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Dual Photoperiodic Regulation to Enable Univoltine Life Cycle in Alpine Silver-Y Moth, Syngrapha Ottolenguii (Noctuidae: Plusiinae) Without Obligatory Diapause

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Dual Photoperiodic Regulation to Enable Univoltine Life Cycle in Alpine Silver-Y Moth, Syngrapha Ottolenguii (Noctuidae: Plusiinae) Without Obligatory Diapause Appl. Entomol. Zool. 43 (1): 105–112 (2008) http://odokon.org/ Dual photoperiodic regulation to enable univoltine life cycle in alpine silver-Y moth, Syngrapha ottolenguii (Noctuidae: Plusiinae) 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 lepidoptera with long life cycles is severe; winter temperatures drop to Ϫ20°C, and adopt obligatory diapause. summers are short. In this severe environment, Syngrapha ottolenguii is a typical Japanese many alpine moths 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 Xestia 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). Syngrapha devergens, 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, Autographa 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.ϭ7, ratio of individuals without sperma- 2006).
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