Dissecting insect responses to climate warming: overwintering and post‐diapause performance in the southern green stink bug,Nezara viridula,under simulated climate‐change conditions

The effect of simulated climate change on overwintering and post‐diapause reproductive performance is studied in Nezara viridula (L.) (Heteroptera: Pentatomidae) close to the species' northern range limit in Japan. Insects are reared from October to June under quasi‐natural (i.e. ambient outdoor) conditions and in a transparent incubator, in which climate warming is simulated by adding 2.5°C to the ambient temperatures. Despite the earlier assumption that females of N. viridula overwinter in diapause, whereas males do so in quiescence, regular dissections show that the two sexes overwinter in a state of true diapause. During winter, both sexes are dark‐coloured and have undeveloped reproductive organs. Resumption of development does not start until late March. During winter, the effect of simulated warming on the dynamics and timing of physiological processes appears to be limited. However, the warming significantly enhances winter survival (from 27–31% to 47–70%), which is a key factor in range expansion of N. viridula. In spring, the effect of simulated warming is complex. It advances the post‐diapause colour change and transition from dormancy to reproduction. The earlier resumption of development is more pronounced in females: in April, significantly more females are already in a reproductive state under the simulated warming than under quasi‐natural conditions. In males, the tendency is similar, although the difference is not significant. Warming significantly enhances spring survival and percentage of copulating adults, although not the percentage of ovipositing females and fecundity. The results suggest that, under the expected climate‐warming conditions, N. viridula will likely benefit mostly as a result of increased winter and spring survival and advanced post‐diapause reproduction. Further warming is likely to allow more adults to survive the critical cold season and contribute (both numerically and by increasing heterogeneity) to the post‐overwintering population growth, thus promoting the establishment of this species in newly‐colonized areas.     

Insects in a warmer world: ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change

Focusing on the southern green stink bug, Nezara viridula (Pentatomidae), in central Japan the effects of climate change on true bugs (Insecta: Heteroptera) are reviewed. In the early 1960s, the northern edge of the species's distribution was in Wakayama Prefecture (34.1°N) and distribution was limited by the +5°C coldest month (January) mean temperature isothermal line. By 2000, N. viridula was recorded 70 km further north (in Osaka, 34.7°N). Historical climate data were used to reveal possible causes of the northward range expansion. The increase of mean and lowest winter month temperatures by 1–2°C in Osaka from the 1950s to the 1990s improved potential overwintering conditions for N. viridula. This promoted northward range expansion of the species. In Osaka, adult diapause in N. viridula is induced after mid‐September, much later than in other local seed‐feeding heteropterans. This late diapause induction results in late‐season ineffective reproduction: some females start oviposition in autumn when the progeny have no chance of attaining adulthood and surviving winter. Both reproductive adults and the progeny die. A period from mid‐September to early November represents a phenological mismatch: diapause is not yet induced in all adults, but it is already too late to start reproduction. Females that do not start reproduction but enter diapause in September have reduced postdiapause reproductive performance: they live for a shorter period, have a shorter period of oviposition and produce fewer eggs in smaller egg masses compared with females that emerge and enter diapause later in autumn. To some extent, N. viridula remains maladapted to Osaka environmental conditions. Ecological perspectives on establishment in recently colonized areas are discussed. A review of available data suggests that terrestrial and aquatic Heteroptera species respond to climate change by shifting their distribution ranges, changing abundance, phenology, voltinism, physiology, behaviour, and community structure. Expected responses of Heteroptera to further climate warming are discussed under scenarios of slight (<2°C) and substantial (>2°C) temperature increase.     

Dispersion of flightless adults of the Asian lady beetle, Harmonia axyridis, in greenhouses containing cucumbers infested with the aphid Aphis gossypii: effect of the presence of conspecific larvae

Nezara viridula (L.) (Heteroptera: Pentatomidae) recently expanded its distribution range in Japan and reached Osaka. In the southern temperate zone, the species overwinters in the adult stage and reproductive diapause is associated with a body colour change from green to russet. In Osaka, the reproductive diapause is only induced in September–October and nymphs from late egg masses are destined to die during winter. However, the fate of adults emerging late in the season remained unknown. Survival, body colour change, and post‐diapause reproduction were studied under quasi‐natural conditions in Osaka in 1999–2000 in those adults that attained adulthood as late as in November. Two experimental cohorts were used: in the Outdoor cohort, insects were reared outdoors starting in their second instar (28 September); in the Laboratory cohort, nymphs and subsequently adults were reared from the same day under diapause‐inducing conditions (L10:D14 at 25 °C), then acclimatized (5 days at 20 °C and 5 days at 15 °C; L10:D14) and transferred outdoors on 1 December. Adults in both cohorts did not reproduce in autumn and survived the winter with a low mortality. More than 20% of adults in the Outdoor cohort failed to change body colour from green to russet during winter, apparently because of the low ambient temperature, suggesting that the environmental conditions required for colour change do not completely coincide with those required for diapause induction, and that the colour of the adults is not always a reliable indicator of diapause in this species. After overwintering, females from the Outdoor cohort produced significantly fewer egg masses and eggs and had a significantly shorter period of oviposition than females that entered diapause under short‐day conditions in the Laboratory cohort. Thus, if progeny from the late egg masses attain adulthood late in the autumn, these adults have high chances of successful overwintering, but their reproductive output after the winter diapause is significantly reduced.     

Some like it hot! Rapid climate change promotes changes in distribution ranges of Nezara viridula and Nezara antennata in Japan

We compared past and current limits of the distribution range of the southern green stink bug, Nezara viridula (L.) (Heteroptera: Pentatomidae), in central Japan. In the early 1960s, the northern limit of the range was in Wakayama Prefecture and was limited by a +5 °C isothermal line for the mean January temperature. In 2006–2007, a new survey demonstrated that this northern limit had shifted northwards by 85 km (i.e., at a mean rate of 19.0 km per decade). The shift was most likely promoted by milder winter conditions. The mean January to February temperature in the region was 1.03–1.91 °C higher in 1998–2007 than in 1960–1969. The number of cold days (with the mean temperature below +5 °C) also significantly decreased, while the annual lowest temperature significantly increased. Nezara viridula was found mostly close to those locations where (i) the mean January temperature exceeded +5 °C, (ii) the mean number of cold days did not exceed 26 in January to February, and (iii) where the mean annual lowest temperature did not drop below –3.0 °C. The general linear model shows that the mean January temperature and number of cold days are the most important factors controlling the northern limit of distribution of N. viridula. All the climatic data suggest that over the last 45 years, environmental conditions have become more favourable for overwintering of N. viridula at many locations in central Japan. This has probably promoted the northward spread of the species, representing a direct response to climate warming. A sympatrically distributed congeneric, Nezara antennata Scott, seems to respond to the warming by a retreat from the ocean coast towards cooler elevated habitats, which might be a complex response to elevated temperature and interspecific mating with N. viridula. It is suggested that the range changes in both species will continue in response to further climate change.     

Timing of diapause induction and its life‐history consequences in Nezara viridula: is it costly to expand the distribution range?

Abstract. 1. From the early 1960s to 2000 Nezara viridula (Heteroptera: Pentatomidae) expanded its range northwards in Japan and reached Osaka following climate warming recorded in the region. 2. The timing of diapause induction and its effect on life‐history traits were studied under quasi‐natural conditions in Osaka. Egg masses were placed outdoors in six series in July–November 1999. Developmental events were monitored until September 2000. 3. Adult diapause was induced in September–October in agreement with the photoperiodic response obtained under laboratory conditions. Induction of diapause in early October ensured the highest winter survival. Nymphs that hatched after late September died by December–April showing that the species cannot survive winter in the nymphal stage. 4. Life‐history traits varied between the early (non‐diapause reproduction) and late (post‐diapause reproduction) series. Thus, non‐diapause females produced significantly fewer egg masses than did females that reproduced only after diapause. The timing of diapause induction strongly affected overwintering success and post‐diapause performance: females that became adults and entered diapause in October lived longer, had a longer period of oviposition, and produced more eggs in larger egg masses than females that attained adulthood and entered diapause in September. 5. Females from the early series reproduced until late November, although progeny from the late September eggs were destined to die during the winter. Pre‐winter reproduction of adults that emerged in mid‐September or later was a result of the imperfect timing of diapause induction. It is an ineffective allocation of resources and may be considered the ecological cost of range expansion. 6. To establish in the region, N. viridula will probably evolve a lengthening of the critical photoperiod of the diapause induction response. This will allow the species to enter diapause earlier and, thus, avoid maladaptive late‐autumn reproduction but, perhaps, increase the cost of diapause because of a possible adverse impact of pre‐winter high temperature conditions on overwintering.     

Photoperiodic response in the subtropical and warm‐temperate zone populations of the southern green stink bug Nezara viridula: why does it not fit the common latitudinal trend?

The photoperiodic response of diapause induction is studied in females of five subtropical and warm‐temperate zone populations of Nezara viridula (L.) (Heteroptera: Pentatomidae) in Japan (26.4–34.7°N; 127.4–135.7°E). Laboratory tests at 25 °C demonstrate that both warm‐temperate and subtropical populations have pronounced photoperiodic responses of adult diapause induction. Under short‐day conditions (LD 10 : 14 h), 73–100% of females enter diapause, whereas, under long‐day conditions (LD 15 : 9 h), 87–100% of females are nondiapause and reproduce. When the critical photoperiod for diapause induction is plotted against the latitude of origin of each population, the data points do not show the expected tendency of increasing critical photoperiod northwards but, instead, vary between 12 h 15 min and 13 h 30 min. It is suggested that adults from different populations of such a highly migratory species move often among subtropical islands (by themselves or being assisted by typhoons), thus constantly destabilizing the photoperiodic responses. Although important for general synchronization of seasonal development in the tropics and subtropics, winter diapause might not be so critical for survival in mild winters in these zones. Such circumstances might make the selective pressure over the photoperiodic response less severe in the tropics and subtropics than in the temperate zone. It is suggested that the current climate warming might contribute to this situation as well by promoting polewards migrations and lessening the selective pressure of overwintering conditions.     

Photoperiodic control of diapause termination, colour change and postdiapause reproduction in the southern green stink bug, Nezara viridula

Abstract.  The effects of day length on adult diapause development, associated with diapause body colour change as well as postdiapause reproduction are studied in Nezara viridula from Japan. Facultative diapause spontaneously terminates under three constant short-day and near-critical photoperiods at 25 °C without low temperature treatment. The period required for body colour change from russet to green and the precopulation and preoviposition periods differ significantly between the photoperiodic treatments, being shortest under LD 13 : 11 h, intermediate under LD 12 : 12 h and longest under LD 10 : 14 h. Photoperiodic conditions do not affect postdiapause reproductive performance: the total egg production, duration of the period of oviposition and other reproductive indices do not differ significantly between the photoperiodic conditions. The total egg production depends on the duration of the period of oviposition but not on how long females remained russet during diapause. It is concluded that diapause in N. viridula does not require low temperature for its successful completion and diapause duration affects winter survival but not postdiapause reproductive performance or longevity. Such independence of the postdiapause reproductive performance from the duration of diapause may have contributed to the continuous worldwide range expansion of this species into temperate zone.     

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.     

Too hot to handle? Phenological and life‐history responses to simulated climate change of the southern green stink bug Nezara viridula (Heteroptera: Pentatomidae)

The effect of simulated climate change on Nezara viridula was studied close to the species' northern range limit in Japan. Insects from the same egg masses were reared for 15 months in 10 consecutive series under quasi‐natural (i.e. outdoor) conditions and in a transparent incubator, in which climate warming was simulated by adding 2.5 °C to the outdoor temperature. The warming strongly affected all life‐history and phenological parameters. In the spring, the simulated warming advanced the timing of postdiapause body colour changes and reproduction. In the early summer, it increased egg production and accelerated nymphal development. In the late summer (the hottest season), the effect of the simulated warming was strongly deleterious: nymphs developed slowly, suffered higher mortality and had difficulties during final moulting; the emerged females were smaller, some exhibited abnormal cuticle, produced fewer eggs and had a decreased life span. In the autumn, the warming accelerated nymphal development, resulted in larger female size, affected the timing of the diapause‐associated adult body colour change from green to russet and enhanced preparation for overwintering. Larger females had higher winter survival rate than smaller females. The warming strongly increased survival rate in both size classes and allowed smaller females to reach the same winter survival rate as larger females had under the quasi‐natural conditions. The winter survival also differed between the green and dark‐coloured females under the quasi‐natural, but not under the warming conditions. However, under the warming conditions, green females survived the winter even better than dark‐coloured females did under the quasi‐natural conditions. The warming also shortened the life span of females from the summer generations and prolonged it in those from the autumn generation. It is concluded that even a moderate temperature increase (+2.5 °C) in the future is likely to have a complex influence upon insects, strongly affecting many of their life‐history and phenological parameters.     

The Effect of Seasonal Changes on Nezara viridula (L.) (Hemiptera: Pentatomidae) and Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in Hawaii

The effect of seasonal changes in temperature and photoperiod on the interaction of Nezara viridula (Hemiptera: Pentatomidae) and its egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae) was investigated in the laboratory. We found no evidence of reproductive diapause in N. viridula under simulated Hawaiian summer and winter conditions. Further, although “diapause” coloration was obtained in the laboratory, it was not correlated with reproductive status. Studies of the survival of T. basalis provided with honey under the same simulated conditions showed that under summer conditions, only 2.1% of the female and 13.5% of the male population were still alive by 60 days. When provided with N. viridula egg masses at 30 days, 79.4% of the eggs were parasitized in a 3-h period. Under winter conditions, 54.3, 28.3, and 14.5% of the females were alive at 30, 60, and 90 days after adult emergence. When provided with N. viridula egg masses at 30, 60, and 90 days for 3 h, 57.6, 32.8, and 47.1% of the eggs were successfully parasitized. These studies suggest the limiting factor in the interaction of T. basalis and N. viridula is not reproductive diapause, but instead the ability of T. basalis to survive summer conditions.     

An evaluation of some natural enemies of >Nezara viridula in northern California

Natural enemies associated with eggs of >Nezara viridula (L.) (Heteroptera: Pentatomidae) wereevaluated by placing sentinel egg masses inweeds and cultivated tomato and bean crops innorthern California. Egg predation wasgenerally less than 10% and normally involvedpredators with chewing mouth parts. Predatorsseldom destroyed an entire egg mass, typicallyeating <40 eggs per exploited mass.Laboratory evaluation of >25 species ofpotential arthropod predators revealed that fewfed on >N. viridula eggs to any extent;however, numerous species fed on >N.viridula nymphs. Five species of eggparasites were recovered from sentinel eggmasses: >Trissolcus basalis (Wollaston),>Gryon obesum Masner and >Telenomuspodisi Ashmead (Scelionidae); and>Ooencyrtus californicus Girault and >O.johnsoni (Howard) (Encyrtidae). The major eggparasite was >T. basalis, the only exoticmember of the parasite guild; it typicallyparasitized 100% of the eggs in an exploitedegg mass. The results indicate thatparasitization of eggs and predation of smallnymphs can be important biotic mortalityfactors for >N. viridula populations innorthern California. It is suggested that acombination of factors – viz., eggparasitization, nymphal predation, regionalshortage of overwintering sites, and localshortages of suitable hosts – maintains thisexotic pest at relatively low levels in theregion.     

Photoperiodic and temperature control of diapause induction and colour change in the southern green stink bug Nezara viridula

Abstract. The effect of photoperiod and temperature on the duration of the nymphal period, diapause induction and colour change in adults of Nezara viridula (L.) (Heteroptera: Pentatomidae) from Japan was studied in the laboratory. At 20 °C, the developmental period for nymphs was significantly shorter under LD 10 : 14 h (short day) and LD 16 : 8 h (long day) than under intermediate photoperiods, whereas at 25 °C it was slightly shorter under intermediate than short- and long-day conditions. It is assumed that photoperiod-mediated acceleration of nymphal growth takes place in autumn when day-length is short and it is unlikely that nymphal development is affected by day-length under summer long-day and hot conditions. Nezara viridula has an adult diapause controlled by a long-day photoperiodic response. At 20 °C and 25 °C in both sexes, photoperiodic responses were similar and had thresholds close to 12.5 h, thus suggesting that the response is thermostable within this range of temperatures and day-length plays a leading role in diapause induction. Precopulation and preoviposition periods were significantly longer under near-critical regimes than under long-day ones. Short-day and near-critical photoperiods induced a gradual change of adult colour from green to brown/russet. The rate of colour change was significantly higher under LD 10 : 14 h than under LD 13 : 11 h, suggesting that the colour change is strongly associated with diapause induction. The incidences of diapause or dark colour did not vary among genetically determined colour morphs, indicating that these morphs have a similar tendency to enter diapause and change colour in response to short-day conditions.     

The impact of global warming and land-use change on the pest status of rice and fruit bugs (Heteroptera) in Japan

Infestation by rice and fruit bugs (Heteroptera) became a nationwide problem in Japan in the early 1970s. Nine rice bug species and three fruit bug species have been designated as economically important. Cropping restrictions for rice produced fallow paddy fields where various rice bugs reproduced and became abundant. Plautia crossota stali, Halyomorpha halys and Glaucias subpunctatus are dominant species of fruit bug that cause damage to a range of fruit crops. However, they require cones in order to complete their life cycle. Coniferous trees planted in the 1950s bore cones after 20 years. A dry and hot summer contributes to good masting the following year and good cone production, in turn, contributes to the abundance of fruit bugs in the third year. Thus, there is strong circumstantial evidence that land‐use changes were responsible for the abundance of both rice and fruit bugs during the last 30 years. Poleward range expansion was observed in Nezara viridula, Leptocorisa chinensis, G. subpunctatus and Paradasynus spinosus. A survey conducted to assess winter mortality revealed that every 1 °C rise in mean winter temperature resulted in a reduction of about 15% in winter mortality of N. viridula and H. halys in localities where the mean winter temperature ranges from 2 to 6 °C. In general, species with low developmental zero (T₀) and small thermal constant (K) show the greatest increase in annual number of generations. Species with a high T₀ for preoviposition period show the greatest increase in reproductive activity, while overwintering insects with a lower T₀ tend to appear earlier in response to the elevation of temperature. Numbers of warnings issued by the prefectures on the occurrence of rice bugs and fruit bugs were correlated. Recent global warming operates in various ways, (e.g. by increasing annual number of generations, reproductive activity and food, to produce such correlation). There are no substantial bug problems in Korea where no significant land‐use changes have occurred. Rice bug outbreaks in Japan are predicted to become less frequent in the future, because there is no further scope for cropping restriction. Planting of coniferous trees has been continuously decreasing since 1970, but the area of coniferous forest is still almost the same. This suggests that the fruit bug problem will continue for the foreseeable future.     

Energy storage during reproductive diapause in the Drosophila melanogaster species group

Summary Temperate species of the Drosophila melanogaster group enter reproductive diapause for overwintering in response to short daylength. During the prediapause period they accumulate triacylglycerols, but not glycogen, as energy resources. The capacity for storing triacylglycerols differs between species, and appears to be closely correlated with diapause and cold-hardiness; cool-temperate species, such as those of the auraria species complex, which enter a deep diapause and are highly cold-hardy, accumulate larger quantities of triacylglycerols than warm-temperate species, such as D. rufa and D. lutescens, which enter a weak diapause and are less cold-hardy. Among the cool-temperate spcies, D. subauraria occurs at a higher latitude and has the greatest capacity for accumulating triacylglycerols. A subtropical species, D. takahashii, which has no diapause in nature and is not cold-hardy, is unable to store the same quantities of triacylglycerols as temperate species.     

Sexual dimorphism in photoperiodic plasticity of body mass in the green dock leaf beetle <Emphasis Type="Italic">Gastrophysa viridula</Emphasis> (Coleoptera,Chrysomelidae)

Sexual dimorphism in body mass was studied in prepupae, pupae and immature adults of the green dock leaf beetle Gastrophysa viridula under a constant temperature of 24°C and two photoperiods (12L:12D and 22L:2D). Females were significantly heavier compared to males at all the three developmental stages; just after emergence from pupae they weighed, on average, 11.4 mg, while males—10.3 mg. Sex differences in photoperiodic body mass plasticity were revealed: under short-day conditions pupal and adult mass in females was significantly higher compared to long day, but not in males. Such a response to short day (the factor inducing reproductive diapause in this species) is likely to promote accumulation of greater amount of nutrients by females which is necessary for earlier oviposition after overwintering.     

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.     

Studies on the adult polymorphism in the southern green stink bug,Nezara viridula (hemiptera: Pentatomidae)

Polymorphism in adult colour pattern of Nezara viridula is determined on the genetic basis. The basic colour patterns of adult are classified into four types, i. e. G, O, R and F. No appreciable differences between these types were observed in respect to various physiological traits of nymphs and adults, except that type G seems to be superior in reproductive ability but to be inferior in ability of surviving winters at least to types R and F. Inter-generation changes in percentage frequency of G type were examined from 1959 to 1967 covering more than 30 generations. Percentage frequencies of G types prior to the severe winter of 1962–3 fluctuated greatly around a mean of 87.9%, while they did to a lesser extent than before with a mean of 85.0% after the winter. Unexpected high percentages of G type were recorded frequently in summer generations, viz. 1st and 2nd. On the other hand, the relative frequencies of G and O types decreased after hibernation in contrast to the increases in those of F and R. This sort of changes in genetic composition related to the winter of 1962–3 was observed in several populations segregated from each other. This seasonal alternation of selective activity in the environments is considered to be responsible for retention of the polymorphism. Alternative possible causes, i. e. difference in habitat preference, non-random mating and selective predation by predators among polymorphs, may safely be rejected as irrelevant to the mechanism in maintaining polymorphism. The polymorphism of this insect seems to be in a transient state rather than balanced one contributing little to population regulation, but the persistence of N. viridula in the periphery range may be assisted by retention of the polymorphism.     

Rapid evolution of photoperiodic response in a recently introduced insect Ophraella communa along geographic gradients

The introduced beetle Ophraella communa was first found in 1996 in Japan and has rapidly expanded its distribution to include regions that encompass a wide range of latitude and altitude and are dominated by different host‐plants. In this study, we investigated geographic variation in its photoperiodic response for the induction of reproductive diapause, with which the beetle adjusts its life cycle to local climate and host‐plant phenology. The beetle lines were collected from 18 sites in Japan. The diapause incidence under a photoperiodic condition of 13 h light : 11 h dark (LD 13:11) and the critical day length differed among the beetle lines. Analysis with the generalized linear model showed that latitude, altitude and host‐plant species (Ambrosia artemisiifolia vs. Ambrosia trifida) had significant effects on diapause incidence under LD 13:11. These results suggest that the O. communa populations have rapidly adapted to local environmental conditions after their colonization. However, the photoperiodic response of the O. communa population in Tomakomai, the northernmost part of its distribution range in Japan, deviated significantly from the general trend. We suggest that this deviation is attributed to either: (i) that this beetle has colonized Tomakomai more recently compared to the other sites; or (ii) that the Tomakomai population has adapted to local environments in a different way from other populations.     

Geographic variability in diapause response of Japanese Orius species

Interspecific and latitudinal variation in diapause characteristics were examined in 12 strains of Orius species (Heteroptera: Anthocoridae) including O. sauteri (Poppius), O. nagaii Yasunaga, O. minutus (L.), O. strigicollis (Poppius), and O. tantillus (Motschulsky) from Japan. A latitudinal cline was found in the photoperiodic response controlling reproductive diapause: the lower the latitude, the lower the diapause incidence and the shorter the critical daylength. To examine the overwintering success, eight strains including four species derived from different latitudes (26–43° N) were reared outdoors in Tsukuba (36° N), central Japan from the autumn of 1998 to the summer of 1999, and their winter survival and spring fecundity were recorded. Most females of the northern strains entered diapause in the autumn when the temperature was still high, and died before winter without oviposition. In the southern strains including a nondiapause Okinawa (26° N) strain of O. strigicollis, females overwintered as well as native strains in a state of quiescence. In all strains, the winter survival was significantly lower in males than in females, and eggs and nymphs failed to overwinter.     

Seasonal cycles in stink bugs (Heteroptera,Pentatomidae) from the temperate zone: Diversity and control

The paper reviews the diversity of seasonal cycles known in stink bugs (Heteroptera, Pentatomidae) from the temperate zone and is based on the data of 43 pentatomid species studied in detail up to date (Saulich and Musolin, 2011). All the seasonal cycles realized by pentatomids in the temperate zone can be divided into two large groups: univoltine and multivoltine cycles. In univoltine cycles, only one generation is annually realized. However, univoltinism of a particular species or population can be ensured by different mechanisms: its control can be endogenous (involving an obligate diapause) or exogenous (environmental, involving a facultative diapause). Furthermore, endogenously controlled univoltine seasonal cycles can include obligate embryonic (egg) diapause (e.g., Picromerus bidens and Apateticus cynicus), obligate nymphal diapause (e.g., Pentatoma rufipes) or obligate adult (reproductive) diapause (e.g., Palomena prasina, Palomena angulosa, and Menida scotti). Exogenously controlled seasonal cycles are more flexible. Many species that are multivoltine in the subtropical or warm temperate zones are univoltine further polewards. In this case, their univoltinism is controlled exogenously, or environmentally. The mechanism often involves such seasonal adaptations as photoperiodic response of facultative winter diapause induction with a high thermal optimum (e.g., Arma custos and Dybowskyia reticulata) or a high critical threshold of winter diapause induction response (e.g., Graphosoma lineatum). The seasonal cycles of some species include not only winter diapause (hibernation) but also summer diapause (aestivation). The diapausing stage can be the same (e.g., Nezara antennata has facultative adult winter and summer diapauses) or different (e.g., Picromerus bidens survives winter in obligate embryonic diapause and spends the hottest period of summer in facultative adult aestivation). All the multivoltine cycles follow the same general pattern, with one, two, or even more directly breeding generation(s) followed by a generation that enters winter diapause. However, this sequence may be complicated by incorporation of specific seasonal adaptations such as aestivation, migrations, different forms of seasonal polyphenism or polymorphism (e.g., seasonal changes of body color), etc. Many stink bugs demonstrate geographic clines of voltinism, producing several generations in the subtropical regions (environmentally controlled multivoltine development) and two or only one generation(s) polewards (environmentally controlled bi- or univoltinism). However, some species demonstrate a strictly bivoltine seasonal cycle: they always produce two annual generations, each with either winter or summer diapause. An example is Nezara antennata which produces two generations and enters facultative winter and summer diapauses. Semivoltine seasonal cycles last more than one year. They are not very rare among insects and are known in true bugs, but have not yet been recorded among pentatomids. Examples of different seasonal cycles are described and discussed in detail. Further discussion is focused on the ecological importance of photoperiodic and thermal responses in cases of natural or artificial dispersal of pentatomids beyond their original ranges. The phytophagous Nezara viridula and the predatory Podisus maculiventris and Perillus bioculatus are used as examples. An attempt is made to compare the phylogeny of Pentatomidae and distribution of realized patterns of their seasonal development. However, it is concluded that reconstruction of phylogenetic relationships cannot yet provide a sufficient basis for prediction of realized seasonal cycles. It is suggested that the terms uni-, bi-, multi-, and semivoltinism should refer to populations rather than species, since the realized patterns of seasonal development often differ between the northern and southern populations of the same broadly distributed species.