Appl. Entomol. Zool. 40 (3): 399–404 (2005)

Appl. Entomol. Zool. 40 (3): 399–404 (2005) http://odokon.ac.affrc.go.jp/

Population establishment of the leafroller Eudemis gyrotis (Lepidoptera: Tortricidae) at a new plantation of bayberry Myrica rubra (Myricaceae)

Shinji SUGIURA*,† Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University; Kyoto 606–8502, Japan (Received 19 December 2004; Accepted 24 February 2005)

Abstract To clarify the immigration process of a phytophagous insect to a new habitat, I examined seasonal changes in the abundance and parasitism of larvae and pupae of a leafroller, Eudemis gyrotis (Meyrick) (Lepidoptera: Tortricidae), at both a new and an old plantation of the bayberry Myrica rubra Sieb. et Zucc. (Myricaceae) on Mt. Tanakami, Shiga Prefecture, central Japan, in 1999. E. gyrotis adults singly lay eggs on only young leaves of M. rubra, and their larvae feed on the leaves. Therefore, the young leaves of M. rubra are necessary for the occurrence of E. gyrotis larvae. The number of E. gyrotis larvae per tree was correlated with the amount of young leaves per tree. At the old plantation where E. gyrotis had already been found in 1998, the larval occurrence of E. gyrotis began in late May. At the new plantation, which was at a distance of ca. 600 m from the old plantation, E. gyrotis larvae had not occurred by late July, although there was an abundance of young leaves of M. rubra in late May. These ﬁndings suggest that E. gyrotis adults that had emerged from the old plantation in July immigrated to the new plantation and laid eggs on the plants there. The parasitoids that attacked E. gyrotis at the new plantation just after immigration were polyphagous. This suggests that those parasitoids switched hosts from other herbivore species to E. gyrotis. In spite of the attack by polyphagous parasitoids, the E. gyrotis population successfully established itself at the new plantation.

Key words: Herbivores; immigration; leaf phenology; polyphagous parasitoids

and Sato, 1990). In particular for herbivorous in- INTRODUCTION sects, the presence of their host plants and para- To predict population dynamics of pest insects in sitoids appear to influence immigration and popu- a newly-created habitat, it is important to examine lation establishment in the new habitat, respec- their immigration processes to new farmlands and tively (Ohsaki and Sato, 1990). Furthermore, the forests. These processes are influenced by the host ranges of herbivores and their natural enemies mode of dispersion, which is itself affected by vari- are also influential in succeeding the immigration ous biotic and abiotic factors (e.g., Stinner et al., and establishment by the herbivores; host plants 1983). Insects utilizing a short-term habitat must might be more important for specialist herbivores constantly migrate in search of new habitats. How- than for generalist ones, while generalist para- ever, even insects that utilize long-term habitats sitoids might influence the herbivores more must migrate to escape from intraspecific competi- strongly than specialist parasitoids. tion and natural enemy pressures (Southwood, Eudemis gyrotis (Meyrick) (Tortricidae: Lepi- 1977). doptera), whose larvae feed on the young leaves of The immigration of insects to a new habitat may Myrica rubra Sieb. et Zucc. (Myricaceae), is a be influenced by the quality and/or quantity of the monophagous leafroller (Yasuda, 1969; Kawabe, food resources in the old habitat, while the popula- 1982). M. rubra, which is an evergreen broad- tion establishment may be influenced by the pres- leaved tree, is distributed in south-western Japan, ence of natural enemies in the new habitat (Ohsaki South Korea, China, and Taiwan (Satake et al.,

* E-mail: [email protected] † Present address: Department of Forest Entomology, Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, Ibaraki 305–8687, Japan DOI: 10.1303/aez.2005.399

399 400 S. SUGIURA

1989). Since M. rubra has attracted attention for (Matsumura) (Ichneumonidae) are common pupal greening and soil erosion control in recent years, it parasitoids (Sugiura and Osawa, 2001, 2002). has been frequently planted in warm-temperate re- These parasitoids have been thought to be general- gions of Japan (Fushimi, 1993). On young trees of ists rather than specialists, since they have been re- M. rubra, the density of E. gyrotis is frequently ported in other microlepidopteran hosts (Habu, high (Sugiura and Osawa, 2001), adversely affect- 1960; Momoi et al., 1975; Yukinari, 1984; Mao ing the early growth of M. rubra samplings. and Kunimi, 1991; Ueno and Tanaka, 1994; Sugi- The life history and parasitoid community of E. ura, S., unpublished data). gyrotis have already been reported (Yasuda, 1969; To clarify the process of pest insect immigration Sugiura and Osawa, 2001, 2002). In mid-May at to a new habitat, I clariﬁed the population estab- Mt. Tanakami, central Japan, overwintered E. gyro- lishment of E. gyrotis at a new plantation by com- tis adults lay eggs on the young leaves of elongat- paring the seasonal abundance and parasitism of E. ing shoots of M. rubra. Hatched E. gyrotis larvae gyrotis between a new and an old plantation of M. roll young leaves with silk thread and then they eat rubra. the leaves inside the rolls before pupating in the rolls. Under natural conditions, it takes approxi- MATERIALS AND METHODS mately 25–35 d from oviposition to adult eclosion; the egg stage is ca. 5–10 d, larval stage ca. 10–15 d Study site. The study was carried out at two and the pupal stage ca. 10 d. E. gyrotis has several sites (a new and an old plantation) at the Sasama- generations per year, with overlapping generations. gatake Experimental Area (34°55N, 135°56E, Thirteen parasitoid species have been recorded 260–280 m above sea level; Fig. 1), on Mt. as primary parasitoids of E. gyrotis (Sugiura and Tanakami, Shiga Prefecture, central Japan. The Osawa, 2001; Table 1): Apanteles sp. (ater-group) mean annual temperature was 12.4°C and mean an- (Braconidae) and Goniozus japonicus Ashmead nual precipitation was 1,411 mm during the years (Bethylidae) are dominant larval parasitoids, while from 1976 to 1980 (Iwatsubo et al., 1982). Brachymeria excarinata Gahan (Chalcididae), B. At the old plantation (ca. 0.1 ha) in the spring of lasus (Walker), and Itoplectis alternans spectabilis 1996, 274 M. rubra trees were transplanted to-

Table1. Primary parasitoids of E. gyrotis larvae and pupae at the old plantation in 1998 and 1999 (Sugiura and Osawa, 2001)

Host stagea Order Parasitism Parasitoid species Family modeb Oviposited Killed

Hymenoptera Chalcididae Brachymeria lasus PPIDB B. excarinata PPIDB Eulophidae Elachertus sp. ML (EL) ML (EL) IDB Elasmidae Elasmus sp. LL LL IDB Ichneumonidae Itoplectis alternans spectabilis PPIDB Pristomerus sp. EL ML KOB Acropimpla sp. LL LL IDB Braconidae Apanteles sp. (ater-group) EL ML KOB Bracon sp. LL LL IDB Bethylidae Goniozus japonicus LL (ML) LL (ML) IDB Diptera Tachinidae Elodia flovipalpis ?L P KOB Nemorilla floralis LL P KOB unidentified species ?L ML KOB

a EL: 1st–2nd instar, ML: 3rd–4th instar, LL: 5th instar, and P: pupa. b Koinobiont parasitoids (KOB) permit their hosts to develop after oviposition, while idiobiont ones (IDB) kill their host during oviposition or prevent it from developing after oviposition. Population Establishment of E. gyrotis on a Plantation 401

ors were reddish or light green, were easily distinguished from mature leaves. At the new plantation, the seasonal abundance of E. gyrotis larvae and pupae was also studied. All the trees (N120) were examined before the abundant E. gyrotis larvae were found. When E. gyrotis larvae or pupae were found, I counted their numbers of them and examined whether its larvae were parasitized or not in the field. Although it was diffi- cult to examine if they were parasitized in the field, I investigate the parasitism by identifying the cocoons of larval parasitoids, Apanteles sp. and G. japonicus, on the basis of morphological characteristics: one white cocoon of Apanteles sp. and many brown cocoons of G. japonicus per host (Sugiura Fig. 1. Study site. and Osawa, 2001). After E. gyrotis larvae or pupae became abundant, I collected them on five ran- gether with Quercus serrata Thunb., Q. glauca domly selected plants to examine the parasitism. Thunb., Alnus pendula Matsum., and Cytisus sco- For each census I also counted the number of elon- parius Link. In February 1999, the average height gating shoots containing young leaves on a host of the surviving M. rubra was 118 cm (N236). At plant. I used different sampling methods before the old plantation, E. gyrotis had already been ob- and after the immigration of E. gyrotis to avoid the served in 1998 (Sugiura and Osawa, 2001). effect of the sampling on the migrating host popu- At the new plantation (ca. 0.1 ha), which was ca. lation. 600 m away from the old one (Fig. 1), 120 M. rubra All the larvae and pupae of E. gyrotis and para- trees were transplanted together with Q. serrata sitoids collected from the roll were individually and Q. glauca in March 1999. The average height reared in plastic petri dishes (90 mm in diameter, of M. rubra was 57 cm (N120). No M. rubra 15 mm in height) containing young leaves of M. grew around the old and new plantation, although rubra and wet tissue paper under laboratory condi- many trees of other species (Pinus thunbergii Parl., tions (Sugiura and Osawa, 2001, 2002). I supplied A. pendula, and C. scoparius) were planted in the fresh young leaves and replaced the paper at inter- vicinity for erosion protection. vals of 1–3 d. The developmental stages of the lar- Sampling procedure. At the old plantation, all vae and pupae were checked at intervals of 1–3 d. the leafrolls were collected from ten randomly se- When the adults of moths or parasitoids emerged, I lected plants of M. rubra at 2-wk intervals from made all the insect specimens for identification. May to October 1999 (Sugiura and Osawa, 2001, Data analysis. The total number of E. gyrotis 2002). In the field and laboratory, I distinguished larvae and pupae and elongating shoots of M. larvae and pupae of E. gyrotis from those of other rubra at both sites were estimated by multiplying lepidopteran species found at the site on the basis their respective numbers per plant by the total trees of morphological characteristics: black spots of the at each site. The number of E. gyrotis and elongat- larval head capsule (Yasuda, 1969) and the color ing shoots of M. rubra ranged over several orders (light brown) and size (7.0–9.0 mm) in the pupa of magnitude, and they included zero values occur- (Sugiura, S., personal observation). For each cen- ring in every sampling day. Therefore, the number sus I counted the number of elongating shoots that was added to one and then log-transformed. Pea- contained young leaves upon which E. gyrotis son’s correlation test was used to compare the sea- adults could potentially lay eggs and their larvae sonal changes in the number of E. gyrotis larvae could exclusively feed. The number of elongating between the new and old plantations. A linear re- shoots was considered as an indicator of the gression model was used to analyze the relation- amount of young leaves available as the food ship between the density of E. gyrotis larvae and source for E. gyrotis. The young leaves, whose col- the number of elongating shoots per host plant. 402 S. SUGIURA

Table2. The relationship between the amount of young leaves and the density of E. gyrotis larvae at the old plantation in 1999

Sampling Slope d.f. r2 F-value p-value day

19 May 1.10 9 0.49 7.57 0.025 6 June 0.30 9 0.47 7.21 0.028 22 June 0.38 9 0.20 1.99 0.196 8 July 0.10 9 0.07 0.58 0.469 22 July 1.40 9 0.43 5.98 0.040 5 Aug. 1.42 9 0.76 25.62 0.001 Fig. 2. Seasonal change in the amount of young leaves of 23 Aug. 0.95 9 0.67 15.91 0.004 M. rubra at a new plantation (open circles) and an old planta- 10 Sep. 0.52 9 0.08 0.71 0.424 tion (closed circles). 27 Sep. 0.23 9 0.03 0.21 0.661 8 Oct. 0.07 9 0.02 0.20 0.670 22 Oct. 0.04 9 0.02 0.14 0.716 Total 0.48 119 0.22 32.45 0.001

RESULTS Variation of the density of E. gyrotis larvae in relation to the amount of young leaves of host plants A total of 1,305 E. gyrotis larvae plus pupae were collected at the old plantation in 1999. The relationship between the number of E. gyrotis larvae and that of elongating shoots containing young leaves per host plant is shown in Table 2. For all pooled data, the slope was significantly positive (Table 2). For each sampling, the slopes were positive in ten out of 11 samplings, five of which had significantly positive slopes (Table 2). This indicates that the density of E. gyrotis larvae depended Fig. 3. Seasonal change in the number of E. gyrotis larvae (closed circles) and pupae (open circles) at the old plantation on the amount of young leaves per host plant. (a) and the new plantation (b). The arrow indicates when E. gyrotis might have immigrated to the new plantation. Seasonal change in the amount of young leaves of host plants M. rubra began to produce young leaves in early gyrotis repeated some generations (Fig. 3a). At the May at the old plantation, but did not produce them new plantation, larvae of E. gyrotis were not de- until late May at the new plantation (Fig. 2). After tected until late July (Fig. 3b), but thereafter the late May, M. rubra continuously produced young seasonal change in the number of E. gyrotis larvae leaves at both the old and new plantations (Fig. 2). was similar to that at the old plantation (r0.86, Therefore, the young leaves of host plants, which N7, p0.05). are necessary for E. gyrotis larvae as a food, were abundant at both sites in late May. Parasitoids attacking E. gyrotis at the new plantation Seasonal changes in the number of E. gyrotis At the new plantation, cocoons of Apanteles sp. larvae plus pupae were observed in the rolls of E. gyrotis in late July At the old plantation, the larvae of E. gyrotis when the larvae of E. gyrotis were detected for the were first found in late May (Fig. 3a), and then E. first time (Table 3). In early August, larvae of G. Population Establishment of E. gyrotis on a Plantation 403

Table3.Parasitism of E. gyrotis at the new plantation

Sampling date

22 July 5 Aug. 23 Aug. 10 Sep. 27 Sep. 8 Oct. 22 Oct.

Total no. E. gyrotis larvae 12 43 40 959.4a 93.6a 23.4a 0a Total no. E. gyrotis pupae 0 1 2 187.2a 70.2a 46.8a 23.4a Sampled no. E. gyrotis larvae per 5 trees — — — 41 4 1 0 Sampled no. E. gyrotis pupae per 5 trees — — — 8 3 2 1 No. parasitized by Apanteles sp. (% parasitism)b 2 (16.7) 3 (7.0) 0 (0.0) 2 (4.9) 1 (25.0) 0 (0.0) 0 No. parasitized by G. japonicus (% parasitism)b 0 (0.0) 2 (4.7) 0 (0.0) 1 (2.4) 0 (0.0) 0 (0.0) 0 (0.0) No. parasitized by B. excarinata (% parasitism) — — — 3 (37.5) 1 (33.3) 1 (50.0) 1 (100.0)

a Values were estimated by random sampling (see text). b Values of parasitism before the random sampling may be underestimated, since we could not examine all the parasitism events (see text). japonicus feeding on an E. gyrotis larva were also the old plantation every year (Sugiura and Osawa, observed (Table 3). Furthermore, Apanteles sp., G. 2001). At the new plantation, M. rubra trees started japonicus, and B. excarinata were observed to to produce young leaves in late May (Fig. 2) since emerge from the E. gyrotis larvae and pupae sam- they had been planted in March. However, after pled after early September (Table 3). These obser- late May, M. rubra continued to produce young vations showed that Apanteles sp., G. japonicus, leaves at both the new plantation and the old plan- and B. excarinata attacked E. gyrotis larvae and tation (Fig. 2). pupae just after the immigration of E. gyrotis to the At the old plantation, E. gyrotis larvae occurred new plantation. from late May (Fig. 3a), showing the same occurrence pattern recognized in 1998 (Sugiura and Osawa, 2001). On the other hand, at the new plan- DISCUSSION tation, no larvae had been found by late July (Fig. The density of insect pests at a site is determined 3b), although young leaves of M. rubra were abun- by two phases of the population process: (1) immi- dant in late May (Fig. 2). Since no M. rubra grew gration of the pest from other habitats, and (2) the in the surrounding area, E. gyrotis adults that had survival rate of species growing at the site (Yama- emerged from the old plantation may have immi- mura and Yano, 1999). I investigated the immigra- grated to the new plantation and laid eggs on the tion of a leafroller, E. gyrotis, to a new habitat by host plants in July. comparing the occurrence patterns of the larvae and pupae between a new and an old plantation. To Establishment of an E. gyrotis population in the clarify the effects of food resources and natural en- new plantation emies on the immigration process of E. gyrotis, I At the new plantation, the seasonal change in the also investigated the amount of food available for number of E. gyrotis larvae after immigration was E. gyrotis and the parasitism rate on it at the new similar to the seasonal change at the old plantation plantation. (Fig. 3), suggesting that the E. gyrotis population was successfully established just after the immigra- Immigration of E. gyrotis to the new plantation tion to the new plantation. This rapid population E. gyrotis larvae exclusively feed on the young growth at the new plantation may have been caused leaves of M. rubra (Sugiura and Osawa, 2001). by the continuous migration of E. gyrotis adults This habit coincides with the result that the number from the old plantation. of E. gyrotis larvae per tree significantly correlated At the new plantation, Apanteles sp., G. japoni- with the amount of young leaves per plant (Table cus, and B. excarinata were recorded as the pri- 2). mary parasitoids of E. gyrotis larvae and pupae M. rubra produced young leaves in late April at (Table 3). These parasitoids were also dominant at 404 S. SUGIURA the old plantation (Sugiura and Osawa, 2001, species. Bull. Natl. Inst. Agric. Sci., Tokyo (C) 11: 2002). 131–363. Apanteles sp. was observed to parasitize the lar- Iwatsubo, G., Y. Hirabayashi and T. Tsutsumi (1982) On the spraying of sewage water in a forest. (II) Effects of the vae of other polyphagous leafrollers on M. rubra in spraying on the run-off water chemicals and the nutrient June at the new plantation (Sugiura, S., personal budgets of the forest watershed. J. Jpn. For. Soc. 64: observation). G. japonicus and B. excarinata have 419–428. been reported to attack various lepidopteran Kawabe, A. (1982) Tortricidae. In Moths of Japan. Vol. 1 (H. species (Habu, 1960; Momoi et al., 1975; Yukinari, Inoue et al. eds.). Kodansha, Tokyo, pp. 62–150 (in Japanese). 1984; Mao and Kunimi, 1991; Ueno and Tanaka, Mao, H. and Y. Kunimi (1991) Pupal mortality of the orien- 1994; Sugiura, unpublished data). Therefore, the tal tea tortrix, Homona magnanima Diakonoff (Lepi- parasitoids recorded at the new plantation were doptera: Tortricidae), caused by parasitoids and thought to be polyphagous. These polyphagous pathogens. Jpn. J. Appl. Entomol. Zool. 35: 241–245 (in parasitoids might have switched hosts from other Japanese with English summary). lepidopteran species to E. gyrotis, just after E. gy- Momoi, S., H. Sugawara and K. Honma (1975) Ichneumonid and braconid parasites of lepidopterous leaf-rollers of rotis immigrated to the new plantation. It is impor- economic importance in horticulture and tea-culture (Hy- tant to detect the parasitism by polyphagous para- menoptera). In JIBP Synthesis: Approaches to Biological sitoids in the early stage of pest immigration. Control. Vol. 7 (K. Yasumatsu and H. Mori eds.). Univ. Among them, Apanteles sp. may be an important of Tokyo Press, Tokyo, pp. 47–60. enemy of E. gyrotis, since the parasitism is tempo- Ohsaki, N. and Y. Sato (1990) Avoidance mechanisms of three Pieris butterfly species against the parasitoid wasp rally density-dependent (Sugiura and Osawa, Apanteles glomeratus. Ecol. Entomol. 15: 169–176. 2002). However, it appears that parasitoids did not Satake, Y., H. Hara, S. Watari and T. Tominari (1989) Wild prevent the establishment of an E. gyrotis popula- Flowers of Japan: Woody Plants. Vol. I. Heibonsha, tion at the new plantation because E. gyrotis adults Tokyo. 321 pp. (in Japanese). continued to migrate from the old plantation. Southwood, T. R. E. (1977) Habitat, the template for ecologi- Therefore, this study suggests that (1) E. gyrotis cal strategies. J. Anim. Ecol. 46: 337–365. Stinner, R. E., C. S. Barfield, J. L. Stimac and L. Dohse (1983) population growing at the old plantation caused Dispersal and movement of insect pests. Annu. Rev. En- rapid population growth at the new plantation, and tomol. 28: 319–335. (2) polyphagous parasitoids switched hosts from Sugiura, S. and N. Osawa (2001) Parasitoid community as- other lepidopteran species to E. gyrotis, just after sociated with the leafroller Eudemis gyrotis (Lepidoptera, E. gyrotis immigrated to the new plantation. Tortricidae) on a bayberry. Entomol. Sci. 4: 25–34. Sugiura, S. and N. Osawa (2002) Temporal response of para- ACKNOWLEDGEMENTS sitoids to the density of the leafroller Eudemis gyrotis (Lepidoptera, Tortricidae) on bayberry, Myrica rubra I am grateful to K. Yamazaki (Osaka City Institute of Public (Myricaceae). Environ. Entomol. 31: 988–994. Health and Environmental Sciences) for his encouragement Ueno, T. and T. Tanaka (1994) Comparative biology of six and comments on this paper. I thank N. Osawa (Kyoto Univer- polyphagous solitary pupal endoparasitoids (Hy- sity) for his valuable advice. I also thank K. Kamijo (Bibai menoptera: Ichneumonidae): differential host suitability City, Hokkaido), H. Shima (Kyushu University), K. Maetô and sex allocation. Ann. Entomol. Soc. Am. 87: (Kobe University) and M. Terayama (the University of Tokyo) 592–598. for their assistance in identifying parasitoids. Yamamura, K. and E. Yano (1999) Effects of plant density on the survival rate of cabbage pests. Res. Popul. Ecol. REFERENCES 41: 183–188. Fushimi, T. (1993) The growth of Yamamomo (Myrica Yasuda, T. (1969) Tortricidae. In Early Stages of Japanese rubra) and the recovery of forest landschaft on the bare Moths in Color. Vol. II (S. Issiki ed.). Hoikusha, Osaka, land along the Setonaikai. Bull. Ehime Univ. For. 31: pp. 85–105 (in Japanese). 1–14 (in Japanese with English summary). Yukinari, M. (1984) Parasitoids of tortricid species in pear or- Habu, A. (1960) A revision of the Chalcididae (Hy- chards. Plant Prot. 38: 421–425 (in Japanese). menoptera) of Japan, with descriptions of sixteen new