Appl. Entomol. Zool. 40 (3): 447–456 (2005) http://odokon.ac.affrc.go.jp/

Effects of photoperiod and temperature on adult oligopause of and larval diapause of A. albipodus (: )

Eriko TATSUMI* and Hajimu TAKADA† Laboratory of Applied Entomology, Graduate School of Agriculture, Kyoto Prefectural University; Kyoto 606–8522, Japan (Received 22 November 2004; Accepted 18 March 2005)

Abstract The effects of photoperiod and temperature on the dormancy of two aphid parasitoids in Japan, Aphelinus asychis and A. albipodus, were studied in the laboratory. Adult (reproductive) dormancy was induced in A. asychis under 10L : 14D at moderate temperatures and under 15L : 9D at low temperatures. Dormant adults started oviposition 6–17 d after emergence under 10L : 14D at 15 and 18°C. Transferring newly emerged adults from 10L : 14D at 15 and 18°C to 15L : 9D at 20°C caused an apparent reversal of dormancy induction within 1–2 d. It was believed that adult dormancy in A. asychis conforms to “oligopause” rather than “diapause” sensu Mansingh (1971). Adults of A. asychis showed an apparent variation in abdominal coloration from yellowish brown to black. The proportion of females with dark abdominal coloration was higher under 10L : 14D than under 15L : 9D and high at lower temperatures. We re- garded this polyphenism as a part of the “diapause syndrome” because oligopause and abdominal coloration were controlled by the same environmental factors. Aphelinus albipodus entered diapause as last instar larvae. The critical photoperiod for diapause induction was 11–12 h at 18°C, and diapause was terminated within six weeks by cold treat- ment (10L : 14D, 5°C).

Key words: Aphelinus asychis; A. albipodus; diapause; oligopause; body coloration

moderate temperatures. Aphelinus sp. near varipes INTRODUCTION from the Ukraine entered diapause as “mummies” It is important to know the dormancy character- under 12L : 12D at 14°C (Prinsloo and du Plessis, istics of parasitoids for understanding their effec- 2000). (Dalman) over-win- tiveness as biological control agents against pest tered usually as pupae and occasionally as adults in . Particularly, the characteristics pertaining England (Wahab, 1985). Aphelinus thomsoni Gra- to the induction, maintenance and termination of ham (as A. flavus Thomson) over-wintered as last dormancy determine not only the usability of the instar larvae within mummified aphids (mummies) parasitoids in autumn and winter, but also their in the Czech Republic (Stary, ´ 1970), but as free- storage term. Aphid-parasitizing aphelinids, the living adults in Scotland (Hamilton, 1973). Al- most common genus of which is Aphelinus, is one though the term “diapause” was not used, A. thom- of the principal natural enemies of aphids. Apheli- soni probably entered adult (reproductive) diapause nus mali (Haldeman) over-wintered as the diapaus- in Scotland because over-wintering females did not ing last instar larvae in the Netherlands (Trimble et contain mature eggs (Hamilton, 1973). Thus, the al., 1990). Aphelinus varipes (Foerster) from south- over-wintering diapause stage differs among the ern Alberta (Yu, 1992, as Aphelinus sp. near species in the genus Aphelinus. In contrast, A. asy- varipes), and A. albipodus Hayat and Fatima from chis Walker (as A. semiflavus Howard), which was Kazakhstan (Yu, 1992, as A. varipes) and western introduced from the Middle East, manifested dia- China (Bernal et al., 2001) entered diapause as the pause neither in California (Schlinger and Hall, last instar larvae under short-day conditions and 1959) nor under a 12-h photoperiod at a low tem-

*To whom correspondence should be addressed at: E-mail: [email protected] † Present address: 40 Ogura-cho, Kitashirakawa, Sakyo-ku, Kyoto 606–8264, Japan DOI: 10.1303/aez.2005.447

447 448 E. TATSUMI and H. TAKADA perature in the laboratory (Force and Messenger, tal stage sensitive to dormancy-inducing cues and 1964). the role of photoperiod on the maintenance and ter- Aphelinus asychis and A. albipodus are suitable mination of dormancy in A. asychis, to discuss the for principal pest aphids on greenhouse vegetable characteristics of adult dormancy of this parasitoid, crops in Japan (Takada, 2002; Tatsumi and Takada, (2) the critical photoperiod for dormancy induction 2005), and are candidates for indigenous biological and the effects of cold treatments on dormancy ter- control agents. Preliminary experiments in the lab- mination in A. albipodus, and (3) the potentials of oratory indicated that A. asychis entered dormancy A. asychis and A. albipodus as biological control as adults, but A. albipodus entered dormancy as agents. last instar larvae under short-day conditions. When A. asychis was reared under 15L : 9D or 10L : 14D MATERIALS AND METHODS at 18°C, adults emerged from mummified aphids in either case, but conspicuous differences were cultures. Table 1 shows the origins of A. found in the ovarian developmental stage and ab- asychis and A. albipodus used in the present study, dominal coloration of the emerged adults. Emerged and Table 2 shows the species of host aphids, their adults reared under 15L : 9D had mature eggs and a host plants, and cages for rearing in respective ex- medium brown abdomen, whereas those under periments and stock cultures. Reproductive cate- 10L : 14D had no visible oocytes and the abdomen gories (Blackman, 1971) of the clones of the two was dark brown. Photoperiodic control of adult host aphids used in the present experiments were diapause has been demonstrated in only a few confirmed by preliminary experiments: Myzus per- species of hymenopterous parasitoids (Numata, sicae (Sulzer): intermediate, Acyrthosiphon pisum 1993). (Harris): anholocyclic. Two types of glass tube In this study, we examined (1) the effects of pho- cages containing excised leaves of the host plant toperiod at various temperatures on dormancy in- were used in the present experiments. Stock cul- duction and abdominal coloration, on developmen- tures of these parasitoids were maintained in plas-

Table1. Collection data for two Aphelinus species used in the present study

Parasitoid Localitya Date Host aphid Host plant (Population)

A. asychis Kyoto, Kyoto June 1997 Aphis gossypii Cucumis sativus (Kyoto) A. albipodus (Kobe) Kobe, Hyogo May 1996 Uroleucon nigrotuberculatum Solidago altissima (Kyoto) Kyoto, Kyoto September 2001 U. nigrotuberculatum S. altissima

a Municipality, prefecture.

Table2. Rearing of two Aphelinus species in the experiments and stock cultures

Experiment Stock culture Parasitoid (Population) No. Host aphid Host plant Cagea Host aphid Host plant Cageb

A. asychis 1-1,3, 4, 5 M. persicae (I) Rs H Aphis craccivora Koch Vf A (Kyoto) 1-2 A. pisum (A) Vf L A. pisum Vf A A. albipodus (Kobe) 2-1 M. persicae (I) Rs H M. persicae Rs B (Kyoto) 2-2 A. pisum (A) Vf L A. pisum Vf A

a Glass tube cage H: 3.5 cm dia.15 cm height, cage L: 5 cm dia.10 cm height. b Plastic ventilated cube-cage A: 202030 cm height, cage B: 202020 cm. I: Intermediate clone. A: Anholocyclic clone. Rs: Raphanus sativus ‘Tokinashi.’ Vf: Vicia faba var. minor. Dormancy of Two Aphelinus Species 449

Fig. 1. Developmental stages of oocytes in the most mature ovariole in 0–1-d-old adults of A. asychis. Immature; no externally visible oocytes, intermediate 1–3; one or two developing oocytes with some yolk, and mature; at least one mature egg. tic ventilated cube-cages containing potted young opment of the ovary was classified into five stages: plants infested with aphids under 15L : 9D at 18°C. immature, intermediate 1–3 and mature as shown General procedure. To obtain aphids of the in Fig. 1. The absence of externally visible oocytes same age, we released apterous viviparous female (immature) was used as the criterion for reproduc- adult aphids into a glass tube cage with leaves of tive dormancy and the presence of mature egg as the host plant for 24 h and then removed the adult. the criterion for reproductive activity. Abdominal Three- to 4-d-old nymphs of M. persicae and 1- to coloration of newly emerged females was classified 2-d-old nymphs of A. pisum were offered to para- into five categories: yellowish brown, medium sitoids in the experiments. One or two female para- brown, dark brown, brownish black and black. sitoids from the stock culture were released for Characteristics of adult dormancy of A. asy- 24 h into a glass tube cage containing about 30 chis. Effects of photoperiod on dormancy induction nymphs of the test aphid under 15L : 9D at 18°C. at 18°C. Aphids exposed to the mated females of After parasitoids were removed, the aphids in the A. asychis were reared under 10L : 14D, 11L : 13D, cage were reared until mummification under the 11.5L : 12.5D, 12L : 12D and 15L : 9D at 18°C. same conditions. Mummified aphids were put indi- Newly emerged female adults were dissected and vidually into small glass vials and checked for the developmental stages of their ovaries were eval- emergence of adults every day. The emerged para- uated. sitoids (0–1-d old) were sorted by sex, and one fe- Effects of photoperiod and temperature on male and one male were introduced together into a dormancy induction and abdominal coloration. small glass vial equipped with a honey droplet and Aphids exposed to mated females of A. asychis were allowed to mate. The mated female (1–2-d were reared under 15L : 9D at 10, 15 and 20°C, and old) was released for 24 h into the cage containing under 10L : 14D at 15, 20 and 25°C. The abdomi- 30 aphids under 15L : 9D at 18°C for oviposition. nal coloration and ovarian developmental stages of After removal of the parasitoids, the aphids were newly emerged females were recorded. exposed to each photoperiod at designated temper- Estimation of preimaginal stages sensitive to the ature conditions. factors for dormancy induction. Aphids exposed to Ovarian development and abdominal col- mated females of A. asychis were reared under oration of A. asychis. The degree of reproductive 15L : 9D and 10L : 14D at 18°C, and transferred to maturity in newly emerged female adults (0–1-d the opposite photoperiodic condition at intervals of old) was examined by dissecting them under a three days. The developmental stages of the para- binocular stereomicroscope. Each ovary was com- sitoids were estimated from the developmental posed of three ovarioles. As development was not rates at respective photoperiodic conditions at always synchronized, the most mature ovariole was 18°C (Tatsumi, unpublished data). The ovarian de- estimated according to the number of oocytes, the velopmental stages of the newly emerged female size of the greatest oocytes in vitellogenesis and adults were evaluated. the presence or absence of mature eggs. The devel- Effects of photoperiod during the adult stage on 450 E. TATSUMI and H. TAKADA dormancy induction, maintenance and termination. within 4 wk after mummification, were dissected, First, to verify the effects of the photoperiod given and the life or death and developmental stages of during the adult stage on dormancy induction, we the parasitoids within the mummies were exam- transferred mated female adults (1–2-d old) of A. ined. Live last instar larvae were regarded as dor- asychis grown under 15L : 9D at 18°C to 10L : 14D mant larvae. The percentage of dormancy was cal- at 18°C, and released them individually into glass culated: [Number of mummies containing a live tube cages containing 30 aphids. Each female was parasitoid larva/(Number of mummies examined transferred to a new cage containing 30 aphids Number of mummies containing a dead larva)] every 24 h until it died. Aphids killed by host feed- 100. ing were counted at the time and the remaining Effects of cold treatment on subsequent post- aphids were dissected three days later to determine dormant development. Aphids exposed to mated the daily fecundity of the parasitoid. Second, to females of A. albipodus were reared under verify the effects of short days on dormancy main- 10L : 14D at 18°C until mummification. Mummi- tenance, we kept some mated female adults (1–2-d fied aphids were removed and placed individually old) grown under 10L : 14D at 15 and 18°C under in small glass vials. Five groups of about 100 the same conditions. The number of eggs deposited mummies were kept under 10L : 14D at 5°C for 1, and aphids killed by parasitoids were examined 2, 4, 6 and 8 wk, and then transferred to 15L : 9D at until they died as in the preceding experiment. 20°C. Another group of 55 mummies was trans- Third, to verify the effects of long days on dor- ferred to 15L : 9D at 20°C immediately after mum- mancy termination, we transferred mated female mification without any cold treatment. The mum- adults (1–2-d old) grown under 10L : 14D at 15 and mies were checked for the emergence of adult par- 18°C to 15L : 9D at 20°C, and examined the num- asitoids every day, and the emergence rate was cal- ber of eggs deposited and aphids killed by para- culated for each group: (Number of emerged sitoids for 14 d as in the preceding experiment. The adults/Number of mummified aphids)100. corresponding values by parasitoids reared The difference in the time to emergence of throughout their lifetime on Macrosiphum euphor- adult parasitoids was statistically analyzed using biae under 15L : 9D at 20°C (Thomas) (Tatsumi Kruskal-Wallis’ test, and if significant differences and Takada, unpublished) were cited for compari- were detected, the difference among the means was son. Mann-Whitney’s U-test was used for compar- analyzed according to the Steel-Dwass procedure. ing the daily number of eggs deposited and aphids The difference between females and males in the killed by parasitoids. time to emergence was analyzed using the Mann- Survival rate of long day-reared and short day- Whitney U-test. Emergence rate was analyzed reared females during cold treatment. Mated fe- using the chi-square test, followed by multiple males (1–2-d old) of A. asychis grown under comparisons of treatment values using the Tukey 15L : 9D at 18°C and 10L : 14D at 15°C were procedure. placed individually in small glass vials equipped with drops of water, and kept under 10L : 14D at RESULTS 5°C for 8 wk. These females were checked for life or death and water was resupplied every week. The Characteristics of adult dormancy of A. asychis survival rate [(number of surviving females/num- Effects of photoperiod on dormancy induction at ber of females examined)100] after 8 wk was an- 18°C. Short days induced reproductive dormancy alyzed using the chi-square test. (Fig. 2). The critical photoperiod, at which 50% of Characteristics of larval dormancy of A. al- females entered dormancy, was between 11 and bipodus. Effects of photoperiod on dormancy in- 11.5 h at 18°C. duction at 18°C. Aphids exposed to mated females Effects of photoperiod and temperature on dor- of A. albipodus were reared under 10L : 14D, mancy induction and abdominal coloration. The 11L : 13D, 12L : 12D and 15L : 9D at 18°C. Mum- reproductive dormancy was induced by the short- mified aphids were placed individually in small day photoperiod, but the induction was strongly glass vials and the emergence of adults was every suppressed at temperatures of 20 and 25°C (Fig. 3). day. Mummies, from which adults did not emerge Dormancy was induced even under long-day pho- Dormancy of Two Aphelinus Species 451

Fig. 2. Effects of photoperiod at 18°C on ovarian devel- opment of A. asychis. Numbers in parentheses above the col- umn show sample size.

Fig. 4. Effects of photoperiod and temperature on abdom- inal coloration of female adults of A. asychis. Numbers in parentheses above the column show sample size.

for dormancy induction. Preimaginal stages, at least from the second instar larva to pupa, were widely sensitive to a dormancy-inducing photope- riod (Fig. 5). The critical stage, if defined as the stage at which 50% of females entered dormancy, was the last instar larval stage when transferred from long-day conditions to short-day conditions, although it was the middle pupal stage when trans- ferred from short-day conditions to long-day con- ditions (Fig. 5). Fig. 3. Effects of photoperiod and temperature on ovarian Effects of photoperiod during the adult stage on development of A. asychis. Numbers in parentheses above the dormancy induction, maintenance and termination. column show sample size. When females grown under 15L : 9D at 18°C were transferred to 10L:14D at 18°C on emergence, all toperiods at 10°C (Fig. 3). The proportion of fe- five females (f–j) started to oviposit 1–2 d after male adults with immature ovaries was higher emergence (Fig. 6B) as in the females (a–e) reared under 10L : 14D at 18°C (Fig. 2) than 10L : 14D at throughout their lifetime under 15L : 9D at 20°C 15°C (Fig. 3). There is a possibility that the capac- (Fig. 6A). All the females (f–j) killed aphids by ity to respond to the photoperiod in the host aphids host feeding almost every day throughout their life- used in the experiments differed (Table 2) and un- time as in the females (a–e). There was no clear ev- known host factors influenced the response of the idence to support the theory that dormancy was in- parasitoid to the photoperiod. The frequency of duced by the short-day conditions given during the darker abdominal coloration was higher under adult stage. short-day conditions than long-day conditions and When females were reared under 10L : 14D at 15 at low temperatures (Fig. 4). or 18°C throughout their lifetimes, the four females Developmental stage sensitive to photoperiod (k–n) grown at 15°C started to oviposit at 8–9 days 452 E. TATSUMI and H. TAKADA

Fig. 5. Ovarian development of newly emerged A. asychis when transferred at various developmental stages from 15L : 9D to 10L : 14D (A) and from 10L : 14D to 15L : 9D (B) at 18°C. Numbers in parentheses at the left of the column show sample size.

Fig. 6. Survival rate and individual oviposition period of female adults, and cumulative number of eggs deposited and aphids killed by female adults of A. asychis. Small solid and open circles indicate the day on which a female deposited at least one egg. A: Females were reared under 15L : 9D throughout their lifetimes, B: Mated females (1–2-d old) grown under 15L : 9D were trans- ferred on emergence to 10L : 14D, C: Females were reared under 10L : 14D throughout their lifetimes, D: Mated females (1–2-d old) grown under 10L : 14D were transferred to 15L : 9D one day after emergence of adults. Dormancy of Two Aphelinus Species 453

Fig. 7. Survival rate of female adults of A. asychis during Fig. 8. Photoperiodic response for larval dormancy induc- cold treatment at 5°C (10L : 14D). Open circle: Females grown tion of A. albipodus at 18°C. Numbers in parentheses near the under 15L : 9D at 18°C, solid circle: Females grown under plot show sample size. 10L : 14D at 15°C. and the four females (o–r) grown at 18°C 6, 9, 13 Table3.Effect of duration of exposure to 10L : 14D at 5°C on subsequent post-diapause development of and 17 d after emergence, but the oviposition was A. albipodus under 15L : 9D at 20°C intermittent (Fig. 6C). The mean daily fecundity of the females (o–r) (meanSD: 2.02.0) was lower Duration Time to emergencebc Emergence of cold (days, meanSD) than that of the females (f–j) grown under 15L : 9D ratea treatment at 18°C (4.11.0) (Fig. 6B), although the differ- (%) ence was not significant (p0.05). The daily fe- (wk) Female Male cundity of the female group (o–r) was not signifi- 0 63.6 b 66.1 7.0 a (23) 56.3 9.2 a* (12) cantly different (p0.05) from that of the female 1 82.1 a 63.510.2 a (56) 57.910.6 a* (34) group (k–n) (2.00.7). The daily number of aphids 2 84.0 a 58.010.3 b (71) 52.6 6.5 a* (18) killed by the female group (o–r) (0.60.2) was not 4 84.5 a 34.315.4 c (52) 26.7 8.4 b (34) significantly different (p0.05) from that of the fe- 6 84.9 a 20.7 4.7 d (55) 18.4 4.1 c* (37) 8 86.0 a 18.3 2.0 e (54) 17.0 2.1 c* (33) male group (f–j) (1.10.3) or female group (k–n) (0.5 0.1). Adult dormancy could not be main- a The values in the same column followed by the same letter tained for a long period under short-day conditions are not significantly different (p0.05, Tukeys procedure). at 15 or 18°C. b Means in the same column followed by the same letter are When females grown under 10L : 14D at 15 and not significantly different at 5% level by Steel-Dwass’ proce- 18°C were transferred to 15L : 9D at 20°C on dure. c Numbers in parentheses show the number of emerging para- emergence, the four females (s–v) grown at 15°C sitoids. started ovipositing in 1–2 d, and the four females * Means are significantly different between females and males (w–z) grown at 18°C 1, 2 or 3 d after emergence at 5% level by Mann-Whitney’s U-test. (Fig. 6D). The daily fecundity and daily number of aphids killed during the first 14 d by the female rate after cold treatment for 8 wk was significantly group (s–v) (meanSD: 9.13.6 and 0.70.5, re- higher (p0.05) in short day-reared females (83%) spectively) and the female group (w–z) (12.33.2 than in long day-reared females (41%) (Fig. 7). and 1.40.3) were not significantly different (p0.05) from those by female group (a–e), which Characteristics of larval dormancy of A. albipo- was grown under 15L : 9D at 20°C throughout their dus lifetimes (9.42.4 and 1.30.3) (Fig. 6A). The Effects of photoperiod on dormancy induction at laying of eggs was immediately induced when the 18°C. The percentage of dormancy decreased as females were transferred to long-day conditions at the photoperiod increased (Fig. 8). The critical 20°C. photoperiod was between 11 and 12 h. Survival rate of long day-reared and short day- Effects of cold treatment on subsequent post- reared females during cold treatment. The survival dormant development. The emergence rate was sig- 454 E. TATSUMI and H. TAKADA nificantly higher (p0.05) in the groups with development soon after being transferred to 1–8 wk cold treatments (82%) than that without 15L : 9D at 20°C (Fig. 6D). Therefore, we thought treatment (64%) (Table 3). Adults without cold that adult dormancy in A. asychis conformed to treatment emerged after about 2 mo. The time to “oligopause”. emergence shortened as the duration of cold treat- Hamilton (1973) stated that second-generation ment increased: about 2 mo after 1- or 2-wk treat- A. thomsoni adults, which emerged in September, ment, about 1 mo after a 4-wk treatment, and about did not oviposit and some of them survived until 20 d after 6- and 8-wk treatment (Table 3). Three May of the next year in Scotland. Furthermore, the and four weeks seem to be critical periods of cold author suggested that first-generation adults, which treatment for accelerated post-dormant develop- emerged in July, were also capable of overwinter- ment. The difference in the time to emergence be- ing. Judging from this description, A. thomsoni tween the groups cold-treated for 6 and 8 wk was may be different from A. asychis in the level of re- significant (p0.05) in females but not in males productive inactivity. Star´y (1970) stated that the (Table 3). adaptation of parasitoids to the lifecycles of their hosts was generally of two main types, i.e., dor- mant states in development and wider host range. It DISCUSSION seems that A. thomsoni, which is specialized to Characteristics of adult dormancy of A. asychis Drepanosiphum platanoidis (Schrank) and exhibits In the ichneumonid Phytodietus vulgaris Cres- a diapause state closely coincident with that of the son, prepupal diapause induced by short-day condi- host, is an example of the former, and polyphagous tions was terminated within 8 d after being trans- A. asychis is an example of the latter. As hosts of ferred to long-day conditions at 20°C, regardless of A. asychis at least 42 species of aphids have been the diapause duration or need for chilling (Coop recorded from Europe (Zuparko, 1997) and seven and Croft, 1990). Reproductive dormant females of species are known in Japan (Takada, 2002; Takada the nymphalid Danaus plexippus (L.) from over- and Tatsumi, unpublished data). Certain species of wintering clusters in Australia showed rapid ovar- host aphids continue parthenogenetic reproduction ian development when exposed to a temperature of through the winter in Kyoto, and so A. asychis fe- 28°C (James, 1982). In Drosophila melanogaster males would be able to find suitable hosts when Meigen, adult diapause induced by short-day con- they awake from oligopause in early spring. ditions at 12°C was terminated rapidly after being Aphelinus asychis shows apparent variation in transferred to higher temperatures (15 or 18°C) or abdominal coloration, i.e., yellowish brown to dark to long-day conditons (Saunders et al., 1989). brown (Hayat, 1998). Prinsloo and Neser (1994) These types of dormancy have been called stated that the abdomen was dark yellow in South “oligopause”. African materials, but entirely blackish in the The term “oligopause” was originally proposed species from Angola as found sometimes in Euro- by Müller (1965). Mansingh (1971) proposed a pean materials. Brown, black and some other red new classification of dormancy in insects and pro- colorations of adult hymenopterous parasitoids are posed three categories: “quiescence”, “oligopause” due to melanin-group pigments within the cuticle and “diapause” in the order of evolutionary devel- itself (Quicke, 1997). The body coloration of para- opment. The term “oligopause” embraces instances sitoids is influenced by temperature (Quicke, of dormancy that are intermediate between classi- 1997). Liu and Carver (1982) demonstrated the ef- cal quiescence and diapause. Mansingh (1971) out- fects of temperature on the adult coloration of lined a number of characteristics associated with Aphidius smithi Sharma and Subba Rao experi- “oligopause”. These criteria correspond well with mentally. The present study, however, showed that the adult dormancy of A. asychis revealed in the the photoperiod is a profound determinant of this present study. The main difference between polyphenism in A. asychis (Fig. 4). It is interesting “oligopause” and “diapause” is that “refractory that the abdominal coloration and adult oligopause phase” is very short and simple in “oligopause” but are controlled by the same sort of environmental long and essential in “diapause” (Mansingh, 1971). factors (Fig. 4 vs. Fig. 3). In other insects, the asso- In A. asychis, dormant females resumed ovarian ciation between body coloration and diapause is Dormancy of Two Aphelinus Species 455 known, and some studies have demonstrated a hor- against pest aphids during the winter. The survival monal linkage between seasonal coloration and rate after 8 wk of cold treatment in A. asychis was diapause (Tauber et al., 1986). Tauber et al. (1986) higher in oligopausing adults (83%) than in repro- considered such a seasonal polyphenism as part of ductive ones (41%) (Fig. 7). The emergence rate the “diapause syndrome”. Aphelinus asychis could after 8 wk of cold treatment in A. albipodus was be regarded as an insect expressing oligopause-me- also higher in diapausing larvae (86%) (Table 3) diated coloration change. However, its adaptive than non-diapausing ones (18%) (Tatsumi and significance is unclear. The darker abdominal col- Takada, unpublished data). Thus, it is possible to oration may provide cryptic effects during dor- store these parasitoids more efficiently by a mancy or thermoregulatory effects after dormancy combination of low-temperature treatment and as Tauber et al. (1986) suggested for some insects. oligopause/diapause. Oligopausing adults of A. asychis could start oviposition immediately after Characteristics of larval dormancy of A. albipo- storage, but diapausing larvae of A. albipodus dus would take more than 2 wk to development until In A. albipodus, dormant larvae did not resume adult emergence after storage (Table 3). Stored A. development until after certain cold experience asychis is capable of responding to user require- (Table 3). So, A. albipodus from Kyoto and Kobe ments more immediately than stored A. albipodus. entered “diapause” as last instar larvae like the A. ACKNOWLEDGEMENTS mali from the Netherlands (Trimble et al., 1990), A. varipes from southern Alberta (Yu, 1992), and We thank Prof. Y. Yoshiyasu and Assoc. Prof. Y. Abe for A. albipodus from Kazakhstan (Yu, 1992) and reading on the manuscript. This study was supported in part by western China (Bernal et al., 2001). The critical a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan (No. photoperiod (11–12 h) of A. albipodus from Kobe 14560042). (Fig. 8) located at 34.41°N was shorter than that (12.5–13 h) from Kazakhstan at higher latitudes of REFERENCES approximately 50°N (Yu, 1992). Trimble et al. Bernal, J. S., D. González and E. 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