Environmental induction of larval diapause and life-history consequences of post-diapause development in the Large Copper butterfly,Lycaena dispar (Lepidoptera: Lycaenidae)

Many insects in temperate zones withstand the adverse conditions of winter through entering diapause and the two most important environmental stimuli that induce diapause are photoperiod and ambient temperature. The Large Copper butterfly, Lycaena dispar Haworth (Lepidoptera: Lycaenidae), is a Palearctic butterfly that hibernates as larvae. Since this butterfly is a near threatened species in some regions, there has been a growing need for a standardized protocol for mass rearing of this butterfly based on the adequate knowledge of its ecology. In the present study, we first identified that L. dispar larvae were sensitive to the photoperiodic induction of diapause during their first larval instar. We then investigated to what extent the diapause-inducing effects of photoperiod could be modified by ambient temperatures in L. dispar larvae by exposing them to the range of day-lengths (L:D 14:10, 12:12, 10:14 and 8:16) at three different temperatures (15, 20 and 25 °C). All larvae were induced to enter diapause at low ambient temperature (15 °C) regardless of photoperiod, whereas most of them (86 %) exhibited direct development when temperature was high (25 °C). The photoperiodic induction of diapause was evident when day-length was shorter than 14 h at intermediate temperature (20 °C). Pre-diapause development was prolonged at low temperatures. Finally, we found that post-diapause development of L. dispar larvae was determined by both the chilling temperature experienced by diapausing larvae and the duration of larval diapause. Adult emergence was enhanced when larvae were chilled at 8 °C and when they had been under the state of diapause for 20 days before they were treated to terminate diapause.     

Geographical variation in photoperiodic induction of larval diapause in the bruchid beetle, Bruchidius dorsalis: polymorphism in overwintering stages

The bruchid beetle, Bruchidius dorsalis Fahraeus (Coleoptera: Bruchidae), has a multivoltine life cycle and shows geographical variation of overwintering stages in Japan. Our previous study found that B. dorsalis enters larval diapause in the final instar under short photoperiods. In cooler areas, we observed that most individuals overwinter in the final larval stage in diapause, whereas beetles at different developmental stages (non‐diapausing young instars, diapausing instars, and adults) were overwintering in warmer areas. In this study, we investigated geographical variation in the photoperiodic response for induction of larval diapause at 20 °C (three populations) and 24 °C (two populations) to clarify the overwintering strategy of B. dorsalis. We observed that (1) diapause incidence at 20 °C changed sharply from ca. 100% to 0% with a change in photoperiod in all the populations, (2) critical photoperiod was longer at 20 °C in populations from cooler areas, and (3) critical photoperiod at 24 °C was shorter than at 20 °C and a fraction of the larvae did not enter diapause, even under short photoperiods. Overwintering stages estimated from these results were consistent with those actually observed in the field. This study indicates that the geographical variation of overwintering stages is likely to reflect adaptive diapause induction in each local environment.     

Voltinism and diapause in the spruce web-spinning sawflyCephalcia arvensis

Cephalcia arvensis Panzer (Hym., Pamphiliidae) spends most of the life cycle as a prepupa inside an earth-walled chamber in the soil of spruce (Picea abies Karst.) forests. There are two types of prepupae in diapause in the soil, the eonymph and the pronymph. Prolonged diapause as an eonymph occurs in prepupae just after soil penetration at temperatures below 12°C. Eonymphs change into pronymphs during the following summer and the life cycle lasts for two years. Mature larvae that enter the soil at temperatures above 12°C change immediately into pronymphs and these individuals will emerge during the next spring. Other factors such as photoperiod do not appear to be correlated with prolonged diapause. The depth reached by the mature larvae in the soil is proportional to their size and inversely proportional to the soil temperature. Consequently, voltinism depends on both the conditions affecting development of the larvae in the crowns and the temperature at different soil depths.     

Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae)

Regulation of growth and development by photoperiod was studied in a population of the speckled wood butterfly, Purarge aegeria L. (Lepidoptera: Satyrinae), from southern Sweden. Individuals were reared in a range of photoperiodic regimes (9L. to 22L) and temperatures (13°C to 21° C). Plasticity was found for important life-history traits- generation time, growth rate and final weight and seasonal regulation of development in response to photoperiod was found to occur at two levels. Purarge aegeria hibernates as a third instar larva or in the pupal stage, cantering one of four major developmental pathways in response to photoperiod: (1) direct development in both the larval and pupal stages, (2) pupal winter diapause with or (3) without a preceding larval summer diapause, or (4) larval winter diapause. In addition to this high-level regulation of individual development, larval growth rate and pupal development rate also appear to be finally regulated by photoperiod within each major pathway. As photoperiods decreased from 22 h to 17 h at 17° C, growth rate among directly developing larvae increased progressively, as was the case for larva? developing according to a univoltine life cycle from 17 h to 14 h. At two photoperiods, 13 h and 16 h (corresponding to shifts between major pathways), both larval and pupal development were extremely variable with the fastest individuals developing directly and the slowest developing with a diapause. This indicates a gradual nature of diapause itself, suggesting that the two level may not he fundamentally different.     

Adult diapause ofCybocephalus nigriceps nigriceps [Col.: Cybocephalidae]

During autumn and winter (October–February)Cybocephalus nigriceps nigriceps (J. Sahlberg) adults undergo a facultative diapause. The diapausing adults agregate in hiding places, development of the ovaries is arrested, and prey consumption is lowered. Diapause can be prevented by exposure to a long-day photoperiod (16 hr light) at high temperatures (29° and 32°C). Diapause is induced mainly by short-day conditions, but the termination of diapause is affected by both photoperiod (long-day conditions) and temperature (29°, 32° and 34°C). In mature females, diapause induction causes ovarian degeneration. The induction or inhibition of adult diapause is affected by photoperiods occurring during larval development as well as during adult life.     

苜蓿切叶蜂滞育的诱导因素研究

苜蓿切叶蜂Megachile rotundata(F.)预蛹的滞育主要受光周期和温度的影响。雌蜂感受光周期的变化是决定子代预蛹是否进入滞育的一个主要因素;当代的幼期,特别是高龄幼虫(约3龄)到预蛹这一阶段所感受的温度变化,对预蛹滞育有很大的影响,此期如果环境温度低于(21.59±1.03)℃,可有超过50%的个体进入滞育。此外,放蜂地区的纬度及蜂的代次对预蛹的滞育亦有重要的影响。     

中华稻蝗长沙种群的生活史及其卵滞育的进化意义

中华稻蝗Oxya chinensis为重要的水稻害虫,在我国除青海、西藏、新疆、内蒙古等未见报道外,南起海南北至东北均有分布,在许多的分布区域1年发生1代。为探索中华稻蝗长沙种群的生活史及其季节适应特征,通过野外和实验室的研究,调查了其发生代数、孵化率和卵滞育率的季节变化及越冬卵的存活率。结果显示,中华稻蝗长沙种群为1年2代和1年1代混合发生:第1代卵产卵后大部分孵化为若虫而1年完成2代,但亦有19.4% -4.1%的卵不孵化而1年只能完成1世代。第1代成虫于6月上旬至8月上旬羽化,6月下旬至8月中旬产卵;第2代若虫于7月初开始孵化,9-10月羽化为成虫,10月上旬至11月下旬产卵。在室外自然条件下,中华稻蝗长沙种群6-8月(第1代)和10-11月(第2代)所产卵块均为部分滞育,滞育率为30%左右,皆无显著差异。然而,其卵滞育率在12月以后显著降低,仅为6.6%或以下,卵滞育快速地得以解除。因此,包括非滞育卵和滞育解除卵,中华稻蝗长沙种群的越冬卵皆以非滞育状态度过其后的寒冷季节。即使是遭遇长江流域2007年末至 2008年初异常寒冷的冬季,在长沙地区越冬后其卵的存活率亦在98%以上。非滞育状态的中华稻蝗长沙种群越冬卵完全能安全地越冬,其滞育的发生并非是为了提高其耐寒性而安全度过不适环境。并探讨了中华稻蝗长沙种群卵滞育的进化意义。     

Seasonal regulation of dormancy in Chrysopa carnea (Neuroptera)

In Ithaca, New York, diapause incidence in Chrysopa carnea exceeds 50 per cent among adults emerging between 31 August and 3 September. Apparently, decreasing late summer day lengths, which exceed the stationary critical photoperiod in the laboratory, act on the sensitive stages and induce diapause. Full diapause intensity occurs about 2 weeks after adult emergence; complete winter coloration appears approximately 2 weeks later. Photoperiodic stimili in combination with the geographic strain largely determine diapause depth.Decreasing autumn day lengths decelerate diapause development and maintain diapause until the winter solstice. Subsequently, short day lengths and cold temperatures slow diapause development. In nature, neither long days, increasing day lengths, nor chilling hasten diapause termination. Diapause duration is largely determined by the interaction between inducing photoperiod, maintaining photoperiodic and thermal stimuli, and geographic strain. In Ithaca, diapause ends (all response to photoperiod ceases) between 22 January and 12 March.After diapause ends, the animals retain their diapause characteristics until temperatures exceed 4°C. Post-diapause reproductive development in females requires approximately 100 heat units above 4°C; however, below 8°C mating and oviposition are absent. Although the winter coloration remains, mating occurs within 1 day after transfer from 4 to 24°C. Temperature determines the rate at which the green summer colour returns.     

Photoperiodic induction of prepupal diapause and its role in synchronization with host phenology in the hibiscus caterpillar,Xanthodes transversa

The hibiscus caterpillar, Xanthodes transversa (Lepidoptera: Noctuidae), is a multivoltine insect that is an important pest of Malvaceae plants such as the okra, Abelmoschus esculentus, and the common rose mallow, Hibiscus mutabilis, in Japan. In the present study, the effects of photoperiod and temperature on the induction of prepupal diapause and the adaptive significance of this diapause were examined in a local population of X. transversa in Miyazaki, Kyushu, southwestern Japan. Larvae showed a long‐day photoperiodic response for controlling the induction of prepupal diapause with a critical day length between 13 and 14 h at 20 to 25°C. Under long‐day conditions larvae rapidly pupated from the sixth instar, but under short‐day conditions they entered diapause in the prepupal stage. Diapause occurrence in the field increased in late September, which was consistent with the laboratory results in terms of the photoperiodic response. Non‐diapause development after this time is maladaptive because most larvae of the next generation could not reach the critical stage (prepupae) before winter and died during early winter in outdoor experiments. Larvae suffered from a high rate of mortality when fed leaves collected late in autumn. The photoperiodic response for controlling the induction of diapause in this insect may play an important role in synchronizing the life cycle with the seasonal changes in food and temperature conditions.     

Effect of photoperiod on the induction and maintenance of diapause and on development of the predatory bugPodisus maculiventris (Hem.: Pentatomidae)

The predatory bugPodisus maculiventris Say displays a reproductive diapause. In the laboratory, at 23±1°C, when the pre-imaginal stages were reared on larvae ofGalleria melonella L. (Lepidoptera: Pyralidae) under a short photoperiod of 8L: 16D, diapause was induced in all adult females, whereas under a long photoperiod of 16L: 8D none entered diapause. Nymphal development was faster under the diapause-inducing short photoperiod than under the diapause-averting long photo-period. By contrast, embryonic development was faster under the long than under the short photoperiod. Diapause maintenance was also under the control of photoperiod. After a 10-d-period of chilling at 4°C, diapause was quickly terminated in adults kept under long photoperiod whereas it was maintained in most of those kept under short photoperiod. The predation rate of non-diapause or post-diapause adult females was much higher than that of diapause females.     

Effect of temperature and photoperiod on diapause development in a Douglas fir seed chalcid, Megastigmus spermotrophus

Douglas fir seeds infested by diapausing larvae of a chalcid, Megastigmus spermotrophus, were transferred under different temperature and photoperiod regimes at various dates during autumn and winter. Both winter diapause and prolonged diapause were compared to the diapause patterns observed in control lots kept under natural conditions. The results showed that exposure to low temperatures in autumn and winter is required for the completion of diapause development. Median adult emergence dates and the date of transfer of larvae to 20°C were negatively correlated. The frequency of prolonged diapause of larvae transferred to 20°C decreased significantly after November. When larvae were submitted to different constant temperatures, the longer the daylength, the higher and faster the reactivation. These results suggest that chalcid larvae can perceive daylength through the seed coat. This phenomenon is probably related to the fact that most of the infested seeds falling in autumn are usually covered by a layer of leaf litter during the winter. Received: 14 June 1996 / Accepted: 24 February 1997     

Effect of temperature on the termination of diapause in the univoltine almond seed wasp Eurytoma amygdali

Diapausing larvae of Eurytoma amygdali Enderlein (Hymenoptera, Eurytomidae) were collected in early August and late September. They were subjected to various photoperiod and temperature regimens for up to 20 weeks, then kept at L16:D8 and 19 °C for another 14 to 26 weeks for diapause to be terminated and pupation to take place. Photoperiod did not affect diapause completion. It was confirmed that the two morphologically distinct diapause stages have different temperature requirements for their completion. The first diapause stage was completed synchronously at temperatures between 16 and 19 °C. A higher temperature of 26 °C delayed diapause development. The second stage required lower temperatures between 4 and 10 °C. Spontaneous termination of diapause was observed at constant 19 °C. When applied to the first diapause stage for 20 weeks, low temperatures made the larvae refractory to subsequent intermediate temperatures. The first stage was thus maintained until a higher temperature of 26 °C made the larvae regain their ability to respond to the intermediate temperatures and complete this stage. Larvae grown in Retsou almonds had a higher diapause intensity than larvae grown in Truoito almonds. The results suggest that, in nature, the high temperatures of late summer and early autumn are likely to maintain the first diapause stage. Subsequently, the less warm temperatures of autumn allow the completion of the first stage by late autumn, and the low temperatures of late autumn and of winter allow the completion of the second diapause stage by mid winter.     

Diapause and cold tolerance in Asian species of the parasitoid Leptopilina (Hymenoptera: Figitidae)

Diapause and cold tolerance are essential for temperate insects to pass the winter, with the mechanisms controlling these two traits varying considerably among insects. In the present study, diapause and cold tolerance are compared among three Leptopilina species: Leptopilina japonica Novkovi? & Kimura, Leptopilina victoriae Nordlander and Leptopilina ryukyuensis Novkovi? & Kimura, all larval parasitoids of frugivorous drosophilid flies, with the aim of understanding their climatic adaptations. The first species is divided into the temperate (Leptopilina japonica japonica) and subtropical subspecies (Leptopilina japonica formosana), and the latter two species are distributed in the tropical and subtropical regions. The temperate subspecies of L. japonica enters prepupal diapause at low temperatures (15 or 18 °C), irrespective of photoperiod, and some individuals enter diapause when exposed to 0 °C for 1 or 2 day(s) or when placed at low humidity. Leptopilina victoriae also shows signs of diapause initiation at 15 °C, although L. ryukyuensis and L. j. formosana from the subtropical regions do not. Preimaginal viability at low temperature (13, 14 or 15 °C) is usually lower in L. victoriae from the tropical regions compared with L. japonica or L. ryukyuensis from the temperate or subtropical regions. Diapausing prepupae of the temperate subspecies appear to be cold tolerant. However, the cold tolerance of nondiapausing prepupae, pupae and adult females varies little among the tropical, subtropical and temperate species or subspecies, and adult males of the temperate subspecies of L. japonica are less cold tolerant than those of the tropical or subtropical species or subspecies. Cold tolerance may be unnecessary, except for diapausing individuals of the temperate species, because nondiapausing individuals appear in warmer seasons.     

Diapause termination, post-diapause development and reproduction in the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae)

Effects of photoperiod and cold exposure on diapause termination, post-diapause development and reproduction in Loxostege sticticalis were examined. Larvae were reared at diapause inducing condition (22 °C, L:D 12:12) consistently or transferred to long day photoperiod (L:D 16:8) and darkness (L:D 0:24) respectively, after entering into diapause. Diapause was terminated in approximately 40% of the larvae after 36 days, and no significant differences were observed between photoperiods, suggesting larval diapause was terminated spontaneously without being induced by photoperiods. Cold exposure significantly hastened diapause termination. The diapause termination incidence increased significantly with peaks of 98% at both 5 °C and 0 °C exposure for 30 days, as compared to 42% in controls not exposed to cold, while the mortality and number of days required for diapause termination decreased dramatically. The optimal low temperature exposure periods under 5 °C or 0 °C were 20 days and 30 days, showing a higher termination incidence and shorter time for diapause termination. This suggests that the low temperatures in winter play an important role in diapause termination under natural conditions. The threshold temperatures for post-diapause development in prepupae and pupae were 9.13 °C and 10.60 °C respectively, with corresponding accumulations of 125 and 200 degree-days. Adults that experienced larval diapause significantly delayed their first oviposition, oviposition period was prolonged, and the lifetime number of eggs laid was decreased, however both males and females have significantly longer longevity. The field validation of diapause termination, the degree-days model, and the relationship between diapause and migration in L. sticticalis were also discussed.     

Effect of photoperiod and temperature on diapause in a Florida strain of the tropical warehouse moth Ephestia cautella

A photoperiodically-controlled diapause of the long-day, short-day type was identified in a brown-winged, yellow-eyed strain of Ephestia cautella (Walker). The proportion of larvae diapausing in very long photoperiods was less than in short photoperiods. The mean critical photoperiod, here defined as that photoperiod giving half the maximum percentage of insects that diapause in response to photoperiod at a given temperature, was between 12 and 13 hr for the long-day reaction at both 20 and 25°C. The principal sensitive phase occurred near the time of the last larval moult. The mean duration of diapause was 2–3 months at 20°C and slightly longer at 25°C. The optimum temperature for diapause development was near 15°C, all larvae pupating within 24 days after a 45-day exposure at this temperature. Diapause could be terminated whenever larvae diapausing at 20°C were exposed to as few as five long (15 hr) photoperiods at 25°C. Long photoperiods at 20°C, or short photoperiods (9 hr) at 25°C were less effective in terminating diapause.     

On the factors inducing the inhibition of diapause in the progeny of diapause females of Trichogramma telengai

The ability to enter diapause in the progeny of Trichogramma Westw. (Hymenoptera: Trichogrammatidae) females that have undergone diapause is markedly reduced or even completely absent. This maternal inhibition of diapause can result from three types of factors: (i) environmental factors that induce maternal diapause; (ii) maternal diapause itself; and (iii) diapause‐terminating environmental factors. The present study aims to determine the factors that prevent diapause in the progeny of a Trichogramma telengai Sor. generation that has undergone diapause. Different tendencies to enter diapause in the maternal generation are induced by different photoperiods (LD 12 : 12 h, 16 : 8 h and 18 : 6 h) during development of the grandmaternal generation and different temperatures (from 10 to 15 °C) during larval development of the maternal generation. To terminate diapause, prepupae of the maternal generation are kept at 4–5 °C in the dark. To estimate the ability to enter diapause, the progeny generation is incubated at 14 °C. The results suggest that the inhibition of the tendency to enter diapause in the progeny of T. telengai females that have undergone diapause is caused by diapause itself rather than by diapause‐inducing or diapause‐terminating environmental factors. This result can be used to clarify the mechanism of the inhibition of diapause in the progeny of females that have undergone diapause.     

Effect of photoperiod on the development and diapause of the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)

To investigate the physiology of Chrysopa pallens, the effect of photoperiod on diapause and development was examined in a Japanese population (33.4°N). The response stage for diapause of C. pallens was considered to be the prepupal stage. The critical photoperiod for diapause induction at 20.0°C was between 13 h light : 11 h dark (LD 13:11) and LD 14:10. The larval developmental period was affected by photoperiod: larvae in diapause took longer to complete their development. This difference of larval developmental period in relation to photoperiod was considered to be an adjustment of larval diapause timing.     

Photoperiod- and temperature-dependent induction of larval diapause in a multivoltine bruchid, Bruchidius dorsalis

The wild bruchid beetle, Bruchidius dorsalis Fahraeus (Coleoptera: Bruchidae), has a multivoltine life cycle and overwinters in several developmental stages in the middle part of Japan. We investigated the incidence of diapause under different conditions of photoperiod (from L8:D16 to L16:D8) and temperature (at 20 °C and 24 °C). Our experiments revealed the following results: (1) B. dorsalis entered diapause at the final (late fourth) instar larva under short photoperiods, (2) the larval diapause incidence was dependent on temperature (critical photoperiods were 12.5 h at 20 °C and 12 h at 24 °C), (3) some individuals did not enter diapause under short-photoperiod conditions at 24 °C, and (4) the sensitive stages to the photoperiod were from the late egg stage to the early first instar larva. Based on these results, we discuss not only the evolution of a complex overwintering strategy inB. dorsalis but also the domestication process of stored-bean pests.     

Diapause induction in the oblique-banded leafroller Choristoneura rosaceana (Lepidoptera: Tortricidae): Role of photoperiod and temperature

Induction of diapause in the larval stage of the oblique-banded leafroller, Choristoneura rosaceana (Harris), was found to be dependent on both photoperiod and temperature. At constant temperatures of 24, 20 and 16°C, short photoperiods induced diapause. The critical photoperiod was between 14–15 h of light per day at 20 and 16°C. At 14 h light: 10 h dark, all larvae expressed diapause. Temperature had a modifying effect, and slightly shifted the larval response to diapause-inducing photoperiods. High constant temperatures of 28°C and above induced diapause in some individuals (< 20%), while fluctuating temperatures of 32 and 16°C in a 12-h cycle resulted in 67% diapause induction, suggesting that diapause could also be induced by fluctuating temperatures, particularly if the higher temperature exceeds 25°C.The first- and the second-instar larvae were the only two stages sensitive to diapause induction. Exposure of adult, egg and third, fourth, and fifth-larval instars to diapause-inducing conditions did not produce diapause. Although diapause was induced in the first or the second instars, it was always expressed in the third or fourth instar.     

Photoperiod-dependent adult diapause within a geographical cline in the multivoltine bruchid Bruchidius dorsalis

Abstract The bruchid beetle Bruchidius dorsalis Fahraeus (Coleoptera: Bruchidae) has been known to undergo larval diapause during the final instar under short photoperiods ( Kurota & Shimada, 2001 ). This species has a multivoltine life cycle and the overwintering stages show a geographical variation across Japan ( Kurota & Shimada, 2002 ). In cooler areas, overwintering occurs during the final instar, whereas in warmer climates overwintering can occur during several developmental stages: non‐diapausing young instars, diapausing instars, and adults. In this study, we investigated the adult reproductive diapause in three populations from different geographical regions to clarify the role of geographical variation on overwintering strategies. We found that: (1) B. dorsalis entered reproductive diapause in addition to larval diapause under short photoperiods, (2) diapause propensity was higher and the critical photoperiod was longer in populations from cooler regions, and (3) the sensitive photoperiod range was the first 5 days after emergence. Predictions of the overwintering stage, derived from critical photoperiods, were consistent with actual overwintering stages observed in each population. The geographical variation in diapause induction is likely to reflect the adaptive overwintering strategy in each local environment.