Appl. Entomol. Zool. 40 (1): 13–29 (2005) http://odokon.ac.affrc.go.jp/ Review

Insect semiochemical research in Korea: Overview and prospects

Kyung Saeng BOO1,* and Kye Chung PARK2 1 School of Agricultural Biotechnology, Seoul National University; Seoul 151–742, Korea 2 Department of Entomology, Penn State University; 104 PRL, University Park, PA 16802, U.S.A. (Received 5 April 2004; Accepted 23 June 2004)

Abstract Rapid progress has been made in research on pheromones and other semiochemicals in Korea during the last two decades. Sex pheromone compositions have been identified in several major orchard and other horticultural pest species and some other species in Korea, such as Helicoverpa assulta, Grapholita molesta, Carposina sasakii, Adoxophyes orana, prunifoliella, Phyllonorycter ringoniella, Dichocrocis punctiferalis, Ostrinia furnacalis and Peridroma saucia. Some of these identified sex pheromones have already been successfully incorporated into IPM systems, and are now being used as direct and indirect pest control means in Korea. Korean populations of many of these species showed significant differences in pheromone compositions from those reported in the neighboring coun- tries of Japan and China, suggesting that such interpopulational pheromone polymorphism is more common across the insect world than previously thought. Sex pheromone compositions were also identified in some aphid species in Korea such as Aphis spiraecola and Tuberocephalus momonis, and it was soon found that the aphid sex pheromone components were highly attractive to their predator lacewings. The presence of kairomones responsible for attracting egg parasitoids was shown in a pheromone component, hot pepper odor and male scale factor for H. assulta, and in male accessory glands for Lymantria dispar. Studies on the regulation of pheromone biosynthesis and release were carried out simultaneously in some species in Korea, resulting in the characterization of PBAN (pheromone biosyn- thesis activating neuropeptide) in H. assulta and Adoxophyes sp. A semiochemical research system has been firmly es- tablished in Korea through these studies. In some areas, successful monitoring and mating disruption technology have been effectively transferred from researchers to the end users in Korea, which will soon be expanded to wider areas. Continuous attempts to identify and use semiochemicals as well as wider applications of semiochemicals in pest con- trol are expected in Korea in the coming years. Since Korean research on semiochemicals does not cover vast areas due to limited resources, focused research and practical application will be needed for selected target insect species.

Key words: Korea; mating disruption; monitoring; pheromone; semiochemical

In Korea, most progress in insect pheromone INTRODUCTION and other semiochemical research has been made Olfactory communication of has been a during the last two decades (Fig. 1). Although there major focus in countless studies for the past 45 had been a number of behavioral and chemo-eco- years since the identification of bombykol in 1959 logical studies on insects in Korea (Lee et al., (Butenandt et al., 1959), a landmark event in in- 1980; Goh et al., 1981; Goh and Lee, 1984), semio- sect-related biology in the 20th century (Chapman, chemicals had not been the major interest of re- 2000). During this period, pheromones and other searchers in Korea until the early 1990s when an semiochemicals have been identified in a number attempt to identify sex pheromone components of insect species. Many of the semiochemicals are in the oriental tobacco budworm, Helicoverpa as- now practically being used as direct and indirect sulta, was initiated. There were some sporadic means for pest control in many countries, and their semiochemical-related studies in Korea before this use and application are expected to grow more rap- period. However, most of these studies were simple idly and widely in the coming years (Jones, 2002). field tests with existing products or readily avail-

* To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2005.13

13 14 K. S. BOO and K. C. PARK

prospects.

IDENTIFICATION OF PHEROMONES AND OTHER SEMIOCHEMICALS Once the involvement of sex pheromone is ob- served, chemical identification is perhaps one of the most demanding next steps, which can then lead to various studies and applications using the identified compounds. It is important to identify Fig. 1. Research activities of semiochemical-related stud- sex pheromone composition for insect populations ies in Korea as shown in the number of references over a 5- in specific regions even for those whose sex year period. Open bars indicate the number of references on pheromone compositions have already been re- chemical synthesis of pheromone and other semiochemical compounds. References include peer-reviewed journals, inter- ported in other regions, as well as yet unknown national symposium proceedings and doctoral dissertations. compositions, because geographical and interpopu- lational differences in sex pheromone compositions able compositions, and follow-up studies have not are not uncommon. Hence, most insect sex been carried out in most cases. Since the success of pheromone research in Korea during the last two a wide range of systematic studies on sex decades has been accompanied by chemical identi- pheromone biology of H. assulta during the fol- fications and field trapping tests (Table 1) to eluci- lowing years, a number of sex pheromone compo- date optimal compositions for Korean populations nents and some other semiochemicals have been even though sex pheromone compositions had been identified in major moth pests, aphids, beneficial reported in other countries. Indeed, these studies insects and some other insect species in Korea, indicated that there were significant differences in leaving us with many solutions as well as many pheromone compositions between populations of questions. Valuable semiochemical-related scien- the same species in Korea and other countries in tific information has accumulated during this pe- many cases. Since the first successful chemical riod, and some has already been successfully incor- identification of sex pheromone composition in porated into IPM in Korea. A robust insect Korea was achieved with H. assulta in the early pheromone research system constructed during this 1990s, pheromone (Table 2) and other semiochem- period will be the major foundation and driving ical (Table 3) compositions have been identified in force for the next generation of semiochemical re- major pest and beneficial insect species. Prior to search in Korea. this period, there was a report in Korea on the iden- While IPM was one of the main issues and prob- tification of sex pheromone composition in the fall lems with broad-spectrum pesticides were a public webworm, Hyphantria cunea (Lee et al., 1978). concern, semiochemicals were actively and suc- However, the identification was not supported by cessfully introduced for pest management in some any other studies and appeared to be incorrect (Hill major crops in and North America. In par- et al., 1982; Zhang et al., 1996). ticular, orchards in European countries had already taken advantage of using sex pheromone as moni- The oriental tobacco budworm toring and mating disruption means. Fruit produc- The first systematic approach of insect tion is one of the major compatible agricultural pheromone research in Korea was focused on the areas in Korea. Encouraged by fruitful pheromone oriental tobacco budworm, Helicoverpa assulta studies, fruit growers in Korea have started accept- (previously known as Heliothis assulta), which was ing the environmental-friendly pest management a serious pest for hot pepper and tobacco plants in technology and now, use of broad-spectrum pesti- Korea. Hot pepper is one of the major horticultural cide is decreasing in some Korean orchards. In this crops in Korea. Mating behavior of H. assulta sug- review, we are going to look back and summarize gested the presence of female sex pheromone (Kim insect pheromone and other semiochemical re- and Boo, 1986), dial activity indicated the peak search in Korea, and project future directions and mating activity at the early scotophase (Cho and Insect Semiochemical Research in Korea 15

Table1. Number of publications in insect pheromone and other semiochemical-related research areas

Number of publicationsa Research area 1974–1983 1984–1993 1994–2003

Chemical identification 1 3 23 Field bioassay (including monitoring) 3 2 32 Wind-tunnel bioassay 0 1 4 Other behavioral study 2 11 10 Sensory physiology (including EAG and SCR) 0 1 12 Microscopy 0 4 4 Biosynthesis, release and regulation, PBAN 1 2 10 Chemical synthesis 1 21 1 Direct control (mass trapping, mating disruption) 0 0 10 Others 0 4 8 Total 8 49 114

a References include peer-reviewed journals, international symposium proceedings and doctoral dissertations. Some references are included in two or more corresponding areas. The actual total numbers of references, considering the overlapping multiple counting of some publications in different areas, are 5, 39 and 68 for 1974–1983, 1984–1993 and 1994–2003, respectively (see Fig. 1).

Boo, 1988), and histological observation showed (Z)-11-hexadecenyl acetate (Z11-16:Ac), one of the location of a sex pheromone gland at the 8–9th the sex pheromone components in a Korean popu- abdominal segments (Moon et al., 1986), which lation of H. assulta (Boo and Yang, 2000), leaving were in close agreement with those reported us the question whether the acetate plays the same for other Heliothis/Helicoverpa and other moth role in Japan, China and Thailand because this species. Shortly after, chemical identification was compound is not present or is behaviorally inactive accomplished in collaboration with British scien- in H. assulta in these countries. In a Korean popu- tists (Cork et al., 1992), and the results were pub- lation, the ratios of the two acetate isomers, Z9- lished a year after a Japanese group reported sex 16:Ac and Z11-16:Ac, to the corresponding alde- pheromone composition of H. assulta in Japan hyde isomers gradually changed in female H. as- (Sugie et al., 1991). Interestingly, the most abun- sulta during the scotophase (Park et al., 1996). But, dant sex pheromone component of H. assulta was a small-scale field experiment showed that effective (Z)-9-hexadecenal (Z9-16:Ald), which was exactly mating disruption for H. assulta could be achieved the opposite from other known Heliothis and Heli- in a Korean hot pepper field with the Korean coverpa species whose major pheromone compo- pheromone composition (Park et al., 1999). nent was (Z)-11-hexadecenal (Z11-16:Ald). Electrophysiological studies (Berg and The chemical identification also showed a no- Mustaparta, 1995) were also carried out along with table difference in the pheromone composition be- ultrastructural observations (Koh et al., 1995) on tween Korean and Japanese populations of the antennal sensilla, providing some new information moth, especially in the composition of acetate iso- on pheromone biology in H. assulta. Male H. as- mers. The geographical variation in the behav- sulta appeared to have a sensilla population re- iorally active pheromone composition was further sponding to a component, (Z)-9-tetradecenal (Z9- confirmed by subsequent wind tunnel and field 14:Ald), which was a non-pheromonal component trapping studies, firmly indicating the presence of in H. assulta but a sex pheromone component in geographic differences in pheromone phenology several other heliothine . A subsequent field among Korean, Japanese, Chinese and Thailand test showed that Z9-14:Ald was a potent inhibitor populations, and confirming again that the corre- of pheromone-mediated communication in H. as- sponding acetate isomers were mainly responsible sulta (Boo et al., 1995), which was similar to the for the differences. It was then found that an egg strong inhibitory effect of another compound, (Z)- parasitoid Trichogramma chilonis was attracted to 11-hexadecenol (Z11-16:OH), against pheromone 16 K. S. BOO and K. C. PARK

Table2. Identification of insect pheromone components in Korea

Species Composition Optimum blenda Reference

Adoxophyes spp. Z11-14:Ac 100 : 5–11 Han et al., 2001b Z9-14:Ac Boo, 1998 14:Ac Z9-16:Ac Adoxophyes orana Z11-14:Ac 95 : 5 : 0 : 0 (apple) Han & Boo, 2002 Z9-14:Ac 63 : 37 : 2 : 31 (tea) 10M-12:Ac E11-14:Ac Aphis spiraecola ()-(4aS,7S,7aR)-Nepetalactone 2 : 1 Hong et al., 2003 ()-(1R,4aS,7S,7aR)-Nepetalactol Archippus breviplianus E11-14:Ac 7 : 3 Jung et al., 2001 Z11-14:Ac Carposina sasakii (Z)-7-Eicosen-11-one singly Boo, 1996 Lee et al., 2002 Dichocrosis punctiferalis E10-16:Ald 70 : 30–80 : 20 Jung et al., 2000b Z10-16:Ald Grapholita molesta Z8-12:Ac 95 : 5 : 1 or 93 : 6 : 1 Boo, 1996 E8-12:Ac Lee et al., 2002 Z8-12:OH Yang et al., 2002b Helicoverpa assulta Z9-16:Ald Cork et al., 1992 Z11-16:Ald Z9-16:Ac Z11-16:Ac Lyonetia prunifoliella 10S,14S-Dimethyloctadece-1-ene singly Park et al., 2002a Matsucoccus thunbergianae (2E,4E,6R,10R)-4,6,10,12- singly Park et al., 1994b Tetramethyl-2,4-tridecadien-7-one Ostrinia furnacalis E12-14:Ac 1 : 2 (corn field) Boo & Park, 1998 Z12-14:Ac 5 : 1 (ginger field) Peridroma saucia Z9-14:Ac 8 : 2 Kim et al., 2002 Z11-16:Ac Phyllonorycter ringoniella Z10-14:Ac 4 : 6 Jung & Boo, 1997 E,Z4,10-14:Ac Boo & Jung, 1998 Spodoptera exigua Z,E9,12-14:Ac 7 : 3 Jung et al., 2003 Z9-14:OH Tuberocephalus momonis (4aS,7S,7aR)-Nepetalactone 85 : 15 Boo et al., 2000 (1R,4aS,7S,7aR)-Nepetalactol

a Optimum blend for field attraction in Korea.

Table3. Identification of non-pheromonal semiochemical components in Korea

Species Composition Activity Reference

Aedes aegypti ()-Fenchone repellent Ahn et al., 2002b (E)-9-Octadecenoic acid Agelastica coerulea Leaf extract of Alnus glutinosa attractant Jung et al., 2000a Chrysopa cognata Nepetalactol attractant Boo et al., 1998 Chrysopa cognata (1R,4S,4aR,7S,7aR)-Dihydronepetalactol attractant Hooper et al., 2002 Helicoverpa assulta Z9-14:Ald inhibition Boo et al., 1995 Ooencyrtus kuvanae Accessory gland secretion of attractant Lee et al., 1997 Lymantria dispar, host egg mass extract Trichogramma chilonis Green fruit and leaf of hot pepper plant attractant Boo & Yang, 1998 Trichogramma chilonis Z11-16:Ac, E12-14:Ac attractant Boo & Yang, 2000 Insect Semiochemical Research in Korea 17 communication in this species (Cork et al., 1992; tive composition for male attraction in G. molesta Park et al., 1994a). Leaf extracts of Capsicum was a 93 : 6 : 1 blend (Yang et al., 2002b) or a annum, a major host-plant, evoked significant elec- 95 : 5 : 1 blend (Han et al., 2001a) of these com- troantennogram (EAG) responses in female H. as- pounds, respectively. Dodecanol (12:OH) showed sulta, which could be related to the observation no significant behavioral activities (Han et al., that females showed more actively calling behavior 2001a). Geographical variation in pheromone com- and produced a larger amount of sex pheromone in position was also found in this species both in the presence of the host-plant (Boo and Ahn, chemical analysis and in field tests, which showed 2001). a major difference in the contents of two alcohols, Z8-12:OH and 12:OH. The relatively low contents Orchard pests of these two alcohols in the Suwon population in The next target moth species for our semiochem- Korea also suggested a minor behavioral role of ical research in Korea were orchard pests. Three these alcohols (Han et al., 2001a). In contrast, the major factors were involved in the target selection Naju population in southern Korea showed much process: 1) potentially highly competitive fruit higher alcohol contents than the Suwon population, crops, 2) growing broad-spectrum pesticide prob- indicating that the Naju population is similar to lem and consumer concerns, and 3) particular diffi- that in the US population (Yang et al., 2002b). culties in traditional pesticide application against However, it is yet unclear if the difference between several major orchard pests. Relatively high suc- the two Korean populations was either entirely due cess in practical application of semiochemicals for to geographical isolations or whether host plant orchard pest management in other countries per- differences are involved. Despite the differences in haps also encouraged the decision. Thus, major fo- the alcohol contents in the gland extracts between cuses were subsequently given to several most eco- the two populations, blend ratios for the best attrac- nomically important and destructive moth pests in tion at the corresponding orchards were not differ- apple, pear and orchards in Korea that were ent from each other (Han et al., 2001a; Yang et al., suffering from vicious cycles mainly due to indis- 2002b). In addition, none of the other four criminate use of broad-spectrum pesticides over a Grapholita species (G. delineama, G. dimorpha, G. long period of time. Mostly through cooperative endrosias, and G. scintillana) known to be present studies between Seoul National University and in Korea were captured in pheromone-baited traps Korean governmental research institutions, sex with various blends containing these compounds, pheromone compositions in Korean populations although many Grapholita species seem to use Z8- were identified in the oriental fruit moth 12:Ac and E8-12:Ac as major sex pheromone com- (Grapholita molesta), the peach fruit moth (Car- ponents (Han et al., 2001a). Similarly, two com- posina sasakii), the summer fruit tortrix (Adoxo- pounds, (Z)-7-eicosen-11-one and (Z)-7-nonade- phyes orana), the smaller tea tortrix (Adoxophyes cen-11-one, were identified in the abdominal tip sp.), the apple leafminer (Lyonetia prunifoliella), extract of female of the peach fruit moth C. sasakii the apple leafminer moth (Phyllonorycter ringo- in Korea, but only a lure containing (Z)-7-eicosen- niella), and the peach pyralid moth (Dichocrocis 11-one was highly attractive to conspecific males punctiferalis) (Table 2), and population monitoring (Boo, 1996; Han et al., 2001a). and mating disruption trials were followed for Pheromone polymorphism within Korea was some of these species. more apparent in Adoxophyes orana. Sex pher- The oriental fruit moth, G. molesta, is a cosmo- omone composition suggested the presence of two politan pest. Among four compounds, (Z)-8-dode- distinct populations (‘apple type’ and ‘tea type’) of cenyl acetate (Z8-12:Ac), (E)-8-dodecenyl acetate A. orana in Korea, as reported in Japan (Sugie et (E8-12:Ac), (Z)-8-dodecenol (Z8-12:OH) and do- al., 1984). The apple type prefers apple, peach and decanol (12:OH), identified in the abdominal tip pear trees, while the tea type prefers tea and pear extracts from virgin females of G. molesta, only trees (Han and Boo, 2002). The apple type was at- three compounds, Z8-12:Ac, E8-12:Ac and Z8- tracted best to a 95 : 5 ratio of a binary blend be- 12:OH, appeared to be behaviorally active (Han et tween (Z)-11-tetradecenyl acetate (Z11-14:Ac) and al., 2001a). Field tests showed that the most effec- (Z)-9-tetradecenyl acetate (Z9-14:Ac), while the tea 18 K. S. BOO and K. C. PARK type was most attracted to a 63 : 37 : 2 : 31 ratio of E11-14:Ac and Z11-14:Ac (Jung et al., 2001). blend of Z11-14:Ac, Z9-14:Ac, 10-methyl-dodecyl Population monitoring with pheromone traps indi- acetate (10M-12:Ac) and (E)-11-tetradecenyl ac- cated the presence of three field generations of A. etate (E11-14:Ac), respectively (Han and Boo, breviplicanus (Jung et al., 2001). 2002). The diel rhythms of activities in mating and Attractive sex pheromone composition in a Ko- male response to pheromone trap were also differ- rean population of the apple leafminer (L. pruni- ent between the two types, with most A. orana foliella) was different from that of an American apple type mating before lights-on but A. orana tea population (Park et al., 2002a). In contrast to a type immediately after lights-on. Concentrations of combination of three compounds fully attractive in sex pheromone in each type peaked during the re- American population (Gries et al., 1997), only one spective mating period (Han and Boo, 2002). In compound, 10,14-dimethyloctadec-1-ene, was at- mating choice experiments in the laboratory, males tractive to Korean population (Park et al., 2002a). of each type showed mate preferences to females The two minor components reported in the Ameri- of the same type, although mating between males can population were not detected in the Korean of A. orana tea type and females of A. orana apple population (Park et al., 2002a). Moreover, the Ko- type took place. In addition to the differences in rean population showed high stereo-specificity in sex pheromone composition, apparent differences field trapping experiments, in which only the in esterase isozyme pattern and mitochondrial 10S,14S-form was attractive and three other DNA sequences between the two types were also stereoisomers were neither attractive nor inhibitory observed, indicating that the isolation of these two (Park et al., 2002a). Antennal receptors of male L. types seems to be almost normal in nature (Han prunifoliella were also sensitive only to the behav- and Boo, 2002). Taken together, all these evidences iorally active 10S,14S-isomer (Park et al., 2002a). lead us to a speculation that these two types of A. The clear difference between Korean and American orana in Korea are in the process of being sexually populations may indicate the presence of two sepa- isolated as a process of eventual speciation (Han rate sub-species (Park et al., 2002a). As the Japan- and Boo, 2002), as documented in Japan (Sugie et ese population was assigned as a sub-species, L. al., 1984). But their sex pheromone compositions prunifoliella malinella (Sekita and Yamada, 1979), differ greatly from the situation in Japan. it is interesting to see active pheromone composi- Three compounds, E11-14:Ac, Z11-14:Ac and tion in Japanese subspecies population, which tetradecanyl acetate (14:Ac), at a ratio of might be close to that of the Korean population. 55 : 22 : 22, respectively, were identified in the ab- After showing an indication of the presence of dominal tip extracts of female Asiatic leafroller, female sex pheromone by behavioral (Jung and Archippus breviplicanus, which is one of two major Boo, 1997) and histological observations, female leafroller pests on apple leaves in Korea together gland extract of another leafminer P. ringoniella in with A. orana (Jung et al., 2001). Although the Korea showed the presence of two compounds, (Z)- pheromone composition in the gland was some- 10-tetradecenyl acetate (Z10-14:Ac) and (E,Z)- what different from that reported in the Japanese 4,10-tetradecadienyl acetate (E,Z4,10-14:Ac) (Jung population (Sugie et al., 1977), the optimal compo- and Boo, 1997). Subsequent wind-tunnel bioassay, sition for conspecific male attraction in the field net-house trapping and field trapping experiments was similar to that in Japan (Sugie et al., 1977), indicated that a mixture of these two compounds at showing the highest attractiveness of a binary mix- a ratio of 4 : 6 was the most attractive to conspe- ture of E11-14:Ac and Z11-14:Ac at 7 : 3 ratio cific males (Boo and Jung, 1998). This optimal at- (Jung et al., 2001). The third component identified tractive blend composition was also different from in the gland, 14:Ac, did not have any significant ef- that in Japan (10 : 3) (Oku, 1993) and China (7 : 3 fect on the attractiveness of the binary blend (Jung to 6 : 4) (Su and Liu, 1992). et al., 2001). In addition to this species, several Three compounds, (E)-10-hexadecenal (E10- other leafrollers such as Choristoneura longicel- 16:Ald), (Z)-10-hexadecenal (Z10-16:Ald) and lana, Archips subrufanus, Rhopobota naebana and hexadecanal (16:Ald), were also identified in the Archips oporanus were also captured in the female gland extract of the peach pyralid moth (D. pheromone traps baited with various binary blends punctiferalis) (Jung et al., 2000b). Among various Insect Semiochemical Research in Korea 19

Table4. Species showing inter-populational and geographical differences in sex pheromone composition either between Korea and other countries or within Korea

Species Major finding Reference

Adoxophyes orana Geographical variation (China, Japan, Korea, Han & Boo, 2002 Okinawa, and Taiwan), Presence of two distinct populations in Korea Carposina sasakii Geographical variation (Japan and Korea) Boo, 1998 Dichocrocis punctiferalis Geographical variation (China, Japan, and Korea) Boo, 1996, 1998 Grapholita molesta Geographical variation (Australia, France, Korea, Boo, 1996, 1998 and U.S.A.) Han et al., 2001a Helicoverpa assulta Geographical variation (China, Japan, Korea, and Cork et al., 1992 Thailand) Sugie et al., 1991 Helicoverpa assulta Intrapopulational variation during scotophase Park et al., 1996 Lyonetia prunifoliella Different attraction (Korea and U.S.A.) Park et al., 2002a Ostrinia furnacalis Geographical variation (China, Japan, Korea, Boo & Park, 1998 Philippines, and Taiwan) Boo, 1998 Peridroma saucia Geographical variation (Canada and Korea) Kim et al., 2002 Struble et al., 1976 Phyllonorycter ringoniella Geographical variation (China, Japan, and Korea) Boo & Jung, 1998 combinations of these compounds, binary blends ances of multiple pheromone deployments with of E10-16:Ald and Z10-16:Ald at a ratio of different blends for several different target species 70 : 30–80 : 20 were the most attractive to the males at the same time to have a firmer foundation for in wind tunnel experiments and field trapping ex- successful practical use of pheromone where multi- periments in orchards (Jung et al., 2000b). Another ple pest species are concerned. compound, 16:Ald identified in the gland extract, Apparently, variation in sex pheromone compo- was not EAG-active, but the behavioral signifi- sitions appears to be far more widespread than pre- cance of this compound still remains in question, viously thought. Several species showed that sex while the component was reported as behaviorally pheromone composition in the gland and optimum active in China (Liu et al., 1994). blend ratio for field attraction in Korea were differ- All the moth species studied here use 12–16 car- ent from other populations in different countries bon aliphatic compounds with at least one double (Table 4). Several species such as H. assulta, O. bond as active sex pheromone components (Table furnacalis and D. punctiferalis showed intermedi- 2). The corresponding saturated compounds usu- ate composition in a Korean population compared ally do not have any significant behavioral activi- to Chinese and Japanese populations, and some ties even though they are present in the pheromone other species such as Adoxophyes and P. ringo- gland. Although we do not currently know the niella showed a totally different response from this exact transduction mechanism in pheromone sensi- trend. For other species, a complete data set is still tive neurons of the moths studied here, it is sug- needed to make comparisons among these regions. gested that the presence of a double bond in the aliphatic compounds plays an important role in the Aphids and beneficial insects transduction process. There are also many overlap- While we were conducting a collaborational ping pheromone components across different study on aphid sex pheromones with British scien- species. In practice, there is often more than one tists, we found that a number of aphids were cap- pest species in the same area where the use of sex tured in sex-pheromone baited traps in the field in pheromone is planned for monitoring and mat- Korea, which became one of our major focuses in ing disruption. Therefore, the often-overlapping semiochemical research for the following years. pheromone components across different, co-exist- During this period we identified sex pheromone ing species should be incorporated into the blend compositions in some Korean aphid species (Table composition. It may be critical to evaluate perform- 2) and also found that some aphid species had been 20 K. S. BOO and K. C. PARK taxonomically misidentified. For the first time, we ically important chrysopid which feeds on aphids then discovered that the sex pheromone compo- both as adults and larvae (Boo et al., 2002), in con- nents of aphids attracted their predator lacewings trast to Chrysoperla carnea which feeds only at the (Boo et al., 1998). In order to work on sex larval stage. Field trapping studies indicated that C. pheromone in host-alternating aphids, rearing tech- cognata was preferably attracted to an aphid sex nique had also to be established to produce sexual pheromone component, nepetalactol (Boo et al., forms during this period (Hong and Boo, 1998). 1998, 2002, 2003). It was also the first evidence for Sex pheromone of the peach aphid, Tubero- the employment of an aphid sex pheromone as a cephalus momonis, was identified as a mixture of kairomone by an aphid predator (Boo et al., 1998). two ubiquitous aphid sex pheromone compounds, Adults of C. cognata caught in aphid-pheromone (4aS,7S,7aR)-nepetalactone and (4aS,7S,7aR)- baited traps in the field were predominantly males, nepetalactol, in a ratio of 4 : 1, and subsequent field in agreement with EAG results which showed that tests showed that the most effective sex pheromone only male adults responded to the aphid sex blend for trapping males was 85 : 15 of nepetalac- pheromones (Boo et al., 1998, 2002, 2003). tone and nepetalactol (Boo et al., 2000). It was un- In subsequent studies through a systematic ap- expected that a large number of presexual females proach it has been suggested that nepetalactol is (gynoparae) of this species were also collected in working as a feeding attractant and feeding stimu- the pheromone-baited traps (Boo et al., 2000). lant to C. cognata males, but not to females (Boo Over 20 other species of aphids were also captured et al., 2002, 2003). In addition to C. cognata, a few in the pheromone-baited traps, indicating once male adults of Chrysopa formosa and Chrysopa again the ubiquitous nature of aphid sex phyllochroma were also captured in pheromone pheromones. Oviparae of another host-alternating traps in the field (Boo et al., 2002, 2003). A similar aphid, Aphis spiraecola, artificially induced on the compound, (1R,4S,4aR,7S,7aR)-dihydronepetalac- dropwort, Oenathe javanica, showed a typical be- tol, also attracted C. cognata in Korea (Hooper et havior of sex pheromone release during the pho- al., 2002). The lacewings trapped were also pre- tophase (Hong et al., 2003). Two pheromone com- dominantly males, implying a possible pheromonal ponents, ()-(4aS,7S,7aR)-nepetalactone and ()- role for these or structurally related compounds (1R,4aS,7S,7aR)-nepetalactol, were then identified (Hooper et al., 2002). A preliminary EAG study in the volatile collection of the calling oviparae showed that female adults responded to male ex- at a ratio of 6 : 1–8 : 1 (Hong et al., 2003). Wild tract (Boo et al., 2002), indicating that a semio- oviparae of the same species collected in the field chemical may be involved in this sexual dimor- had a somewhat different pheromone composition, phism. However, no semiochemical involved in this showing a ratio of around 2 : 1 for the two com- process has yet been chemically identified.2 It is in- pounds (Hong et al., 2003). Oviparae of these teresting that all three species, C. cognata, C. for- aphids showed a circadian rhythm in sex mosa and C. phyllochroma, were preferably at- pheromone production, producing sex pheromone tracted to nepetalactol, but not to nepetalactone. during the photophase (Hong et al., 2003). In a The hypothesis that the lacewing uses aphid sex separate study on the relationship between host- pheromone to locate aphid prey has not been plant preference and DNA polymorphism in proved (Boo et al., 2003). The nocturnal rhythm of aphids, eight different clones of the green peach C. cognata responding to aphid sex pheromone aphid, Myzus persicae, did not show any relation- chemicals does not coincide with the diurnal re- ship between RAPD polymorphism and host pref- lease rhythm of aphid sex pheromone (Boo et al., erence (Kim et al., 1996). 2003). It was suggested that aphid pheromone can Chrysopids are good candidates for biological stay on the leaf surfaces and exert its effects hours control as aphid predators. In Korea, Chrysopa later. However, there is no supporting evidence for cognata1 (Neuroptera: Chrysopidae) is an econom- this suggestion and, in fact, the much higher

1 Classification of this lacewing is controversial now. Chrysopa cognata is recognized as a proper species name by a Russian taxonomist (Makarkin, 1990), but this name must be C. septempunctata according to a US taxonomist (M. J. Tauber, personal communication). 2 Recently Chrysopa oculata was claimed to produce male-aggregation pheromone, (1R,2S,5R,8R-iridodial), by male pheromone (R. Aldrich et al., personal communication). Insect Semiochemical Research in Korea 21 volatility of aphid sex pheromones compared to process between parasitoids and their hosts. It was moth pheromones greatly reduces the likelihood suggested that olfactory signals (kairomones) from that they will stay on the leaves for such a long scale and egg chemicals (Boo and Yang, unpub- time. The contribution of aphid sex pheromone in lished observation) might be the first step for T. locating aphids by lacewings would be small com- chilonis to locate its host (Boo and Yang, 1998). pared to the entire food need and aphid consump- tion. The main aphid prey would be non-sex Other insects pheromone producing aphids. Sex pheromones have also been identified in Kairomones responsible for host location of an some other insect species in Korea (Table 2). Fe- egg parasitoid Trichogramma chilonis on its host male abdominal tips of the oriental corn borer H. assulta were identified (Table 3). T. chilonis was moth (O. furnacalis) in Korea contained three attracted to Z11-16:Ac, a sex pheromone compo- major compounds identified as 14:Ac, E12-14:Ac nent of H. assulta, and to (E)-12-tetradecenyl ac- and (Z)-12-tetradecenyl acetate (Z12-14:Ac) (Boo etate (E12-14:Ac), a sex pheromone component of and Park, 1998). In corn fields, a 1 : 2 mixture of another moth species, the oriental corn borer (Os- E12-14:Ac and Z12-14:Ac was the most attractive trinia furnacalis) (Boo and Yang, 2000). The para- blend to conspecific males, but in a ginger field the sitoid was more attracted to the hot pepper than to most attractive blend was 5 : 1 (Boo and Park, other plants such as tobacco, eggplants and carrots 1998). In O. furnacalis, the most active calling be- (Boo and Yang, 1998). The attraction of hot pepper havior was observed for 2 h from the 5th to 7th plants was greater with both leaves and green fruits hour during the scotophase among 2- and 3-d-old rather than plants with only leaves or fruits, and females (Park and Boo, 1993, 1994), which coin- plants with red fruits were the least attractive to cided with female sex pheromone titers first de- the parasitoid (Boo and Yang, 1998). However, tected at 2 h into the scotophase (16L:8D) and the combination of hot pepper odor and sex gradually increased to reach the maximum level at pheromone of H. assulta did not enhance attrac- the end of the scotophase (Boo and Park, 1998). tiveness compared with the pepper odor or sex The response of 3-d-old males to 3-d-old females pheromone alone (Boo and Yang, 1998). Eggs of was higher than that to any other age of females H. assulta were even more parasitized by T. chilo- during the 5th–8th hour of the scotophase (Park nis when the eggs were treated with male moth and Boo, 1994). scale extract of H. assulta (Boo and Yang, 2000). Female sex pheromone components of a Korean These experiments suggested that some sex population of the variegated cutworm, Peridroma pheromone components and hot pepper odor are saucia, which was first found in Korea in 1996 and attractive to the parasitoid T. chilonis, and male subsequently became a quarantine pest insect, were scale factor has another factor attracting the para- identified as Z9-14:Ac and Z11-16:Ac (Kim et al., sitoid, but interactions of these compounds were 2002), and field trapping studies showed that the not clear. Another egg parasitoid, Ooencyrtus ku- optimum blend ratio for male attraction was 8 : 2 vanae, showed the greatest attractiveness, a rela- between these two components. Monitoring field tively longer examining period, and a shorter prob- populations using this blend showed the occurrence ing duration to the adhesive materials secreted of a different number of generations in different re- from reproductive accessory glands of the host, the gions of Korea, from two generations per year in gypsy moth (Lymantria dispar) (Lee et al., 1997). Milyang to five generations per year in Jeju island Among different extractions of host egg mass (Kim et al., 2002). In P. saucia, the density of the using six different organic solvents, n-hexane ex- adult population was observed to become the high- tract elicited the highest responses from the egg est in the first generation (May–June) of the year parasitoid, and the parasitoid reared in vivo was (Kim et al., 2002). more attracted to hexane extract than that reared in Three components, (Z,E)-9,12-tetradecadienyl vitro (Lee et al., 1997). The presence in the acces- acetate (Z,E9,12-14:Ac), (Z)-9-tetradecenol (Z9- sory gland of male moths of compounds attractive 14:OH) and Z9-14:Ac, were identified in the fe- to their parasitoids is perhaps more wide spread, male gland extract of the beet armyworm, being adapted through the long co-evolutionary Spodoptera exigua in Korea (Jung et al., 2003). 22 K. S. BOO and K. C. PARK

Field tests showed broad attraction of males to a Ahn et al. (2002b) identified two plant-derived wide range of binary blends of Z,E-9,12-14:Ac and compounds, ()-fenchone and (E)-9-octadecenoic Z9-14:OH in two different regions in Korea (Jung acid, as potential repellents for the mosquito Aedes et al., 2003). Among the blends, the 7 : 3 blend was aegypti. the most attractive (Jung et al., 2003), which is similar to that of a Japanese population (Mochizuki PHEROMONE BIOSYNTHESIS AND RE- et al., 1994). Only Z11-16:Ac showed a significant LEASE synergistic attractive effect to the binary blend among three minor sex pheromone components, Physiological aspects related to pheromone (Z)-9-hexadecenyl acetate (Z9-16:Ac), Z11-14:Ac biosynthesis and release were studied in most of and Z9-14:Ac, reported in local Korean popula- the species mentioned in the previous sections. tions (Jung et al., 2003). However, the presence in Most insect species studied showed distinct circa- the gland and the behavioral significance of Z11- dian rhythm in adult (sexual) behavior and 16:Ac in Asian countries including Korea is still pheromone secretion/biosynthesis. Usually, the uncertain (Jung et al., 2003). There were only maximum activity in pheromone secretion and sex- minor differences in the optimal ratio of these ual behavior does not initiate right after the start of compounds for field attraction among the popula- the scotophase. H. assulta mainly used palmitic tions in Japan (Wakamura, 1987), China (Dong et acid (16:Acid) as the substrate for their two major al., 1999), Taiwan (Cheng et al., 1985) and Korea and minor sex pheromone components (Z9-16:Ald (Jung et al., 2003). This species is a serious pest and Z11-16:Ald) with help of two desaturases, D 9 worldwide, and sex pheromone was used for moni- and D 11 desaturases (Choi et al., 2002). This was toring and mating disruption in some cases in different from Helicoverpa zea, which used Korea (Kim et al., 1995; Park and Kim, 1995; Yoo palmitic acid (16:Acid) for its major component of et al., 1995). Z11-16:Ald and stearic acid (18:Acid) for its minor Sex pheromone of the black pine bast scale, components of Z9-16:Ald and Z7-16:Ald. Matsucoccus thunbergianae, was identified, and More detailed studies regarding pheromone field-trapping experiments were carried out with a biosynthesis and release including activities of synthetic compound (Park et al., 1994b). Although PBAN (pheromone biosynthesis activating neu- the results were promising and use as a monitoring ropeptide) were also carried out in some species, means was suggested, there has been no record of such as H. assulta, Helicoverpa armigera, and using the pheromone for monitoring populations Adoxophyes sp. (Choi, 1999; Choi et al., 1998a, b, since then. The cigarette beetle, Lasioderma serri- 2004). More intensive studies on pheromone corne, a stored-product insect pest, was studied for biosynthesis were carried out in H. assulta with monitoring of its seasonal occurrence in tobacco characterization of its PBAN (Has-PBAN) cDNA storage warehouses in Korea, which showed that (Choi et al., 1998a). In this study, it was predicted the occurrence could be successfully monitored by that the cDNA has a PBAN domain with 33 amino using sex pheromone traps (Sone and Ohh, 2001). acids and four additional peptide domains: 24 Some plant-derived semiochemicals were also amino acid-, 7 amino acid-, 18 amino acid- and 8 investigated during this period. In an attempt to amino acid-long sequences, with FXPR(or K)L identify olfactory-active compounds for the alder (XG, T or S) amidated at their C-termini, sug- leaf beetle, Agelastica coerulea, in the Japanese gesting that H. assulta adult females use their own alder, Alnus glutinosa, which was attractive to this PBAN for regulating sex pheromone biosynthesis species, seven compounds were identified by using (Choi et al., 1998a). In H. assulta, it was also sug- GC-EAD: 3-cyclohexene-1-methanol, 2-cyclo- gested that 1) PBAN is released continuously into hexen-1-ol, 5-methyl-2-(1-methylethyl)-cyclohexa- the haemolymph to stimulate pheromone biosyn- nol, 5-alpha-androstan-17-beta-ol, 3-ethyl-3-hy- thesis at least during the first half of the sco- droxy-androstan-17-one, (Z)-2-(9-octadecenyloxy)- tophase, 2) PBAN is synthesized and accumulated ethanol and hexadecanoic acid (Jung et al., 2000a). independent of photoperiod or sex, and 3) the re- However, the behavioral significance of these com- lease starts just prior (about 1 h) to the beginning pounds is still unknown. In a more recent study, of the scotophase (Choi et al., 1998b). H. armigera Insect Semiochemical Research in Korea 23 had the same kind of PBAN as that of H. assulta a small-scale mating disruption trial were carried (Choi, 1999). But the primary structure of PBAN out in a hot pepper field in Korea to investigate the from Adoxophyes sp. had only 31 amino acids, two potential value of the synthetic sex pheromone of fewer than in most other insect species, and also re- the oriental tobacco budworm, H. assulta (Park et vealed quite a low homology of less than 50%, al., 1999). The pheromone trap was more effective when compared to that of Helicoverpa spp. (Choi in detecting the field population than the black- et al., 2004). Hez-PBAN (PBAN of Helicoverpa light trap, and a mating disruption trial with con- zea) activated female sex pheromone synthesis at trolled-release PVE resin dispensers loaded with 20 pmol level in Peridroma saucia (Kim et al., synthetic sex pheromone, applied at a rate of 30 2002). g/ha in the field, showed a significant reduction of Sex pheromone production of H. assulta was trap catches, indicating effective disruption of mostly terminated within 3 h after mating, and a pheromonal communication of H. assulta. The dis- low pheromone titer was maintained for 3 d until ruptive effect of the PVC formulation lasted for at resumption of pheromone production (Ahn et al., least 1 month in the field (Park et al., 1999). 2002a). The mating, however, did not inhibit Practical use of sex pheromone has been particu- PBAN biosynthesis and receptivity of the larly successful in apple and pear orchards in pheromone gland, but is responsible for blocking Korea. The lack of proper monitoring means for of PBAN release from the head. Hence, it was sug- the oriental fruit moth, G. molesta, demanded the gested that a humoral factor(s) produced in the development of a convenient monitoring system male reproductive gland is transferred to the fe- for this species (Han et al., 2001a). Field popula- male during copulation, and a chemical sub- tions of two fruit moth pest species, G. molesta and stance(s) in the humoral factor(s) from the male is C. sasakii, have been effectively and systematically responsible for the loss of biosynthesis in H. as- monitored through an internet-based monitoring sulta. system using sex pheromone traps, leading to an immediate reduction of pesticide use (Lee et al., 2002; Yang et al., 2002a). Field monitoring of G. PRACTICAL APPLICATION molesta indicated the presence of four distinct an- Korea is a peninsula nation in far-eastern Asia. nual generations. Now monitoring with pheromone The agricultural production areas of the country traps is an effective decision-making tool for apple cover a range of temperate latitudes. The range of growers with regard to pesticide spraying needs crops therefore represents a diversity of pest man- and timing (Lee et al., 2002). Evaluation of the agement problems. Specific control strategies mating disruption trials for G. molesta over three should be properly developed to fit conditions and consecutive years (1998–2000) indicated that mat- needs of the specific regional agricultural system in ing disruption was an effective direct control order for semiochemical use to be successful in means in a pear orchard (10% damage reduction managing insect pests. Korean agricultural systems with 50 g/ha or higher treatment) and effectiveness are characterized by a relatively small size, crop di- of disruption was enhanced through successive versity and often hilly and mountainous terrain. It suppression year after year at the same site (Yang also became apparent that it is particularly impor- et al., 2003). However, the efficacy of pheromone tant to identify the appropriate regional pheromone treatment could not be predicted using the capture compositions since the pheromone polymorphism of males in synthetic-pheromone baited traps among different populations occurs widely, as (Yang et al., 2003). A relatively lower mating dis- shown in a number of lepidopteran species (Guerin ruption efficacy of edge area in uniformly et al., 1984; Bailey et al., 1986; Cork et al., 1992; pheromone-treated orchard could be significantly Boo, 1998; Han et al., 2001b). Current semiochem- improved by placing more pheromone dispensers ical application systems in other countries, which at the outer area than in the inner area of the mat- are mostly suitable for much larger, uniform-scale ing disruption orchard (Yang et al., 2003). Even in agriculture systems, may need to be modified for the orchard where population density of G. molesta optimal efficiency in the Korean environment. was relatively high, a commercially acceptable In the early 1990s, a monitoring experiment and control level (1.7%) could be achieved by mating 24 K. S. BOO and K. C. PARK disruption with increased amount of pheromone cordingly in semiochemical research. (Yang et al., 2003). Mass trapping and mating disruption was also FUTURE DIRECTION AND PROSPECTS evaluated for Spodoptera exigua (Park and Kim, 1995, 2002). Mass trapping showed a significant Communication plays a critical role in our daily reduction of both egg mass and larval infestation in lives, and so it does for insects. Chemical signals a pheromone-trap installed field, and a mating dis- are even far more important than any other kind of ruption trial also showed a significant reduction in communication means in many insect species. The damage level. research on semiochemicals has been growing fast, A research group in Korea once actively en- providing a number of valuable answers as well as gaged in chemical synthesis of insect pheromone leaving a number of new questions. After the initial components in the mid 1980s–early 1990s (Kang et scientific evidence of the presence of insect sex al., 1985, 1990) (Table 1, Fig. 1). However, it was pheromone in the 19th century (Fabre, 1886), rather unfortunate that the active research was chemical structure of pheromone was first identi- not extended to practical use, and the otherwise fied in 1959 (Butenandt et al., 1959). After the first productive research on chemical synthesis of findings and debates on the possible olfactory role pheromones has become much less active since of insect antennae in the 1920s, it was experimen- that time. tally proved in the 1950s that the antennae are in- deed olfactory organs (Boistel and Coraboeuf, 1953; Schneider, 1957). After the first suggestion INTERNATIONAL COLLABORATION AND of the potential of semiochemicals for use in pest ORGANIZATION management in the 1940s (Karg and Suckling, Along with growing research activities, semio- 1999), the practical application was initiated in the chemical-related international meetings and organ- late 1970s. Thereafter, semiochemical research has izing activities also became active. Several semio- been accelerated with technical developments in chemical-related international symposia and other various disciplines. Recently, attempts are even meetings were held in Korea during the last decade being made to use whole insects or the antennae as (Boo et al., 1996; Boo, 2002). Perhaps one of the an olfactory biosensor to detect and locate odor of most valuable achievements in terms of interna- interest such as landmine, food odors, etc. (Park, tional collaboration in this region was the organiza- 2002; Park et al., 2002b). As relatively recent par- tion of the Asia-Pacific Association of Chemical ticipants, Koreans researching semiochemicals Ecologists (APACE) and the initiation of the Jour- have taken advantage of these pioneering studies, nal of Asia-Pacific Entomology. Regular biannual and are now ready to join the frontlines. After initi- meetings of APACE have been held twice in this ating from a simple identification work in a single region. However, it is rather unfortunate that the species, semiochemical communication systems first scheduled combined meeting of the Interna- have begun to be understood in more complicated tional Society of Chemical Ecology and APACE, systems as shown in the roles of semiochemicals in which was scheduled to be held in Korea in 2003, tritrophic relationships. had to be cancelled due to the outbreak of SARS. In the highly competitive domestic and interna- But the third APACE meeting may be held in 2005 tional market, because of growing consumer’s con- in conjunction with the fifth APCE (Asia-Pacific cerns about residual chemicals and increasing Congress of Entomology) meeting in Jeju, Korea. quarantine concerns and barriers, there is a greater A relatively rapid development in semiochemical demand than ever to produce environmentally research in Korea could be accomplished by close sound and chemical residue-free agricultural prod- collaborations with foreign scientists as well as by ucts. The demand for pesticide-free products and motivated Korean scientists. In chemical ecology quarantine requirement of pest-free products can research in Korea, perhaps it would be important to be achieved by managing pest populations using have close collaboration and information exchange. semiochemicals. The continuous global growth Geographic, climatic and agricultural characteris- (10% annually) in semiochemical use for pest tics in different regions should be recognized ac- management during the last decade is expected to Insect Semiochemical Research in Korea 25 continue for the next several decades although tra- introduce and apply existing yet-to-be-introduced ditional pesticide use still appears to be inevitable. technologies into our semiochemical research sys- Indiscriminate use of broad-spectrum pesticides tem. has already caused a number of problems and as a Korean semiochemical research has mainly fo- result a vicious cycle has been occurring in a num- cused on horticulture-related species, and this can ber of instances. Initial doubt and obstacles against be expanded to other target insects such as forestry using semiochemicals for pest management have pests, other crop pests, stored-product pests and been overcome in recent decades. hematophagous pests. So far, most semiochemical The eventual goal of semiochemical research research in Korea has focused on insect-derived would be a fundamental understanding of olfactory compounds. However, as shown in recent studies communication systems from molecular phenom- (Bengtsson et al., 2001; De Moraes et al., 2001; ena to the ecosystem level, and its practical appli- Knight and Light, 2001; Hern and Dorn, 2002), cation in various ways. Basic research may require there are a number of plant-derived semiochemi- a longer period and may not have an immediate cals regulating insect behavior. This would be an- economic impact, but once this is accomplished it other promising research area, which may provide can have profound impacts on various related a useful means to manipulate behavior of insect fields. Species-specific ecology and physiology re- pests. In fact, there are many research efforts in lated to semiochemicals should be understood in a progress on plant-derived semiochemicals that greater detail, and more fundamental and broader show promise for use in manipulation of behavior physiological questions, such as the transduction of lepidopteran pests, for example, apple leaf and mechanisms, integration of olfactory information pear volatiles for the female codling moth (Hall, in the brain, central process governing behavior, 2002). and regulating mechanisms for all these processes Successful technology transfer for the apple should be addressed. Further, an understanding of orchard community in Korea to use sex phero- these processes at the molecular level should be mone for controlling insect pests (Lee et al., 2002) achieved. Current major understandings of the ol- is a good example and can be used as a guide factory communication system also need to be ex- for other future applications. Internet-based, field- panded from an individual level to more complex population monitoring system using semiochemi- systems. In Korean farming systems that can be cals, which has been successfully constructed characterized as a mixture of various plants and in- for apple farmers in Korea (Lee et al., 2002; sects in a relatively small farming area, more effec- www.iloveapple.co.kr), can be expanded to other tive use of semiochemicals can be achieved by in- insect pests to cover a wider area and to integrate a tegrated approaches considering the entire ecosys- variety of insect pests and target plants. Long-term tem and components in the area with an under- mating disruption/mass-trapping trials and evalua- standing of the complex semiochemical communi- tion programs will be needed. A good example of cation system in the given ecosystem. the need for long-term evaluation of semiochemi- As mentioned earlier, technological advances cal application is that sequential trials over years have been directly playing a critical role in the on the same area can have a significant effect on major advances in our understanding of semio- controlling insect pests using pheromones (Yang et chemicals. Analytical chemistry and electrophysi- al., 2002a). More recent semiochemical application ology are among the best examples. GC-EAD tech- strategies such as lure and kill, push-pull strategy nique made it possible to determine which of the and stimulo-deterrent diversionary strategies compounds in an odor mix produced a physiologi- (SDDS) (Campbell and Pope, 2002) will also cal response, and so might be behaviorally impor- need to be practiced in Korean fields. Routine tant (Moorhouse et al., 1969; Chapman, 2000). quarantine examination can effectively use semio- Molecular biology and computer technology have chemicals. Pheromone analogues may replace also greatly influenced semiochemical research in pheromones when these are costly to prepare or un- many ways, as they have done in almost every stable under field conditions (Renou and Guerrero, other biological science. Together with use of tradi- 2000). tional methodologies, we will need to be ready to Legislative support should also be prepared to 26 K. S. BOO and K. C. PARK use semiochemicals more effectively and to facili- Entomol. 1: 17–23. tate it. Semiochemicals should not be treated as a Boo, K. S. (ed.) (2002) Korea-UK Bilateral Workshop on sibling category of toxic pesticides, as shown in Chemical Ecology. Seoul National University, Suwon, Korea. 140 pp. some other countries. Chemical synthesis and de- Boo, K. S. and S. J. Ahn (2001) Electroantennographic re- velopment of proper dispenser systems is another sponses of the oriental tobacco budworm, Helicoverpa important factor in using semiochemicals. A robust assulta, to plant volatile compounds. In Second Asia- research system in chemical ecology and semio- Pacific Conference on Chemical Ecology. Penang, chemical research should be maintained in Korea, Malaysia, pp. 43–44. Boo, K. S., M. Y. Choi, I. B. Chung, V. F. Eastop, J. A. Pickett, and the information obtained through semiochemi- L. J. Wadhams and C. M. Woodcock (2000) Sex cal research will be extremely important not only pheromone of the peach aphid, Tuberocephalus momonis, in IPM of agriculture but also bio-security and na- and optimal blends for trapping males and females in the tional security in a broader context. field. J. Chem. Ecol. 26: 601–609. Boo, K. S. and C. H. Jung (1998) Field tests of synthetic sex ACKNOWLEDGEMENTS pheromone of the apple leafminer moth, Phyllonorycter ringoniella. 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