from diseased plants to healthy plants.Bemisia tabaci acquires the virus when it takes food from diseased plants or plants that have been infected with the yellow virus.The virus taken from diseased plants enters through the digestive tract, penetrates the intestinal wall, circulates in the insect's body fluids (hemolymph) and then in the salivary glands.When B. tabaci sucks food from healthy plants, the virus that has been in the salivary glands will indirectly enter the body of the plant along with the fluids from the insect's mouth.
The incidence of yellow disease increased at the age of 45 DAP and there was no significantly difference between the corn treatment and the control.This can be caused by transmission of yellow virus disease which has occurred since the vegetative phase, both in the treatment and control.The success of Gemini virus transmission is closely related to the vector insect and the incubation period.Selangga et al. (2019) stated that the incubation period for Gemini virus in chili plants ranges from 7-28 days after the plants are inoculated with the virus.

Results of the Repellence Test of Corn Volatile Compounds against B. tabaci Using an Olfactometer
The olfactometer test was only carried out on corn plants aged 6 WAP where the results of observations showed that the population of B. tabaci was the lowest compared to other corn age treatments.
The results of the corn volatile compound repellence test against B. tabaci are shown in Table 2.
The percentage of repellency of corn volatile compounds against B. tabaci was 68.57± 27.53 (%) and entered class 4. The resulting repellent index comes from the greater number of B. tabaci in the control hand than the B. tabaci in the corn volatile compound treatment hand.The large number of B. tabaci in the control hand was because corn plants contain compounds that act as insect repellents.Repellent volatile compounds are produced from plant secondary metabolites, including: monoterpenes, diterpenoids, aromatic esters, flavonoids, and alkaloids.These compounds are obtained from all parts of the plant, namely flowers, leaves, shoots, and nectar (Pohan, 2014).The results of Tyasningsiwi et al.'s research (2019) which was conducted on a greenhouse scale showed that corn plants aged 6 WAP produced citronellyl acetate compound which was repellent to B. tabaci with a repellency rate of

CONCLUSION
Corn crops were able to resist the presence of B. tabaci on chili crops, and corn aged 6 WAP was proven to provide the most optimal repellence effect.However, the presence of corn crops did not significantly affect the incidence of yellow disease in chilies.
Figure 1.Chili and corn planting design

Figure 2 .
Figure 2. The population of Bemisia tabaci caught in the yellow sticky trap at each age treatment of corn crops (numbers followed by different letters were significantly different according to Tukey Test [α = 0.05]; WAP = weeks after planting)

Figure 3 .
Figure 3.The population of Bemisia tabaci before and after the corn plants were harvested at each age treatment of the corn crops (numbers followed by different letters were significantly different according to t-Test [α = 0.05]; WAP = weeks after planting)

Table 1 .
Incidence of yellow disease at various ages of corn plantingRemarks: Numbers followed by the same letter were not significantly different according to Tukey Test (α = 0.05); WAP = weeks after planting; DAP = days after planting Table 2. Results of the repellency test for corn volatile compounds against Bemisia tabaci with an olfactometer Age of Corn Planting Incidence of yellow disease in chili crop (%)