Life history of Adalia bipunctata ( Coleóptera : Coccinellidae ) in Japan

Adalia bipunctata is a well-known predaceous ladybird distributed in Europe, Central Asia and North America. This spe­ cies has not been recorded in Japan. Recently, we found this species in the Osaka Bay area in central Japan, and assume that it was imported with goods such as timber by ships. We studied the life history and the distribution in the Osaka Bay area since the initial discovery. The larvae and adults preyed on aphids (mainly, Periphyllus viridis) on trees such as Acer buergerianum and Rhaphiolepis umbellata. The over-wintered adults appeared in March and laid eggs. The adults emerged in spring, and were in the rolled leaves throughout the rest of the year. Thus, in Japan this ladybird is univoltine with long inactivity in adult. The life history of Japa­ nese population of A. bipunctata differs considerably from other areas where populations are multivoltine. The developmental threshold was estimated to be 6.3°C and the sum of effective temperatures was 322.6 day-degrees for the period from egg to adult emergence. Predation on prepupae of A. bipunctata by the larvae of native species such as Harmonia axyridis was observed occa­ sionally.

This ladybird had not been reported from Japan, although ten ladybird species (most of them may be immigrants) were recently recorded (Sasaji, 1992).We first discovered one A. bipunctata adult on 16th December 1993 in Osaka Bay area, Japan (Sakuratani, 1994).This adult overwintered under the bark of a dead tree in a park.The following spring active indi viduals of A. bipunctata were observed in the park.
Recently, several predaceous coccinellid species, for exam ple Harmonia axyridis (Pallas) and C. septempunctata were introduced to Europe or North America,respectively (e.g.; Ted ders & Schaefer, 1994).They are competing there with the native species such as A. bipunctata.
We are investigating the life history, population dynamics and the inter-species relationships of A. bipunctata with the native coccinellid species in Japan.In this paper, we report on the life history in Japan.

Field observations
The seasonal occurrence of the developmental stages of A. bipunctata was observed in the Central Park of Osaka Nanko (34.6°N, 135.4°E; alt. 5 m a.s.l.; area of 25 ha) Osaka City, Osaka Pref., Japan, from 1996 to 1999.The census was carried out on trees such as maple, Acer buergerianum Miquel and grasses applying a transect method 1-4 times per month or sea son.The presence and behavior of native ladybirds on these plants were also recorded.The number of adults aestivating and overwintering was checked in each site.

Laboratory study
Progenies from several A. bipunctata females were reared under four constant temperatures of 15 ± 1, 20 ± 1, 25 ± 1 and 30 ± 1°C, the relative humidity of about 70%, and a photoperiod of 14L : 10D.Several aphid species, mainly Periphyllus viridis (Matsumura) infesting a maple tree, A. buergerianum, were fed to larvae and adults.The developmental zero and the sum of effective temperatures were calculated.

Field observations
The percentages of each developmental stage found in four years are shown in Fig. 1.The eggs are not included, because it was difficult to distinguish them from those of native cocci nellid species such as Menochilus sexmaculatus (F.).Mating and oviposition of A. bipunctata was observed in late March and April in each year.Egg masses were found only in spring.Larvae appeared from mid April to late May.They preyed on aphids, P. viridis on A. buergerianum, and other aphids infesting shrubs such as Rhaphiolepis umbellata Makino and Hibiscus syriacus L.
Pupae were found attached to leaves of maple, R. umbellata and other trees during May and early June, and often aggregated on leaf (Fig. 2).In spite of aggregations, cannibalism to pre pupae or pupae by the larvae or adults of A. bipunctata was not found, although we looked for it.However, on the several trees the larvae of H. axyridis preyed often on the prepupae or pupae of A. bipunctata in each year (Fig. 3).
The newly emerged adults were observed each year in early May preying on aphids on the maple and other trees.They appeared to enter aestivation in mid June.They were dormant in "webs" made by spiders or caterpillars or between overlapped leaves or in rolled leaves of maple, evergreen oak and other trees (Fig. 4).There were one to ten aestivating adults in one site.
Adult A. bipunctata was inactive through the summer, but some adults preyed on aphids in autumn.However, no eggs or larvae were observed during the summer and autumn.The adults apparently entered aestivation and hibernation diapause.The overwintering sites were in the webs on evergreen oak, like in aestivation, but some individuals were found under the bark of live A. buergerianum.Some inactive adults in the webs observed at a census time were not found next time (after sev- In Japan, the dark forms (Hodek & Honek, 1996) of adult of this ladybird were very rare (less than 1%), and almost all were the typical two-spot form in each year.

Developmental period
Figure 5 shows the developmental periods under four constant temperatures.The developmental zero was 8.2, 4.8, 7.5, 6.3°C for egg, larva, pupa and egg-adult emergence, respectively (Table 1).The sum of effective temperatures was 43.9, 192.3, 86.2, 322.6 day-degrees, for egg, larva, pupa and the period from egg to adult emergence, respectively (Table 1).No females laid eggs at 15 and 30°C.The preoviposition periods were 24.6 days at 20°C and 29.9 days at 25°C.

DISCUSSION
In Osaka City, Japan, A. bipunctata is univoltine with spring breeding.Immature stages and newly eclosed adults are only observed in the spring.The adults are inactive from summer to  next spring, though some adults actively fed in the autumn but did not reproduce.The life history type of A. bipunctata in Japan is aestivo-hibernation (Hagen, 1962).In North America and Eurasia, this ladybird is typically multivoltine (Hodek & Honek, 1996), though in Finland it is univoltine with summer breeding (Hamalainen, 1976).
This ladybird was first discovered in Japan near an interna tional harbor.This species overwinters in aggregations under the bark of the wood and other sites (Hemptinne,1985;Hodek & Honek, 1996).A. bipunctata may have been introduced in winter with logs, but the original distribution area cannot be  The number of individuals fluctuated among years, and some individuals were attacked by native coccinellids, especially H. axyridis.However, A. bipunctata bred continuously for the six years of the study.In North America or Europe, H. axyridis or C. septempunctata were introduced to control aphids and many studies on these species were carried out (e.g.; Tedders & Schaefer, 1994;Coderre et al., 1995;Dreistadt et al.,1995;Kidd & Nalepa, 1995;Phoofolo & Obrycki, 1995).The number of H. axyridis increased every year, and causes strong competition with native species (Horn, 1999).In Japan, prepupae and pupae of A. bipunctata were often eaten by the larvae of native species such as H. axyridis.The developmental zero of A. bipunctata is 6.3°C and the sum of effective temperatures is 322.6 daydegrees for the period from egg to adult emergence.These values are smaller than those of H. axyridis (Kawauchi, 1979).In Japan both species start breeding in spring.
In each year A. bipunctata was in the prepupal or pupal stage, when H. axyridis was in larval stage.On the same trees the pre-

Fig. 1 .
Fig.1.Seasonal changes of percentage of developmental stages of Adalia bipunctata in Japan, based on the relative abundance in the transect census.Eggs are not shown because of the difficulty of identification.eral weeks); apparently due to our disturbance adults moved to other sites.In Japan, the dark forms(Hodek & Honek, 1996)  of adult of this ladybird were very rare (less than 1%), and almost all were the typical two-spot form in each year.Developmental periodFigure5shows the developmental periods under four constant temperatures.The developmental zero was 8.2, 4.8, 7.5, 6.3°C for egg, larva, pupa and egg-adult emergence, respectively

Fig. 2 .
Fig. 2. Aggregation of pupae of A. bipunctata attached on a maple leaf.Fig. 3. Predation on prepupa of A. bipunctata by a larva of native ladybird, Harmonia axyridis.

Fig. 4 .
Fig. 4. Inactive adults of A. bipunctata aestivating in the leaf with web made by spider.
determined.The distribution of this ladybird has not yet spread over Japan; still it has been found only in the Central Park of Osaka Nanko (area of 25 ha), Osaka City.

Table 1 .
Developmental threshold (to) and total effective tem perature (K) in Japanese population of Adalia bipunctata.