Appl. Entomol. Zool. 43 (1): 105–112 (2008) http://odokon.org/

Dual photoperiodic regulation to enable univoltine life cycle in alpine silver-Y , ottolenguii (: ) without obligatory diapause

Satoshi YAMAMURA, Masaki IKARASHI and Masami SASAKI* Division of Applied Entomology and Zoology, Graduate School of Agriculture, Tamagawa University; Machida, Tokyo 194–8610, Japan (Received 4 July 2007; Accepted 25 September 2007)

Abstract Syngrapha ottolenguii (Noctuidae: Plusiinae) is a typical Japanese alpine moth with adults appearing from mid to late summer. Field and laboratory studies show that this species has a univoltine cycle in 1 year, although one generation can be completed in 60 days at 16L-8D and 20°C. We found two strategies—short-day-induced prolongation of 2nd and 3rd instar larval stages for winter, and long-day-induced arrestment of reproductive maturation in adults for sum- mer to enable the univoltine life history without obligatory diapause in the severe alpine climate. As a result, oviposi- tion is delayed into autumn, and the late-hatching, cold-tolerant larvae overwinter under deep snow. Larvae before and after overwintering develop very slowly due to their unique behavior of hiding from the sun’s radiant heat.

Key words: Alpine-moth; diapause; photoperiod; pre-reproductive-period; voltinism

dominates in univoltine species at northern lati- INTRODUCTION tudes (Danilevskii, 1965). This general trend might The alpine climate of central and northern Japan suggest that alpine with long life cycles is severe; winter temperatures drop to 20°C, and adopt obligatory diapause. summers are short. In this severe environment, Syngrapha ottolenguii is a typical Japanese many alpine and butterflies are known to alpine moth (Fig. 1a, b) found in the alpine vegeta- take 2 or more years to complete their life cycle. tion dominated by the alpine pine, Pinus pumila. It For example, Oeneis melissa and a borealis is also recorded in China, Russia, and Attu and take 2 years (Jinbo, 1984; Varkonyi and Ahola, Atka in the outer Aleutian Islands of Alaska (La- 2001), Parnassius eversmanni and Gynaephora fontaine and Poole, 1991; Jinbo and Watanabe, daisesuzana take 3 years (Jinbo, 1984; Kusunoki 1994). Its ecology and life history have been re- and Yasuda, 2002). , a con- ported but the data are fragmentary (Nishio, 1986; generic species to Syngrapha ottolenguii (alpine Kusunoki and Yasuda, 1997, 2002; Jinbo et al., silver-Y, Noctuidae: Plusiinae) in the present study, 2002). Field observations and trial rearing indi- is a typical moth of the European Alps with larvae cated that the food plants are Vaccinium vitis- that overwinter twice and emerge as adults in June idaea, V. uliginosum, or Empetrum nigrum (Kusu- or July (Goater et al., 2003; Ahola and Silvonen, noki and Yasuda, 1997, 2002; Jinbo et al., 2002). 2005). However, information about the regulatory Our field studies on Mt. Zao (1,800 m asl), Mt. mechanism in alpine lepidoptera is very scant. Kiso-Komagatake (2,600 m asl) and Mt. Ontake Multivoltine species living in temperate climates (2,500 m asl) confirm that E. nigrum is the pre- usually enter facultative diapause according to pho- ferred food plant. toperiod exposure (ex. Hyphantria cunea, Gomi, In recent comparative ecological studies on 2004). On the other hand, obligatory diapause Plusiinae moths, including serious pests like Tri-

*To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2008.105

105 106 S. YAMAMURA et al.

Fig. 1. a: Syngrapha ottolenguii adult. b: Fifth instar larva. c: Larvae feeding on artificial diet. d: Immature (left) and mature (right) eggs in ovary. choplusia ni, gamma, and A. ni- expected obligatory diapause somewhere in the lar- grisigna, we successfully reared S. ottolenguii on val stages but preliminary experiments indicated an artificial diet and can now analyze its life his- neither obligatory diapause, nor common faculta- tory in the laboratory. tive diapause with a critical photoperiod. Conse- The present study focuses on the effects of pho- quently, we investigated the number of days for toperiod on development and possible diapause in each larval instar from hatching to pupation at larval stages, and on the pre-reproductive period of 7 photoperiods (10L-14D, 12L-12D, 14L-10D, adults. We discuss how the univoltine life cycle 14.5L-9.5D, 15L-9D, 15.5L-8.5D and 16L-8D) at takes 1 year in severe alpine conditions where lar- 20°C, using successively reared second (G2) or vae overwinter under deep snow for more than 6 third (G3) generation moths. In parallel experi- months. ments, we recorded the number of feces under the same LD regimes as an index of feeding during each instar. We discovered delayed development at MATERIALS AND METHODS an LD regime of 12L-12D. Laboratory rearing. We reared successive gen- Mating season and frequency in alpine field. erations of S. ottolenguii in the laboratory on an ar- Syngrapha ottolenguii is seen on the wing from tificial diet (Fig. 1c). Mated females oviposited on late July until mid-September (Jinbo, 1984). The E. nigrum and hatched larvae were fed on the com- longevity is longer than other alpine moths, sug- mercial artificial diet Insecta LF-S (Nihon Nosan gesting possible voltinism regulation in adult Kogyo Co. Ltd.) at 16L-8D and 20°C to prevent di- stages as well as larval stages. To check this apause. hypothesis, we counted the number of sper- Larval diapause at different photoperiods. We matophores in females collected on 22–23 August Univoltine Life Cycle in S. ottolenguii 107

2003 and 8–9 August 2004 on Mt. Zao. Abdomens were boiled in a detergent-water solution and the number of spermatophores in the bursa copulatorix was counted under a binocular microscope. Evaluation of ovarian development. To deter- mine the pre-reproductive period (PRP) from adult emergence to sexually mature state with chorion- ated eggs, the ovary development of five age groups was compared using first-generation (G1) females kept at 12L-12D and 20°C. Females with ovaries filled with chorionated eggs were evaluated as sexually mature, while females without chorion- ated eggs and with a body cavity filled by bulging Fig. 2. Effect of photoperiods from 16L-8D to 10L-14D fat bodies were evaluated as not ready to oviposit. on duration of all larval stages from hatching to pupation. Fig- Mature eggs are easily distinguished as flattish, ures in parenthesis are numbers of larvae. Bars are standard deviations. Groups with different letters are significantly dif- yellowish, and hardly chorionated (Fig. 1d). Imma- ferent at 5% level by Tukey’s HSD test after significant ture eggs are spherical, whitish, and matted. We ANOVA. used the following five categories to evaluate sex- ual maturity based on Macaulay (1972). sence of obligatory diapause, we observed the ef- 1. No chorionated egg in ovarioles and full of fat fect of photoperiod on larval development. As Fig. body in body cavity 2 shows, there was no facultative diapause at a crit- 2. Small whitish eggs in ovarioles and well-devel- ical photophase. Instead, gradual and continuous oped fat body in body cavity lengthened larval duration is found with increasing 3. Many large whitish eggs in ovarioles and devel- photophase. A photoperiod of 16L or 15.5L—cor- oped fat body in body cavity responding to midsummer in the field—made lar- 4. Many yellow and whitish eggs in ovarioles and vae pupate for less than 40 days, a short day of little fat body remaining 12L-12D caused around 100 days of pupation. The 5. Many yellow, mature eggs in ovarioles and only prolongation seems saturated at 12L or 10L. Figure atrophied fat body remaining 3 shows the development details for three typical Second (G2) and third-generation (G3) adult fe- cases. There was large individual variation, espe- males were used to evaluate the effect of photope- cially at 14.5L and 12L, when the earliest larva pu- riod on ovarian development (Fig. 5). Six individu- pated in 30 days, while the last one needed 140 als were kept in plastic containers (W: 210 mm, D: days. 150 mm, H: 140 mm) for 40 days at three photope- Next, we determined the larval instar when pro- riods of LL, 16L and 12L. The evaluation method longation occurred by comparing the responses be- was the same as described above. tween two photoperiods. As Fig. 4 shows, a re- Effect of JH on ovarian development. To ex- markable delay occurred in the 2nd and 3rd instars, amine the effect of juvenile hormone (JH) on ovar- but there was no such delay in the 1st and 5th in- ian development, day-0 female adults were topi- stars. From our field work, we know that the 2nd cally applied with 1 ml (10% v/v isopropylalcohol and 3rd instars overwinter under deep snow. solution) of methoprene (Wako Chemical Co. Ltd.) To determine the physiological state during this on the dorsal abdomen. Treated females were kept development delay, we monitored defecation under for 7 days at either 12L-12D or LL, and ovarian de- the same photoperiod conditions. Larvae continued velopment was examined as described above. feeding (data not shown) but the rate was distinctly slower. This agrees well with the observation that the body of the 2nd and 3rd instar larvae is dark, RESULTS instead of transparent, reflecting the absence of Larval developmental period at different pho- food in the intestine. In the allied boreo-subalpine toperiods species Autographa buraetica, which has complete Since preliminary experiments showed the ab- obligatory diapause, the transparent period extends 108 S. YAMAMURA et al. for as long as five months (Yamamura and Sasaki, (max.7, ratio of individuals without sperma- 2006). tophore69.8%, N43), while the number was 5.04.8 (max.13, ratio16.7%, N6) in fe- Mating timing and frequency in field males captured later (22–23 August 2003). This To clarify the mating status of the females in the suggests that only 30% of the emerged population field, we captured females on two dates. The aver- has mated by early August and some females had age number of spermatophores in females captured not mated even by the late August. Also, the num- earlier (8–9 August 2004) was only 1.22.1 ber of matings indicated by the number of sper- matophores in S. ottolenguii was found to be ex- traordinary large.

Ovarian development in response to photope- riod To determine the effect of photoperiod on ovar- ian development, we kept females for 401 days under three photoregimes of 12L-12D, 16L-8D, and LL simulating the arctic midnight sun. Neither males nor food plants were provided and no ovipo- sition was seen. As shown in Fig. 5, the effect of photoperiod is clear—long days inhibit ovarian de- velopment and short days allow development. The 16L regime suppressed the number of mature eggs to 200 or less and about half the females remained

Fig. 3. Three typical developmental responses in larvae: details of distribution of larval period at 15.5L, 14.5L and 12L Fig. 4. Comparison of average duration of each larval in- (original data same as in Fig. 2). Arrows indicate average pe- star between 15.5L-8.5D, allowing minimum larval duration riod of each experimental group. and 14.5L-9.5D where growth clearly arrested.

Fig. 5. Effect of photoperiod on sexual maturation: Left half is ratio of virgin females with (open portion) and without (hatched portion) mature eggs at 40 days after emergence. Black bar of right half is average number of mature eggs found in all 40- day-old females. Open bar on right is same but based on females with mature eggs. * Significantly different at 5% level by Chi- square test. Groups of open bars with different letters are significantly different at 5% level by Tukey’s HSD test after significant ANOVA. Univoltine Life Cycle in S. ottolenguii 109 in ovary development categories 1–3. Females kept mature G1 or G2 females shown in Fig. 5. The rea- under 12L had an average of 500 chorionated eggs son is discussed later. and all were categorized as grade 5. This tendency extended to LL, but the average number of mature Effect of JH on ovarian development eggs was only 100. Since keeping adult females To determine how adult life is prolonged and for 40 days may be too long considering field sexual maturity is regulated, we examined the ef- longevity, we investigated ovary development with fect of methoprene, a stable JH analog, using G1 or aging under 12L-12D. As shown in Fig. 6, 90% of G2 females as shown in Fig. 5. The effect of JH the virgin females remained in the immature state was clear (Fig. 7) and more than 400 chorionated with no chorionated eggs at 6–7 days old, which is eggs were developed even in 7-day-old females different from usual Plusiinae female moths, which kept at LL, where strong inhibition was seen in un- already have developed ovaries at this age (unpub- treated females. lished data). At 9–10 days old, most females have developed mature eggs (mean 9581) and the DISCUSSION number of chorionated eggs increased to 193177 at 40-days old. The number (193177) was Species in the Syngrapha are distributed smaller and the variance was bigger than in fully widely over boreal regions and alpine areas of tem- perate regions and some have a circumpolar distri- bution. Many, especially the European species, are thought to have 1-year life cycle. An exception is S. devergens, taking 2 years for one cycle (Goater et al., 2003; Ahola and Silvonen, 2005). In Japan, Jinbo et al. (2002) speculated that S. ottolenguii might take 2 years to complete one generation on Mt. Daisetsu. However, our present laboratory analyses and evidence from year-round field sur- veys indicate that S. ottolenguii has a 1-year life cycle with no obligatory diapause, instead length- ening both middle larval stages and adult pre-re- productive period by different responses to summer and autumn photoperiods.

Short-day-induced larval diapause Fig. 6. Relationship between advancement of aging and Univoltine behavior with endogenous diapause sexual maturation of female S. ottolenguii shown by number of mature, chorionated eggs (solid circle) and percentage of fe- induction is common in many species living at high males without mature eggs. Figures under histogram are aver- latitudes (Saunders, 1977). For example, subalpine age number of eggsSD. and north-adapted Autographa buraetica, A. ex-

Fig. 7. Effect of methoprene, JH analog, on sexual maturation of females under LL and 12L-12D for 7 days after emergence: Left half is ratio of virgin females with (open portion) and without (hatched portion) mature eggs. Black bar of right half is average number of mature eggs found in all 7-day-old females. Open bar on right is same but based on females with mature eggs. 110 S. YAMAMURA et al. celsa, and enter obligatory diapause males had 52579 mature eggs and 0% had no in the larval stages (Yamamura and Sasaki, 2006). mature eggs (Fig. 5). The difference in the number However, high-latitude-adapted S. ottolenguii is of mature eggs between the G1 and G2 or G3 gen- different (Figs. 3 and 4) with prolonged middle-lar- erations possibly results from bias during labora- val stages under short-day conditions, which is tory culturing, where operators might tend to similar to the behavior seen in the temperate Ore- choose females with a short PRP and with a big sia emarginata, and the spotted cutworm Xestia c- egg maturation capacity. nigrum (Oku, 1984; Ogihara et al., 1995). By contrast, reproductive maturation is strongly S. ottolenguii never enters endogenous diapause. inhibited at long-day conditions where almost half In the field, hatched larvae grow slowly and most of females had not developed mature eggs even probably enter hibernation as the 2nd and 3rd in- after 40 days (Fig. 5). In the field, this means that stars in November. We have not yet found larvae oviposition is inhibited for 1 month or more during hibernating under deep snow, but we have found mid-summer. The duration corresponds to about many larvae in dense bushes of E. nigrum in May half the length of the adult emergence period from just after finishing hibernation. These larvae are late July to mid-September. This prolonged PRP in resting or hiding on the thin, brown stems under adult females under long-day conditions conflicts the dense green crown of their food plant. Data with normal theories that earlier reproduction has logger records show that the temperature at the adaptive benefits in short alpine summers. suggested overwintering site under deep snow is Since the degree of inhibition is linear and constant at 0°C throughout the winter. We have not day-length dependent (Fig. 7), it seems to work yet determined the lower threshold temperature strongly on moths emerging earlier in the season, (developmental zero point) for the 2nd and 3rd in- but disappears for moths emerging later in Septem- star larvae, but it should be around 5°C, because ber when oviposition can begin with minimum they survive and continue feeding for more than 6 delay. This agrees well with the presence of high months at a constant 4 to 5°C in preliminary obser- numbers of unmated females in alpine fields in the vations. After hibernation, the larvae restart slow middle of the adult emergence season. This pho- growth again and pupate in late July or early Au- toperiod-dependent prolongation of PRP is not gust in the field. To keep the developmental veloc- seen in species like Erythroplusia pyropia and ity slow, they never crawl out onto the warm upper eriosoma, and clearly the adult re- surface of the crown leaves during sunny days. Al- sponse to long days is a significant regulator of though they only eat young, fresh leaves of E. ni- voltinism in S. ottolenguii. grum, feeding is restricted to cool nights or foggy rainy days. As a result, they spend 10 months or Regulation enabling univoltine life cycle more as larval stages. Contrary to our first beliefs and speculation by No indication of diapause or any type of arrest- Jinbo et al. (2002), S. ottolenguii has a 1-year life ment was seen in egg and pupal stages. As shown cycle achieved by overwintering of larval stages. in Figs. 3 and 4, the prolongation or arrestment The larvae are cold tolerant and develop slowly (shallow diapause) is seen only in 2nd and 3rd in- with a unique hiding behavior to escape the sun’s star larvae under short-day conditions. On the other heat. The species has slow and adjustable develop- hand, some few larvae completed the larval stages ment of both larval and adult stages using two pho- without any prolongation even at 12L-12D. They toperiod-dependent processes—short-day-induced look like an exception, but similar cases were also prolongation (shallow diapause) of larval period, seen sporadically in the 10L-14D and 14L-10D and long-day induced prolongation of PRP in groups (data not shown). adults. The delay in adult sexual maturation by long Long-day-induced prolongation of PRP in adults days, instead of short days (Fig. 5) is interesting. Under 12L-12D, most 9–10 day old females had Regulation of PRP is common, especially in migra- mature eggs and the PRP seems to be 7–9 days tory Lepidoptera. In these cases, many species re- (Fig. 6). At 40 days after emergence, G1 females produce under long days and high temperatures, had 194177 mature eggs (Fig. 6), G2 and G3 fe- and migrate under short days and low temperature Univoltine Life Cycle in S. ottolenguii 111 with inhibited ovary development and reproduction diapause? (McNeil et al., 1995). For example, in Autographa Endogenous diapause is a major strategy for gamma, which is famed for its migratory nature adapting to arctic climates. However S. ottolenguii and is closely related to S. ottolenguii, PRP is may either not have had a chance to acquire this shortened by longer days and lengthened by short strategy or lost it in the past, subjecting the moth to days (Hill and Gatehouse, 1993). The PRP re- a risky multivoltine strategy depending on climatic sponse of S. ottolenguii to photoperiod is the oppo- conditions. To avoid this risk and maintain a uni- site of A. gamma. voltine system, S. ottolenguii seems to exploit a However, the JH mode of action in regulating combination of two easy strategies: dual photope- PRP of S. ottolenguii is same as that seen generally riod-dependent prolongation of larvae and PRP in in other moths. Adult females topically applied adults. Prolongation in larvae is common in many with JH analog on emergence day developed more diapausing Plusiinae species; prolongation of PRP than 400 eggs within 7 days irrespective of pho- is also common in migrant species like A. gamma. toperiod (Fig. 7). Usually, long days and high tem- S. ottolenguii may have adopted this strategy due peratures induce high JH titers and resultant repro- their distribution origins. Looking at the present duction, while short days and low temperatures in- life history, there is some chance of become bivol- duce prolonged PRP and migration (McNeil et al., tine by shortening the larval period. However, an 1995). From this evidence it seems that JH produc- opposite strategy has evolved instead whereby the tion is inhibited during the prolonged PRP in S. ot- larvae have adopted a unique behavioral response tolenguii. to avoid the sun’s radiant heat and achieve very The natural S. ottolenguii population we studied slow development. As mentioned, S. ottolenguii is on Mt. Zao area never experiences a long day of thought to have moved to Japan from the far north more than 16 h even at midsummer. Consequently, and the southward spread may have favored grad- the inhibitory effect of long days on sexual matura- ual lengthening of larval period to achieve a uni- tion is not so strong, but must still function to sta- voltine system that was not a reasonable strategy in bilize the timing of the life cycle in the alpine cli- their original cooler distribution. mate, especially when the weather is abnormal. S. The shallow diapause with large variation (Figs. ottolenguii is distributed up to Attu in the Aleu- 2 and 3) is explained below. In general, the advan- tians at 53°N, where days are longer than 18 h in tage of deep diapause is avoidance of the risk of midsummer. Perhaps the inhibition evolved in this too early activation and death caused by wild tem- high-latitude environment. Indeed, Jinbo (1984) perature fluctuations in spring. However, the alpine suggests that S. ottolenguii reached Japan from the environment is different and features early snows far north and not west from the Korean peninsula. and late thaws at regular times every year; overwin- tering larvae always have a stable environment at Why combination of two shallow diapauses in- 0°C under deep snow. Consequently, exposure to stead of usual obligatory diapause? lethal temperatures is rare once the snow has disap- In Plusiinae moths, there seems to be a clear re- peared. Probably both this environmental feature lationship between climate and diapause strategy. and cold tolerance allow the larvae to overwinter Species (A. nigrisigna, agnata, Ery- with shallow diapause. A similar strategy is throplusia pyropia) inhabiting plains to montane adopted by the Shonai ecotype of the rice stem areas in temperate zones do not show diapause; borer, Chilo suppressaris (Fukaya, 1967). Large boreo-montane to subalpine species ( variation in the prolonged larval period at short day stenochrysi, D. chryson) show photoperiod-de- length (Fig. 3) may occur because the selection pendent (facultative) diapause; and subalpine pressure has not operated for long in the stable species (Autographa buraetica, A. excelsa, and snow environment. Syngrapha ain) show endogenous obligatory dia- pause (ex. Oku and Kobayashi, 1978; Yamamura REFERENCES and Sasaki, 2006, 2007). Against this background, Ahola, M. and K. Silvonen (2005) Larvae of Northern Euro- why does the alpine S. ottolenguii show a combina- pean Noctuidae. Vol. 1. Apollo Books, Svendvorg. tion of two shallow diapauses instead of obligatory 657 pp. 112 S. YAMAMURA et al.

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