Appl. Entomol. Zool. 45 (1): 121–128 (2010) http://odokon.org/

Nocturnal flight activities of the female Asian gypsy moth, Lymantria dispar (Linnaeus) (Lepidoptera: Lymantriidae)

Ren IWAIZUMI,1,* Kenryo ARAKAWA1 and Chiharu KOSHIO2 1 Research Division of the Yokohama Plant Protection Station; Yokohama, Kanagawa 231–0801, Japan 2 Naruto University of Education; Naruto, Tokushima 772–8502, Japan (Received 5 November 2008; Accepted 17 August 2009)

Abstract The flight and other behavior of the female Asian gypsy moth, Lymantria dispar, were observed in a net cage under natural photoperiodic conditions in May–August in Yokohama City, Japan. Both virgin and mated females moved by flight between 19:00 and 21:00, which coincided with one to two hours after sunset. Virgin females continued releas- ing pheromone, i.e., calling behavior, at the new site and sometimes copulated with males at night. If they could not copulate that night and in the subsequent daytime, they flew again the subsequent evening. Mated females started oviposition after their flight and thereafter did not move again. The mean flight speed of a virgin female was estimated as 21.3 m/min. The flight duration was approximately 10 min for both virgin and mated females, and therefore females could move 200 m on average and a maximum of 750 m during one night. These nocturnal activities of the Asian gypsy moth should be considered in order to establish effective control.

Key words: Asian gypsy moth; flight activity; Lymantria dispar; mating behavior; reproduction

Asia (China, Korea, Far East Russia etc.). In Japan, INTRODUCTION L. dispar japonica is distributed in Honshu, The gypsy moth, Lymantria dispar (Linnaeus), Shikoku, Kyushu and southwestern Hokkaido, and is distributed widely in temperate regions and at- L. umbrosa is distributed in Hokkaido. Studies to tacks a very wide variety of trees; thus, it is the clarify the taxonomic status of each AGM are un- most notorious pest of forests and ornamental trees derway. in the world (Leonard, 1974). It is classified into Recently, the U.S. and Canadian governments two groups (types), the European gypsy moth have become very anxious about the invasion of (EGM) and Asian gypsy moth (AGM), and the bio- AGM into their territories (Myers et al., 2000), and logical differences between the two groups, e.g., have requested that countries with AGM control host range, female behavior, as well as genetic dif- them in port export areas, and to certify that ships ferences examined by DNA analysis, were reported destined for the United States and Canada are free (Bogdanowicz et al., 1993, 1997; Pfeifer et al., from AGM egg masses (Yokochi, 2007). Thus, 1995; Schreiber et al., 1997; Reineke and Zebitz, Japanese port authorities initiated an AGM control 1999). program in 2007 to reduce the AGM population in According to Pogue and Schaefer (2007), EGM ports. is a single subspecies of L. dispar dispar which oc- The evaluation of female AGM flight ability is curs throughout Europe, near to the Ural Moun- important, especially to determine the control area tains, North Africa and introduced into North around ports, because it is likely that the risk of America, while AGM is composed of several egg masses attaching to vessels is strongly related species and subspecies, which occur throughout to the numbers of females attracted to their light temperate Asia, including Japan. Among them, L. sources at night; however, we have insufficient dispar asiatica is distributed widely in continental knowledge on their behavior. Koshio (1996)

* To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2010.121

121 122 R. IWAIZUMI et al. reported the pre-oviposition behavior of AGM After emergence, they were kept in the department females and clarified that mated females showed until the start of experiments. fluttering, walking, and flight behavior for about Just before the start of each experiment, all fe- one hour after sunset to search for oviposition sites, males were marked on their forewings with an oil and then oviposited during the night. Charlton et marker for individual recognition. Female behavior al. (1999) reported a similar observation of AGM was observed in a net cage (experimental cage: in central Siberia and Germany (an invasive popu- 1.9 m height, 1.3 m width and 2.9 m depth) in- lation). Higashiura (1989a, b) observed that AGM stalled in a greenhouse under natural photoperiodic females chose the height of oviposition sites to conditions. In the center of the experimental cage, avoid predation by birds. we placed a cherry branch (ca. 150 cm in height, We observed virgin and mated AGM female be- 2 cm in diameter) supplied with water, on which fe- havior, especially flight behavior, in a net cage males were placed on day 0 to 2 after emergence. under natural photoperiodic conditions in order to Observing conditions were 25–32°C controlled by evaluate female flight ability to establish effective air-conditioning and the natural day length of May control methods for AGM. We also observed other to August. The sunset time during the experimental nocturnal behavior to obtain an overview of AGM period was 18:40–19:00. Moth behavior was ob- female reproductive behavior. served at intervals of 30–60 min, except for the pe- riod from around 22:00–5:00 (no observations). Night observation (19:00–22:00) was conducted MATERIALS AND METHODS with a portable light (K-1600; Toshiba Co.), taking All observations were conducted at the Research care to avoid directly lighting the female body. Division of the Yokohama Plant Protection Station Observation 1: Behavior of virgin females. in Yokohama City. Most observations were con- Virgin females of 0 d old were placed in the experi- ducted in 2007 and additional data were obtained mental cage on different days and observed until in 2008. 20:00 on July 26, 2007 without mating. Two fe- The moths examined in this study were collected males were placed in the cage in the late afternoon as larvae or egg masses in the field, and reared by on July 24, one in the early afternoon on July 25, feeding them cherry and pear leaves. We collected and the other in the early afternoon on July 26 (see larvae in Yokohama City (35°20N, 139°40E) on Fig. 1). The weather was fine throughout the exper- May 22, 2007 and egg masses in Chiba City imental period. Two virgin females were also used (35°30N, 140°10E) on November 30, 2006. In for the same experiments on May 23–25, 2008. 2007, we reared larvae and pupae in our depart- The weather was cloudy on May 23 and rainy on ment (room temperature, 27–30°C and natural pho- May 24–25. toperiod). In 2008, they were reared outdoors in a In 2007, we observed female behavior for 5 min plastic case with a screen net, or in the insect rear- at hourly intervals during the daytime. From 19:00 ing room (Koito Co., PCSH-3, 20–25°C, 40–80% to 21:00, when females are expected to be more ac- relative humidity (RH), 16L8D) from egg masses tive (Koshio, 1996), we conducted continuous ob- laid by adults of 2007, collected in Chiba only. servation. After 21:00, their behavior was checked

Fig. 1. Periodic activities of four virgin females in a net cage in 2007. No male was released in the experimental cage. R: Rest- ing, C: Calling by release of sex pheromone, M: Movement by flight, —: no observation. During the periods highlighted in bold, we conducted continuous observation, whilst we observed female behavior for 5 min at hourly intervals during the daytime. Flight Activity of the Female Gypsy Moth 123 at 21:30 and 22:00. In 2008, we observed female were transferred to the experimental cage installed behavior mainly at dusk: from 19:00 to 21:00 on in a greenhouse. We observed female behavior May 23 and from 19:00 to 20:00 on May 24. Their until 21:00 and recorded the start and end of their behaviors were classified into 3 types: rest, calling flight. In order to check re-flight after the end of by pheromone release, and movement by flight. each observation, the position of each female was Calling was judged by the protrusion of the recorded and checked again in the next morning, pheromone gland at the tip of the abdomen, but in 6:00–9:00 am; however, most (16 virgin and 17 some individuals, it could not be discriminated mated), except two individuals (one virgin and one from rest easily. In those cases, we checked more mated), did not fly around midnight. carefully by spending extra times on assessment. Apart from the above three types of behavior, flut- RESULTS tering and walking were observed before and after flight or independently. We did not record these be- Observation 1: Behavior of virgin females haviors precisely, however, because of the continu- Figure 1 shows the periodic behavioral change ous change from calling to these behaviors. of four virgin females examined in 2007. Virgin fe- Observation 2: Behavior of mated females. males rested for several hours after emergence, and From June 22 to August 12, 2007 and July 14–16, then initiated calling behavior. In the following 2008, we used 21 virgin females, including 3 out of days after emergence, calling behavior was initi- 4 females from observation 1 (Nos. 1, 2, and 4 in ated again in the morning and lasted until late Fig. 1), to observe mating and post-copulatory be- evening. Movements by the flight of virgin females havior. During this observation, one to eight males were observed in a limited period from 19:00 to were always present in the experimental cage. 20:00, which coincided with one hour after sunset. After copulation, mated females were kept to Virgin females flew every evening, and two indi- oviposit in the cage until their deaths. We observed viduals (Nos. 2 and 4) showed movement and re- and recorded the time and duration of copulation peated calling during the evening of July 26. Call- and movement by flight, time of discovering the ing was observed at night, as Koshio (1996) men- first oviposition, and longevity of females. In some tioned. In 2008, two virgin females also showed cases, we could not observe female flight behavior flight behavior in a limited period of 19:00–20:00 directly but observed significant changes in their for two nights in succession. resting sites. In these cases, we also identified that they moved by flight once or more. Observation 2: Behavior of mated females Observation 3: Flight distance and speed of a Copulation was observed not only during the day virgin female. In order to estimate the adult dis- but also at night (Table 1). In two cases, it started persion ability of AGM, we measured female flight at 21:15 or 20:03, although females and males speed; however, it was difficult to record their flight were released from 10:00 or 14:00 (Nos. 13 and behavior using a video camera because almost all 20). In four cases, copulation started at 20:03 or virgin and mated females flew at night (see Re- 20:05, only 3 or 5 min after male release (Nos. sults). Only a virgin female flew actively before 14–17). In some cases (Nos. 6, 14–17, and 20), dark on July 10, 2007. We were therefore able to copulation did not finish within the period of ob- record her flight track in the experimental cage servation, but all completed copulation and con- from 16:00 to 17:00 using the video function of a ducted the first oviposition the next morning. digital camera (Pentax Optio 750Z) and estimate Most females did not fly before copulation, ex- the flight speed. cept for females that could not mate during the Observation 4: Flight duration of females. daytime (Nos. 13–16). In general, females moved In May–July, 2007 and 2008, we examined the once after copulation, and then started the first flight duration of 17 virgin and 18 mated females. oviposition within 12 h. However, three females During the daytime, some females were introduced that did not start oviposition within 12 h showed a into a small net cage (mating cage: 30 cm height, second movement the next night or the night after, 30 cm width and 45 cm depth) with males to mate. and then initiated the first oviposition (Nos. 7, 9, At around 17:00, both virgin and mated females and 10). Five females started oviposition without 124 R. IWAIZUMI et al. first after first death first first after oviposition oviposition Days between between Days No. copulation and movement Date of oviposition 2(16-Jul:19:15–19:37, 22:00–5:00) 17-Jul, 5:00 1 0 25-Jul 2(26-Jul:19:15, 22:05–5:00) 27-Jul, 5:00 1 0 3-Aug 3(24-Jul:22:00–5:00, 25-Jul:19:30, 26-Jul:19:15) 27-Jul, 5:00 1 0 1-Aug 2(10-Jul:22:00–5:30, 12-Jul:20:20) 12-Jul, 20:20–23:20 2 0 20-Jul 2(11-Jul:21:00–5:00, 12-Jul:19:30–19:40) 12-Jul, 20:20–23:20 2 0 20-Jul 1(9-Jul:21:40–5:00) 10-Jul, 5:00 1 0 17-Jul 1(22-Jun:17:00–6:00) 23-Jun, 6:00 1 0 1-Jul a Starting and observed Time finishing time observed (time) No. movement first of copulation Table 1. to death change of the female gypsy moth from emergence behavioral Successive 89 10-Jul-2007 10-Jul-2007 10-Jul, 16:00 10-Jul, 16:00 16:10–16:40 16:55–17:55 1(10-Jul:21:30) 11-Jul, 10:00–13:00 1 0 19-Jul 7 10-Jul-2007 10-Jul, 16:00 16:05–16:55 234 6-Jul-20075 7-Jul-20076 6-Jul, 18:30 9-Jul-2007 8-Jul, 17:20 9-Jul-2007 18:40–19:50 9-Jul, 17:30 9-Jul-2007 17:30–20:10 1(6-Jul:19:50) 9-Jul, 17:30 17:35–18:35 1(8-Jul:20:10) 9-Jul, 17:30 17:50–19:50 1(9-Jul:19:50) 17:40–21:40C 1(9-Jul:19:50) 7-Jul, 6:00 9-Jul, 6:00 10-Jul, 5:00 10-Jul, 5:00 1 1 1 1 0 0 0 0 13-Jul 14-Jul 17-Jul 19-Jul 1 22-Jun-2007 22-Jun, 16:00 16:10–17:00 21 16-Jul-2008 17-Jul, 14:00 14:30–15:20 1(17-Jul:19:30–19:53) 17-Jul, 21:00 0 0 25-Jul 1718 12-Aug-200719 14-Jul-2008 13-Aug, 20:0020 15-Jul-2008 20:03–22:03C 15-Jul, 13:20 0 16-Jul-2008 15-Jul, 13:20 15:05–15:50 16-Jul, 14:00 13:21–13:52 1(15-Jul:19:22-19:47) 20:03–22:00C 1(15-Jul:19:16–19:32) 15-Jul, 21:30 15-Jul, 21:30 14-Aug, 6:00 0 0 0 1 0 22-Jul 0 20-Jul 19-Aug 16 26-Jul-2007 26-Jul, 20:00 20:05–22:05C 1011 10-Jul-200712 11-Jul-200713 11-Jul, 10:30 11-Jul-200714 12-Jul, 10:00 12:30–13:00 11-Jul-200715 12-Jul, 10:00 11:40–12:05 24-Jul-2007 2(11-Jul:20:00, 12-Jul:20:20) 12-Jul, 10:00 13:10–13:50 24-Jul-2007 0 26-Jul, 20:00 21:15–22:20 1(12-Jul:20:20) 26-Jul, 20:00 20:05–22:05C 1(12-Jul:20:20) 3(24-Jul:19:20, 25-Jul:19:30, 26-Jul:19:15) 20:05–22:05C 27-Jul, 5:00 13-Jul, 5:00 1 2 12-Jul, 23:20–5:00 13-Jul, 5:00 0 0 0 12-Jul, 15:00–17:00 2-Aug 0 1 17-Jul 0 0 0 15-Jul 20-Jul 18-Jul No. emergence of examination When the copulation did not finish within the period of observation, C was added after time. All finished the next morning. added after time. All finished the next C was When the copulation did not finish within period of observation, a Individual Individual Date of Starting time Flight Activity of the Female Gypsy Moth 125

Fig. 2. Tracks of the flight of the female gypsy moth in the experimental cage. These are views from above the cage. The fe- male flew only in the upper portion of the cage. Three replications of 30 s are shown. movement after copulation (Nos. 11, 13–15, and Observation 4: Flight duration of females 17). Thirteen of 20 female moved between 19:00 The mean flight duration was measured at 10.6 and 21:00 before the initiation of oviposition. This min (SD9.2, n17) for virgin females and 12.6 period coincided with about one to two hours after min (SD5.7, n18) for mated females. There sunset, as sunset time during the experimental pe- was no significant difference in flight duration be- riod was 18:40–19:00. Six other movements oc- tween virgin and mated females (t-test, p0.05). curred after 21:00, and the other occurred after The maximum record was 35 min for virgin fe- 17:00. Once oviposition had started, females did males and 25 min for mated females, while the not fly (Table 1). minimum was zero for both females. The longevity of 21 females used in the mating observations was 8.50.6 (d, meanSD). DISCUSSION Observation 3: Flight distance and speed of a Koshio (1996) reported the preovipositional virgin female flight behavior of mated females. Our results indi- The simplified flight tracks of a virgin female cate that not only mated females but also virgin fe- based on the video recorded by digital camera are males fly actively after sunset without mating. It is shown in Fig. 2. She flew between locations on the most likely that the preovipositional flight behavior upper surface and higher points of the experimen- of mated females has the function of ovipositional tal cage without landing on the ground. No prefer- site selection, such as optimal height (Higashiura, ence for a particular direction was observed. 1989a, b). In virgin females, in contrast, their flight She sometimes touched the upper portion of the behavior seems to be to move to a more appropri- lateral net, but the influence on the estimation of ate site for mating. During daytime, virgin females flight distance seemed to be minimal because she continue calling behavior to attract males. If they did not stay there long (within one second) cannot copulate with males, they move by flight throughout the recording periods. soon after sunset and then call males again from The flight distances (m) measured during tracks new sites from that night. In other words, in the of 30 s were 10.4, 9.9, and 11.7, respectively. As a evening, virgin females fly to search for a more ap- result, the flight speed (m/min) was estimated at propriate site for mating where males are abundant, 21.31.9 (meanSD). while males fly to search for females during the daytime. We also observed some copulation at night (Nos. 126 R. IWAIZUMI et al.

13–17, and 20 in Table 1). In two cases (Nos. 13 and continue calling from the new site. These fe- and 20), females could not copulate during the day- males copulate with males during that night or in time, although males were present and females the subsequent daytime. Virgin females repeat were calling from the morning or afternoon. In the flight behavior every evening until they copulate. If other four cases, mating experiments were started females mate at night, they usually start oviposition at 20:00, and they copulated within 5 min (Nos. at the same sites without flight. In contrast, females 14–17). Five of these females moved just before mated during the daytime usually fly to the oviposi- copulation (Nos. 13–16, and 20). Cardé et al. tion site after sunset. Females oviposit intermit- (1974) reported a periodic change in the attraction tently for several nights in succession and then die of pheromones or virgin females for males in after completing the egg mass. northern Connecticut, USA. The results showed a The mean flight speed of a virgin female was double peak of male attraction, 10:00–11:00 and 21.3 (m/min), and the flight duration was measured 19:00–20:00. Fullard and Napoleone (2001) also at 10.6 min for virgin females and 12.6 min for showed both diurnal and nocturnal activities in a mated females. So far, the flight speed, duration Canadian population of gypsy moths. Moreover, and distance of moths have been measured or esti- Cardé et al. (1996) reported that male Asian gypsy mated mainly using a flight mill (Noda and Ka- moths were attracted to synthetic pheromone and mano, 1988; Shirai, 1991, 1998; Shumacher et al., showed a bimodal pattern of attraction, the first 1997; Shirai et al., 1998; Shirai and Kosugi, 2000; peak in early to mid-afternoon and the second peak Ishiguri and Shirai, 2004). Using the method, the at the subsequent sunset. This suggests that both flight speed (m/min) of virgin females was Asian and European gypsy moths have nocturnal recorded as follows, Spodoptera litura (50–60), mating systems as well as diurnal mating systems. Plutella xylostella (15), Cydia pomonella (50–60), Our results demonstrate the nocturnal matings of Ostrinia furnacalis (30), Homona magnanima Asian gypsy moths under semi-natural conditions. (20–30), Adoxophyes honmai (20–30), Carposina Females who copulated at night often started sasakii (20–30). The flight speed of a virgin female oviposition in place without moving (Nos. 13–15, of Lymantria dispar in the present study is almost and 17 in Table 1). the same as those of Homona magnanima, Adoxo- Our results and Koshio (1996) give an overview phyes honmai and Carposina sasakii, although the of gypsy moth female flight behavior (Fig. 3). The method of measurement was different from the eclosion of females was observed most frequently method for the three species. around noon except for a few females that emerged We were not able to record the flight behavior of in the morning (7:00) or evening (19:00) (R. all other individuals in the dark to estimate their Iwaizumi, unpublished data). Females start calling flight speed, and could not compare the flight pat- and copulate with males usually on the day of tern of this virgin female with that of other fe- emergence. If they cannot mate during the daytime, males, including mated females. In our observa- they move by flight soon after sunset that evening tions, no particular difference was observed in the

Fig. 3. Outline of AGM female behavior. During the daytime, females continue calling and copulate if males approach. Both mated and non-mated females fly in the evening. Mated females then start oviposition and never fly again. Non-mated females con- tinue calling even at night and copulate if males approach. Virgin females repeat calling and flight in evening until they can copu- late. Flight Activity of the Female Gypsy Moth 127

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