Food Plants and Life Cycle of Lymantria Bantaizana Matsumura (Lepidoptera: Lymantriidae) in Northern Honshu, Japan

Entomological Science (2004) 7, 125–131

ORIGINAL ARTICLE

Food plants and life cycle of Lymantria bantaizana Matsumura (Lepidoptera: Lymantriidae) in northern Honshu, Japan

Tadao GOTOH,1 Paul W. SCHAEFER3 and Nobuo DOI2 1Tohoku Research Center, Forestry and Forest Products Research Institute, Morioka and 2Gokurakuno, Shizukuishi, Iwate, Japan; and 3United States Department of Agriculture, Agricultural Research Service, Beneﬁcial Insects Introduction Research Laboratory, Newark, Delaware, USA

Abstract The food plants and life cycle of Lymantria bantaizana were investigated in Iwate Prefecture, northern Honshu, Japan from 2000 to 2002. Eggs laid in July hatched approximately 10 days after oviposition. Hatched larvae fed only on Juglandaceae, Juglans mandshurica var. sachaliensis, J. regia var. orientalis and Pterocarya rhoifolia when reared in the laboratory. In field rearing, the plants of Juglans enabled the moth to complete its life cycle. Differing from all other known Lymantria species in Japan, the moth overwintered not in the egg stage but in the fifth or sixth instar larval stage. Lymantria bantaizana had eight larval instars in both sexes. Moth emergence occurred mostly in July at a field-trapping site in Iwate Prefecture. Key words: Juglans, moth emergence, overwintering, seasonal development.

INTRODUCTION MATERIALS AND METHODS Lymantria bantaizana Matsumura is a locally common Collection of eggs lymantriid moth, occurring in the north of the Chubu Four female moths were caught by a light trap in mid- district, Honshu Island, Japan (Inoue 1982; Hoya July in 2000 and 2001 at Iwashimizu (141∞9¢E, 1996). However, little is known of its biology besides 39∞43¢N), Morioka, Iwate Prefecture. They were placed adult seasonality. Zhao (1982) stated in remarks on singly in plastic cups with tissue paper, on which eggs L. bantanizana that the moth is a pest of the Persian were laid. In 2002, we obtained eggs from a female, walnut, Juglans regia, in China, but did not comment which was reared from its larval stage and mated in a on its immature stages and life cycle. gauze bag. Larvae hatched from the eggs were used for Of the nine species of Japanese Lymantria, there is no experiments. information about host plants for L. bantaizana and L. minomonis Matsumura distributed in western Japan, Laboratory and field rearing of larvae or about overwintering stages in L. bantaizana and To examine food plant preference, the foliage of 10 L. sakaguchii Matsumura occurring in the south- species of six plant families (Table 1) was offered simul- western islands (Inoue 1982; Miyata 1983). In the taneously to the hatched larvae in an insect-rearing present study, we clarified food plants of L. bantaizana plastic case (270 mm in height ¥ 410 mm in width ¥ and its life cycle by laboratory and field experiments. 230 mm in diameter) in the laboratory on 25 July 2000. Twigs bearing the foliage were inserted into small vessels filled with water to prevent leaf desiccation. The plants that larvae fed on were recorded for 1 week. Correspondence: Dr Tadao Gotoh, Tohoku Research Center, Forestry and Forest Products Research Institute, 92-25 Field experiments were conducted in the garden of Aza-Nabeyashiki, Shimokuriyagawa, Morioka, Iwate, Tohoku Research Center (141∞8¢E, 39∞45¢N) from 2001 020-0123 Japan. Email: [email protected] to 2002 to clarify whether the moth could complete its Received 28 April 2003; accepted 18 December 2003. life cycle on Juglans species, which the hatched larvae

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Table 1 Food plant preference of Lymantria bantaizana larvae Adult emergence in the field hatched during laboratory rearing To record male emergence in the field, 20 pheromone- Family Species Acceptance baited sticky traps were set up from 5 July to 19 August Oleaceae Fraxinus mandshurica – 2002 in the Siebold walnut-dominated riverain forest at Magnoliaceae Liriodendron tulipifera – Mizunashi (141∞18¢E, 39∞53¢N), Iwate Town, Iwate Fagaceae Quercus acutissima – Prefecture. The traps were checked at intervals of Quercus dentata – approximately 7 days. The chemical structure of the sex Castanea crenata – pheromone of L. bantaizana has not yet been published. Fagus crenata – We followed Satake et al. (1989) for scientific names Ulimaceae Ulmus davidiana – of Japanese plants. Juglandaceae Juglans mandshurica var. + sachaliensis Juglans regia var. orientalis + Pterocarya rhoifolia + RESULTS +, accepted; –, avoided. Food plants Hatched larvae showed distinct food preference for favored in the preference experiment. On 3 August Juglandaceae, chewing only the leaves of J. mandshurica 2001, three gauze bags (860 mm in length ¥ 480 mm in var. sachaliensis (Fig. 1C), J. regia var. orientalis and width) were prepared and 40 hatched larvae were P. rhoifolia, and did not feed on any of the other seven placed in each bag. These larvae were released on a tree species (Table 1). Of the three acceptable species, living tree of the Siebold walnut, Juglans mandshurica the larvae seemed to prefer the former two species to var. sachaliensis, by caging foliage within each bag. Ten the latter, judging from eye measurement of defoliation, hatched larvae were similarly released on Juglans regia although we did not quantify their preference. In the var. orientalis. field-rearing experiment in 2002, the hatched larvae had In 2002, the field-rearing experiment was conducted very low survival and poor growth performance on to compare suitability of food plant. On 30 July, P. rhoifolia. Survival rate was only 6.7% on P. rhoifolia, 30 hatched larvae were released on foliage of significantly less than that on the other two Juglans J. mandshurica var. sachaliensis, J. regia var. orientalis species (Fig. 2A). Furthermore, surviving larvae on and Pterocarya rhoifolia caged by a gauze bag. The P. rhoifolia and J. regia var. orientalis gained signifi- number of surviving larvae and larval fresh weights cantly less weight than those on J. mandshurica were recorded for each group on 30 August. Before (Fig. 2B). The average weight of surviving larvae was release, natural enemies of the larvae, particularly spi- only 2.5 mg (n = 2) on P. rhoifolia, while it was 18.3 mg ders, were carefully removed by shaking the foliage. (n = 27) on J. mandshurica var. sachaliensis and 12.2 mg (n = 24) on J. regia var. orientalis. Seasonal development In the field-rearing experiment, conducted from 2001 to Life cycle 2002, molted head capsules were periodically collected Eggs (Fig. 1A) hatched approximately 10 days after ovi- for the larvae in gauze bags on the trees of Juglans position. Newly hatched larvae (Fig. 1B) were black in species to estimate seasonal development. The width of color with whitish third thoracic and fifth abdominal each molted head capsule was measured to determine segments. Mature larvae (Fig. 1E) were black, dorsally the number of instars. On 4 December, 36 surviving had irregular white markings on the third thoracic seg- larvae in total were separated into two groups of 15 and ment, and had a white band along the posterior margins 21. To address overwintering sites, 15 larvae caged in a of the fourth and fifth abdominal segments. gauze bag were placed in the litter under the snow, and The molted head capsules of fourth instar larvae col- 21 larvae were similarly caged on a tree at a height of lected on J. mandshurica var. sachaliensis on 19 Septem- 1.5 m from the ground, subject to ambient tempera- ber indicated that most larvae had developed to the fifth tures. Overwintered larvae were placed again in a gauze instar by mid-September (Fig. 3). On 4 October and 4 bag set on each Juglans species on 22 April 2002, December, the larvae were found to have crawled into shortly before budding. The dates of pupation and adult folds at the base of gauze bags or inside a curled dead emergence were recorded. leaf (Fig. 1D) to overwinter, and the molted head cap-

126 Entomological Science (2004) 7, 125–131 Food plants and life cycle of L. bantaizana

Figure 1 Life stages of Lymantria bantaizana. (A) Eggs; (B) hatched larvae; (C) young larvae chewing the leaf of the Siebold walnut; (D) overwintering larva on a dead leaf; (E) mature larva; (F) pupa; (G) newly emerged male adult. sule was also found near each larva, suggesting that the ity (93.3%) occurred in the larval group overwintering larvae moved to an overwintering site, then molted and under the snow, presumably due to the wet environment overwintered there. and/or to the pressure of snow weight. Eighteen out of 21 larvae successfully overwintered In early May, the 18 overwintered larvae resumed under ambient temperatures. In contrast, heavy mortal- feeding on young leaves. Most of the 12 molted head

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Figure 2 Survival rate (A) and average weight (B) of larvae 1 month after release on different food plants. Bars with different letters are signiﬁcantly different by Bonferroni test (P < 0.01) for survival rate and by Kruskal–Wallis test with non-parametric Tukey-type multiple comparison (P < 0.05) for weight. J.m, Juglans mandshurica var. sachaliensis (n = 27); J.r, Juglans regia var. orientalis (n = 24); P.r, Pterocarya rhoifolia (n = 2). Vertical lines indicate 95% conﬁdence limits.

Figure 3 Seasonal changes in size of molted head capsules collected in the rearing bags on Juglans mandshurica var. sachaliensis in Morioka, Iwate Prefecture on (A) 22 June; (B) 22 May; (C) 4 October (n = 4) and 4 December (n = 24) (these data were combined because the larvae on both of these days were in the stage of overwintering); (D) 19 September; (E) 3 September; and (F) 20 August. *In each of these instars, several of the smallest and largest head capsules might be from the preceding instar and the following instar, respectively.

128 Entomological Science (2004) 7, 125–131 Food plants and life cycle of L. bantaizana

Figure 5 Trap catches of male moths in Mizunashi, Iwate Pre- fecture (n = 160).

These 10 larvae then pupated between 25 June and 4 July (Fig. 1F) without further molting. It was impossible to measure the molted head capsules of eighth instar larvae, because they normally split open during pupation. Finally, four males (Fig. 1G) and six females emerged between 14 and 19 July. On J. regia var. orientalis, the developmental stages were clearly traced (Fig. 4). Only two larvae had sur- vived by 4 October and overwintered. Two molted head capsules of fifth instar larvae on 27 May indicated that the larvae overwintered at the fifth instar stage. After overwintering, they molted three times to become eighth instar larvae, then pupated (Fig. 4). Finally, one male Figure 4 Seasonal changes in size of molted head capsules and one female adult emerged on 17 July and 24 July, collected in the rearing bag on Juglans regia var. orientalis in respectively. Morioka, Iwate Prefecture on (A) 3 July; (B) 27 May; (C) 4 In the field, male adults were caught mostly in July October; (D) 19 September; and (E) 20 August. Instars were of molted head capsules. with a peak toward the end of the month (Fig. 5). More than 80% of the total was caught between 20 July and capsules collected on 22 May and the smallest five cap- 2 August. Fifty percent of the total trap catch occurred sules collected on 22 June were determined by size to between 20 and 26 July. be from sixth instar larvae, indicating that most larvae overwintered at the sixth instar stage. However, the DISCUSSION smallest two head capsules on 22 May overlapped with those of fifth instar larvae in size, within a range of Our results on food preference indicate that 1.75–1.90 mm (Fig. 3), indicating the possibility that a L. bantaizana favors only Juglans species. Although the few larvae overwintered at the fifth instar stage. hatched larvae also chewed the leaves of P. rhoifolia, the As some larvae escaped by eating holes in the gauze low survival rate on these leaves and very slow growth bags, only 10 larvae remained on 22 June. They were of larvae suggest that this plant is not a suitable food. considered to be eighth instar, because nine molted head In addition, it was demonstrated that J. mandshurica capsules larger than 2.85 mm collected on the same date var. sachaliensis and J. regia var. orientalis enabled the were determined by size to be of seventh instar (Fig. 3). moth to complete its life cycle. Therefore, we consider

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Figure 6 Estimated life cycle of Lymantria bantaizana on Juglans mandshurica var. sachaliensis in Mori- oka, Iwate Prefecture. that Juglans species could be the only host plants for larvae overwinter on trees, possibly staying in crevices L. bantaizana in nature. Juglans regia var. orientalis is, or under loose outer bark. however, not native to Japan, having been introduced It was demonstrated in the present study that from China in the 18th century (Shimura et al. 1989). L. bantaizana had eight larval stages both on The original host plant for L. bantaizana in northern J. mandshurica var. sachaliensis and on J. regia var. ori- Honshu may be J. mandshurica var. sachaliensis. To entalis. This number of instars seems great among draw a conclusion on host plants, direct observation of lymantriid moths, considering that five to seven instars larval feeding in the field is necessary. In addition, occur in Lymantria dispar on its favored host plants Juglans mandshurica var. cordiformis growing naturally (Igarashi 1982; Nagasawa 1988), and five to seven in the Chubu district and Platycarya strobilacea in west- instars occur in Lymantria monacha (Linnaeus) (Beijer ern Japan should be investigated to determine the full 1988). While rearing Lymantria serva Fabricius from extent of host plants. Taiwan in Newark, larvae successfully completed Larvae taken to the US Department of Agriculture in between seven and nine molts, indicating up to 10 Newark, DE, USA readily accepted foliage of Juglans instars in this Ficus feeder (P. W. Schaefer, unpublished nigra, and most of them successfully completed devel- data, 1999). In the present study, the emergence dates opment to adult stage (P. W. Schaefer, unpublished data, of the adults raised in the field-rearing experiment were 2002). Therefore, J. nigra would seem to be another coincident with those in the field, demonstrated by the acceptable food species. pheromone trap catch in Mizunashi. This result suggests Considering that J. mandshurica var. sachaliensis is that the larvae reared in the field successfully developed widely distributed throughout Japan (Yamazaki 1989), without a prolonged larval period. Thus, eight larval L. bantaizana may also inhabit Hokkaido and western instars seem to be usual and common to L. bantaizana. Japan, where there has been no record of occurrence. In Although the normal oviposition site for L. ban- mid-August 2002, the moth was discovered in Hok- taizana is still unknown, a mated female deposited her kaido, using the same pheromone traps as those used fertilized eggs on a branch in the field-rearing experi- for monitoring in the present study (P. W. Schaefer, ment (Fig. 1G). Thus, there is a possibility that females unpublished data, 2002). in nature lay their eggs on branches and even on leaves Our studies on the life cycle of L. bantaizana demon- of host plants. strated that it overwintered not in the egg stage but in The result of male catch by pheromone traps in the the larval stage. The results of head capsule sizing indi- field indicates that moth emergence occurs with a single cated that the larvae overwintered at the stage of fifth peak from early July to early August in Iwate Prefecture. or sixth instar. Seven out of nine species of Japanese The life cycle of L. bantaizana in Iwate Prefecture Lymantria have been known to overwinter as eggs is summarized in Figure 6. Although the life cycle in (Miyata 1983); thus, overwintering in the larval stage nature still remains uncertain, it could be clarified appears to be a unique feature of the life cycle of through periodical sampling of larvae on foliage or sam- L. bantaizana. The high survival rate of larvae exposed pling of molted head capsules by frass traps throughout to ambient temperatures in winter may suggest that the larval feeding season in the Siebold walnut-

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dominated forest. The findings from our study should of the Japanese Forestry Society] 64, 486–490. (In be useful in planning such sampling schedules. Japanese.) Inoue H (1982) Lymanatriidae. In: Inoue H, Sugi S, Kuroko H, Moriuti S, Kawabe A (eds) [Moths of Japan, I], ACKNOWLEDGMENTS pp 628–638. Kodansha, Tokyo. (In Japanese.) Miyata A (1983) [Handbook of the Moth Ecology – Moths We thank Dr Gerhard Gries (Simon Fraser University, as an Indicator of the Environment]. Showado Printing Burnaby, Canada) for providing us with synthesized sex Publishing Division, Nagasaki. (In Japanese.) pheromone of Lymantria bantaizana. The Morioka Nagasawa S (1988) Number of larval instars of the gypsy Rural Development Office of Iwate Prefecture permitted moth in Japan (Lepidoptera: Lymantriidae). Applied Entomology and Zoology 23, 441–448. us to use the riverain forest for our field study. Satake Y, Hara H, Watari S, Tominari T (1989) [Wild Flowers of Japan – Woody Plants.] Heibonsha, Tokyo. (In Japanese.) REFERENCES Shimura I, Hotta M, Ogata K (1989) Juglans. In: Hotta M, Ogata K, Nitta A, Hoshikawa K, Yanagi M, Yamazaki K Beijer B (1988) The nun moth in European spruce forests. In: (eds) [Useful Plants of the World], pp 571–573. Heibon- Berryman AA (ed) Dynamics of Forest Insect Populations sha, Tokyo. (In Japanese.) – Patterns, Causes, Implications, pp 211–231. Plenum Yamazaki K (1989) Juglandaceae. In: Satake Y, Hara H, Press, New York. Watari S, Tominari T (eds) [Wild Flowers of Japan – Hoya T (1996) Lymantriidae of Miyagi. In: Insects of Woody Plants], pp 29–30. Heibonsha, Tokyo. (In Miyagi 14, pp 1–79. T. Hoya, Ishinomaki, Miyagi. (In Japanese.) Japanese.) Zhao ZL (1982) Lymantriidae. In: [Iconographia Heterocer- Igarashi Y (1982) [Life history of Lymantria dispar Linne orum Sinicorum, II], pp 163–190. Science Press, Beijing. (Lepidoptera: Lymantriidae) in Kochi, Shikoku.] [Journal (In Chinese.)

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