Thecodiplosis japonensis Uchida et Inouye mainly inhabits Korea and Japan. In Korea, population outbreaks of this insect were first recorded in 1929 in Biwon, Seoul, and Mokpo basin, Jeollanam-do (Takagi et al, 2003). These two areas have become the distribution sources of T. japonensis, and its outbreaks have expanded throughout Korea.

Thecodiplosis japonensis forms galls on the needles of Korean red pines and Japanese black pines, impeding the growth of new branches and causing damaged needles to die within the infected year. In the case of black pines, the needles remain on the trees until the next year, reducing the quantity of food assimilation, thus hindering plant growth and vigor, and resulting in the occurrence of secondary harmful insects (Yim et al, 1981).

Many studies have been conducted on T. japonensis including its life cycle, ecology, and control strategies in Korea and other countries. Studies have investigated morphological features of dead and alive trees (Jeong and Hyun, 1986). Gall formation rate of T. japonensis has been reported to increase rapidly for six to 12 generations in newly invaded areas (Park and Hyun, 1983). As a result, pine growth decreases, leading to mortality, and decreases in tree densities. In addition, the initial and recovery periods of T. japonensis have been compared within and between generations, and it was reported that differences in larval stages of each region were caused by larval death and a parasitic bee (Lee, 1986). Ecological variation among populations of T. japonensis in southern and northern areas of Korea, such as Mooan of Jeonnam and Hoingseong of Gangwon (Hwang and Yim, 1990), indicated that genetic differentiation has occurred across 60 generations of T. japonensis. A study on population dynamics of T. japonensis indicated that decreases in the death rate within the entire population under the same ecological conditions was 23.1% during the warm period, 14.2% inside the gall , 25.0% during the underground period before wintering, and 52.9% and 32.0%, respectively, during the prepupal and pupal periods; changes in soil water content were most important to T. japonensis mortality. Furthermore, as the amount of damage by T. japonensis increased, the emergence rate and size of their larvae decreased (Park and Hyun, 1977).

In nature, insects exist as a part of biotic community and different environmental factors can cause variations in their evolution. Plant damage caused by pollutants has been shown to influence the ecological adaptation of insects in a report on environmental biological indicators (Jeong and Hyun, 1986). Air pollution caused by petrochemical industry also can affect crops and forests and has become a serious social issue. Furthermore, studies have reported that plant production varies with proximity to pollution sources (Kim, 1988). Thus, the distribution of T. japonensis around an industrial complex may provide insight into T. japonensis damage on trees.

Accordingly, this study was conducted to investigate the relationships between gall formation rates of T. japonensis and air pollutants of the Onsan industrial complex of Ulsan. Sites were selected according to their distance from the pollution source (i.e., Onsan industrial complex) to investigate the habitat distribution of T. japonensis to provide basic information for future insect control.

Materials and Methods

Site selection

Ulsan Duckshin, Ulsan Haknam, Ulsan Okdong, Ulsan Duwang, and Ulsan Chungryang were selected as investigation areas according to their distance from industrial factories around the Ulsan petrochemical industrial zone. These sites were divided into three sub-areas of pine forest to investigate the level of damage caused by T. japonensis (Fig. 1).

T. japonensis and pine needle measurements

Gall formation rates of T. japonensis were compared among sites to investigate the damage level to pine needles. Five trees were randomly selected from each sub-area, for a total of 15 trees per site. In addition, between 2015 and 2016, the sites were classified into up and down, and two new trees were randomly collected in four directions. The rate of gall formation was calculated from the total number of needles.

Two hundreds new needles in each site were randomly collected from pine trees with symptoms of T. japonensis damage in 2015 and 2016, and the length of the needles was measured using calipers. The size (i.e., body length and width) of 50 escaped larvae per site and the number of larvae inside 30 gall damaged needles per site were measured using a stereoscopic microscope.

Results and Discussion

Gall formation rates of T. japonensis

Site environmental included various chemical industries around Ulsan coastline. Although there were hills inland, pollutants emitted from high chimneys can be distributed broadly without barrier. Sea and land winds were interchanged during the day and night due to the sea, so the temperature range did not fluctuate compared to farther inland. The main winds blew in a southeastern direction, from the sea to inland, and therefore should have been affected directly by pollutants. The average diameter at breast height and height of the pine trees were 15-20 cm and 6-9 m, respectively, and the age of the pine trees was 25-35 years old. The gall formation rate of T. japonensis from this study indicated that gall formation rate in the area near the Onsan industrial complex was higher than in areas farther from the complex after 35 years of production (Table 1).

As shown in Table 1, gall formation rates of T. japonensis in Ulsan Chungryang, the site with lowest level of environmental pollution, was 10.95 and 9.94, respectively, for 2015 and 2016. These rates were lower than the gall formation rates of Ulsan Duckshin (46.42%, 47.94% for 2015 and 2016, respectively), Ulsan Haknam (37.77%, 32.96%), Ulsan Okdong (24.69%, 23.26%), and Ulsan Duwang (19.89%, 19.76%), in which air pollution caused by petrochemical industrial complex was higher. Gall formation rate of T. japonensis has been found to increase as the distance from pollutants decreases. Accordingly, these findings seem to be the result of stoma damage, destruction of the wax layer on pine needles, and soil acidification due to air pollution and acid rain caused by petrochemical industrial complexes (Seo et al., 1995; Bae et al., 1987; Han, 1984). Pine trees also are very sensitive to air pollution; high levels of pollution can cause physical deterioration of the soil, resulting in decreased tree health and reproduction (Park and Hyun, 1983). Therefore, as pine resistance to disease and insect pests decrease, T. japonensis outbreaks occur. In addition, damage caused by T. japonensis in sites with high levels of nitrogen and calcium (including areas surrounding industrial complexes, dump, and filled ground) has increased recently. Gall formation rates also have increased as a result of increased in habitat for T. japonensis caused by sulfur and nitrogen oxides, which are pollutants emitted from petrochemical industries.

Pine needle damage by T. japonensis by site

There were not large differences in the lengths of healthy needles and needles damaged by T. japonensis between early July, when galls started to form, and the middle of October, when imago growth of T. japonensis was completed (Table 2). Damaged needles do not grow once a gall is formed in the basal end of the needle (Ko, 1968). In the present study, accordingly, new plant part with damaged symptom on pine tree for the last two years have been collected and the lengths of healthy and damaged leaves have been measured. The results indicated that the average lengths of damaged and healthy needles at Ulsan Duckshin were 4.5 cm (49.9%) and 9.2 cm, respectively. Furthermore, the average lengths of damaged and healthy needles of Ulsan Chungryang, the site farthest from the industrial complex, were 4.9 cm (47.6%) and 10.5 cm, respectively, indicating differences between the sites nearest and farthest from the industrial complex. A previous report did not find distinct differences in the lengths of damaged or healthy leaves according to distance from the industrial complex (Hwang and Yim, 1990). However, this study found a 0.9 time difference in the lengths of damaged needles according to the distance from the source of environmental pollution. This difference in damaged needle lengths may have occurred as a result of the deterioration of pine trees caused by T. japonensis damage (Table 2).

Number of larvae inside gall damaged pine needles

The average number of larvae in damaged pine needles was 3.4 per gall in Ulsan Duckshin and 2.4 in Ulsan Chungryang (Table 3), thus the number of larvae per gall in damaged needles of T. japonensis within the site close to industrial complex was 0.7 times higher than the site farthest from the complex. This result indicates that the needles of pine forest, of which resistance is very low due to environmental pollution caused by industrial complex, seems to be a good habitat for larvae of T. japonensis. Furthermore, this result is very similar to previous studies that found higher densities of T. japonensis in pine forests where environmental pollution had increased (Ferrell, 1980; Kim et al., 1985) (Table 3).

Size of mature larvae within gall damaged pine needles

Under laboratory conditions, larvae inside gall-damaged needles were induced to leave the galls, and the size of mature larvae was calculated by site. Under laboratory conditions, larvae inside gall-damaged needles were induced to leave the galls, and the size of 50 mature larvae was calculated by site using a stereoscopic microscope (Table 4). Comparison of larval sizes between the site near the industrial complex and the site farthest from the complex (Table 4) indicated that body length and width were 2.40-2.55 mm and 0.70-0.72 mm, respectively, and there were no differences in fullgrown larval sizes between different sites (Table 4).