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Studies on the phenology of local populations of invasive insects are necessary for monitoring and predicting their dispersion. We investigated the phenology of the brown marmorated stink bug

Facultative winter adult diapause in

The available data on seasonal development of plant bugs (Mirinae: Mirini) are reviewed, and the level of understanding of their seasonal adaptations is evaluated. The ecological responses involved in control of seasonal development of 14 species from 5 genera (Adelphocoris, Apolygus, Lygus, Lygocoris, and Stenotus) are analyzed in detail. All the studied species are broadly polyphagous and produce a varying number of annual generations in different climatic zones. The studied members of four genera, namely Adelphocoris, Apolygus, Lygocoris, and Stenotus, hibernate at the embryonic stage while bugs of the genus Lygus do so at the adult stage. Some species of the genera Adelphocoris and Lygus, in particular Lygus pratensis, have acquired a pronounced ability to fly over long distances, facilitating the search for flowering vegetation. However, unlike many insects that make distant migrations in the state of adult diapause, females of plant bugs of the genus Adelphocoris migrate with mature eggs in their oviducts. This feature allows Adelphocoris females to successfully colonize new areas even in the absence of males, since females do not need additional mating in the colonized area. For the majority of Mirini species experimentally studied in the laboratory, the temperature parameters of development and the sum of effective temperatures needed to complete the full generation were calculated. When combined with observations done under natural conditions, these data allowed us to determine the exact number of annual generations produced by the species or population. The role of day length in the control of seasonal development was analyzed in detail in three species of the genus Adelphocoris: A. triannulatus, A. suturalis, and A. lineolatus. The conditions inducing and terminating adult diapause were studied in detail in Lygus hesperus in the southern United States. The seasonal development of Lygocoris pabulinus is an unusual example of an obligate host plant change during the year. The diapausing eggs of this species overwinter in the tissues of woody plants but the nymphs then migrate onto herbaceous plants on which the summer generations develop. Such a seasonal strategy is more characteristic of aphids (Homoptera) than of true bugs (Heteroptera). On the whole, our analysis of the available data indicates that the control of seasonal development of plant bugs of the subfamily Mirinae is still poorly understood despite their high economic importance. Most reports deal with a small number of experimentally studied species and are limited to the data on temperature parameters of development. The important role of photoperiodic adaptations in the control of seasonal development has been demonstrated only for a few well-studied species (e.g., Adelphocoris triannulatus); such data are crucial for analysis and prediction of seasonal development and spread of harmful and beneficial insects, since the seasonal cycle of each population of a given species is strictly synchronized with the local conditions.

Data on seasonal development of plant bugs from subfamily Bryocorinae (Miridae) are reviewed and analyzed. All of the species of bryocorines whose seasonal development has been studied so far belong to the tribe Dicyphini, owing to the latter’s economic importance as agents of biological control in greenhouses. Macrolophus melanotoma, M. pygmaeus, and Nesidiocoris tenuis have homodynamic seasonal development and the lower developmental threshold of about 8–9°C. If food is available, they can remain active all year round and produce annually a varying number of generations, depending on the local climatic conditions. To survive adverse low-temperature winter conditions these species use various natural protected microhabitats and can overwinter at different developmental stages. The other two bryocorines studied (Dicyphus errans and D. hesperus) exhibit heterodynamic seasonal development and overwinter in the state of adult diapause. Induction of this diapause is controlled by a long day-type photoperiodic response. Also, the nymphal growth rate of D. errans is affected by day length and this quantitative photoperiodic response ensures that nymphs of this species reach the diapausing stage (adult) in appropriate time, which is crucial for successful overwintering. The threshold photoperiod for induction of winter adult diapause varies with latitude in D. hesperus, only nymphs being sensitive to day length in this species. Pilot experimental studies should precede any planned introduction of a biocontrol agent, as these may reduce the risk of invasions. During the early stages of settling in a new area, it is seasonal adaptations controlling development of bug populations in their natural environments that are particularly important. In greenhouses, higher efficiency of biocontrol measures can be achieved with southern multivoltine populations of homodynamic species, especially if these grow rapidly as immatures, have high reproduction rates at the adult stage, and easily switch to novel prey. Under field conditions, polyphagous heterodynamic univoltine species and populations with deep obligate diapause are more likely to naturalize successfully.

Invasive pentatomid Halyomorpha halys recently arrived to the Black Sea region and began damaging agricultural and ornamental plants. We studied the effects of day length and temperature on the pre-adult development and diapause induction in H. halys from Sochi (Russia) under laboratory conditions (20, 24, and 28 °C and several photoperiods). The pre-adult development of H. halys was noticeably faster under L:D 12:12 compared with L:D 15:9. The sum of effective temperatures required for the pre-adult development was ca. 530 and 590 degree days under these two conditions, respectively, whereas the lower developmental thresholds were similar (ca. 13.3 °C). Adults of H. halys demonstrated a typical long-day-type photoperiodic response of facultative winter adult diapause induction: Short days (photophases of 12–15 h) induced diapause in all adults, whereas long days (with photophases longer than 15 h) promoted reproduction. The photoperiodic responses of diapause induction of females and males were very similar. At 24 °C, the threshold of the response was between 15 and 16 h. At 20 °C, even under the very long-day conditions (L:D 18:6) about 50% of adults entered diapause. Field records suggest that H. halys likely produces two generations per year in Sochi. Short days might accelerate nymphal growth of the second generation in August and then induce winter diapause in adults. Phenological studies and monitoring are needed for a better understanding of the adaptation process of this invasive pest to new conditions.

Facultative winter adult diapause in Halyomorpha halys is regulated by a long-day photoperiodic response. Day length also influences nymphal development, which slows down at the critical (near-threshold) day lengths. We compared the photoperiodic responses of one native (Andong, South Korea) and three invasive (Torino, Italy; Basel, Switzerland; and Sochi, Russia) populations in a laboratory common-garden experiment. Nymphs developed and emerging adults were reared at 24 °C in a range of photoperiods with day lengths of 14.0, 14.5, 15.0, 15.5, and 16.0 h. The critical day lengths of the photoperiodic responses of both sexes fell between 14.5 and 15.0 h in the native Korean population and between 15.0 and 15.5 h in three invasive European populations. The differences between the three invasive populations were not significant, despite their distant origins. Moreover, the difference between the Korean and European populations was much smaller than was expected. The microevolution was possibly ‘too slow to keep up’ with the rapid spread of the invader across Eurasia. It is expected that soon the critical day length of the invasive H. halys populations will gradually change to adapt better to local conditions. At present, the critical day length for diapause induction of 15 h 15 min can be used to model the phenology, further spread, and response to climate change for all European populations of the pest.

Insects living in the temperate climate include summer diapause, or aestivation, in their seasonal cycle to solve various problems related to adaptation to unfavorable seasons. Unlike winter diapause, summer diapause occurs in summer and is usually terminated in autumn when active feeding, development, and/or reproduction are restored. Typically, high temperature and long day induce summer diapause and then maintain it, whereas short day and low temperature prevent induction of this diapause or terminate it. The summer diapause syndrome is basically similar to that of winter diapause; it includes prior development of large fat body, decreased level of metabolism, increased general resistance to unfavorable abiotic and biotic conditions, etc. Inhibition of morphogenesis and gametogenesis is under the control of the endocrine system. The onset of summer diapause is often accompanied by migrations to varying, sometimes significant distances to the sites of aestivation. The selective factors responsible for evolution of summer diapause vary between insect species. Climatic factors and, consequently, availability and abundance of food, as well as pressure of predators and parasites are likely to be the main factors that stimulate its occurrence. In some species, prolonged diapause begins in spring or early summer and ceases only after over-wintering. When studied in detail, such prolonged diapause often turns out to be a sequence of two independent diapauses, summer and winter ones, occurring in succession without detectable external changes.

Halyomorpha halys is native to Asia, but was recently accidentally introduced to North America and Europe. This species was recorded for the first time in Russia in 2013 (2014) and in both Serbia and Abkhazia in 2015. In 2015–2017, we conducted surveys in Russia, Serbia, and Abkhazia and found that H. halys had not only successfully survived its first winters in new regions, but also started to establish locally, spread, increase populations, and damage local crops. In Sochi (Russia) and Abkhazia, H. halys was recorded to feed on 32 species and cultivars from 16 plants families. In Serbia, it has so far been observed on only four species from four plant families. H. halys is already widely spread in Abkhazia and causes serious damage to many crops: in 2016, the yield of peach, mandarin orange, persimmon and other crops fell down by 13.2–87.4% if compared to the long-term means of yield. The losses are likely to be mostly caused by feeding of H. halys. We conclude that H. halys was accidentally introduced to Russia in 2012–2013 most likely with woody plants imported to Sochi from Italy or Greece for urban landscaping before the 2014 Winter Olympics. The species established in Sochi and quickly moved to Krasnodar (Russia), Abkhazia, and beyond—to Georgia. Populations in Serbia most likely arrived in 2015 traveling on railway cars or in commodities on the Bucharest–Belgrade railway line. We discuss phenology and prospects of further expansion of H. halys in Europe.

Analysis of data on seasonal development of noctuid moths of the subfamily Plusiinae shows that the control of their seasonal cycles is poorly understood. At the same time, the available data demonstrate considerable diversity of the seasonal patterns of Plusiinae species from different regions. The homodynamic type of seasonal development has been found in Trichoplusia ni and Ctenoplusia agnata of the tribe Argyrogrammatini and in Autographa gamma of the Plusiini. The seasonal development of these southern noctuids is accompanied by regular interzonal migrations of flying adults. When spreading northwards, they can produce a different number of annual generations, depending on the local climatic conditions, and establish temporary local populations whose longevity is limited by the available thermal resources. Adults of some species may fly back southwards, but it is more likely that individuals from temporary local populations cannot survive long winters and are destined to die. The heterodynamic type of seasonal cycles allows insects to survive in the regions with pronounced seasonality of climate. This type of seasonal development includes univoltine, multivoltine, and semivoltine seasonal cycles. Univoltine seasonal cycles with obligate diapause are known in Autographa buraetica, A. excelsa, and Syngrapha ain (Plusiini). Diapause provides tolerance to both low temperatures and a prolonged period when food is unavailable. In Syngrapha ottolenguii (Plusiini), the same result is achieved by inclusion of two photoperiodically controlled diapauses (winter larval and summer adult ones) into the life cycle. The semivoltine seasonal cycle has been reported in only one species of Plusiinae, namely Syngrapha devergens. Larvae of this moth overwinter twice before pupation. Multivoltinism is common in the tribe Plusiini. Depending on the latitude, different species of this tribe can produce up to four generations per year and overwinter as middle-instar larvae in the state of facultative diapause. However, the characteristics of diapause vary substantially between the species: diapause can be deep and stable (as in Diachrysia chrysitis, Plusiini) or unstable and thus not ensuring successful overwintering and steady population growth (as in Macdunnoughia confusa, Plusiini). The seasonal adaptations known in Plusiinae include migrations, winter and summer diapauses, photoperiodic control of larval growth rates, and seasonal polyphenism of larval body coloration. In general, seasonal adaptations of Plusiinae are determined by local environmental conditions and only loosely associated with the systematic position of particular taxa. Only the tribe Abrostolini stands apart from other taxa of Plusiinae: moths of this tribe differ not only in morphology but also in peculiarities of their seasonal development, because all the species of this tribe overwinter as pupae and their seasonal cycles are therefore different from those of the rest of Plusiinae.

The influence of photoperiod and temperature on the growth and development of the scarce silver-lines Bena bicolorana (Fuessly, 1775) (Lepidoptera, Noctuidae) was studied in Belgorod Province, Russia (50°N, 36°E). At temperatures of 21 and 24°C, all photoperiodic regimes with 12 to 17 h of light per day induced diapause in the IV instar larvae. At 24°C, under long-day conditions with a photophase of 18 h, both diapausing and nondiapausing (i.e., directly developing) IV instar larvae were recorded in almost equal proportions; this photoperiodic regime may thus be considered as the threshold one. Diapause induction in B. bicolorana was associated with the larvae changing color from light green to brick-red. The larval growth rates, their weight dynamics, and timing of diapause induction are under photoperiodic control. Thus, seasonal development of B. bicolorana is controlled by two photoperiodic responses: the qualitative one that controls larval diapause induction, and the quantitative one that regulates larval growth parameters before diapause induction. In Belgorod Province B. bicolorana annually produces only one generation, what agrees well with the parameters of both of its photoperiodic responses. The results of the experimental eco-physiological studies support the separation of the monotypic genus Bena because it includes the only species in the subfamily Chloephorinae (B. bicolorana) that overwinters at the larval stage.

The paper focuses on the influence of the day length on larval and pupal development of the dark spectacle Abrostola triplasia (Lepidoptera, Noctuidae: Plusiinae, Abrostolini) in the central European Russia (50°N, 36°E). The long-day qualitative photoperiodic response of diapause induction controls formation of the winter pupal diapause and determines a bivoltine seasonal cycle of the species in the forest-steppe zone. Seasonal development of the local population of A. triplasia has the following peculiarity: if adults of the overwintered generation emerge late (in the second half of June), larvae of the first generation develop under the critical, or threshold, daylength conditions, which results in the presence of both diapausing and non-diapausing fractions of the pupae. The diapausing pupae overwinter, whereas the non-diapausing ones develop into adults that produce the second generation; the pupae of this second generation overwinter. Therefore, the hibernating population of A. triplasia consists of individuals from both generations. Thus, the dark spectacle has a very flexible seasonal development pattern in the forest-steppe zone: the presence of two generations allows the species to fully utilize the resources of the vegetation season; at the same time, the first generation already has a reserved hibernating fraction in case the weather conditions of the particular year are not favorable for completion of two generations.

The beet webworm, Loxostege sticticalis L. is a very dangerous polyphagous insect pest. The beet webworm overwinters at the pronymphal stage. In some individuals, the diapause can last from the first generation to the next spring. The influence of 30-days-long exposure at temperatures of +5, +10, +15, +20, and +25°C on survival and subsequent reactivation of diapausing pronymphs of L. sticticalis has been investigated in laboratory conditions. The beet webworm was shown to be very thermotolerant: although the temperature of +5°C, as expected, was optimal for reactivation, the other thermal regimes did not cause a significant decrease in survival and in the proportion of individuals reactivated before the end of the experiment (in 120 days). These data suggest that the southern boundary of the geographical range of L. sticticalis is determined not by high winter temperatures, but rather by some other factors (possibly, by high summer temperatures).

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.

The beet webworm, Loxostege sticticalis L., is a very dangerous polyphagous insect pest whose outbreaks periodically occur in southern Russia and northern China. The aim of our work was to describe the photoperiodic response of beet webworm populations from western (Krasnodar Territory and Rostov Province) and eastern [Buryatia and China (Hebei Province)] parts of the pest range. The insects were reared under constant photoperiods of 12–18 h and constant temperatures of 19–25°C. Incidence of diapause at different photoperiods did not show any considerable geographic differences, and the critical day length at which 50% of prepupae arrested their development was about 14–15 h in all the populations studied at experimental temperatures. The results obtained agree with the hypothesis on the existence of an area (or areas) where the pest survives during adverse periods and wherefrom it spreads when an outbreak begins (Saulich et al., 1983; Goryshin et al., 1986). Presumably, the larger part of the pest native habitats (to the north of the steppe zone) is occupied by temporary populations, incapable of surviving for long periods without an inflow of migrants from more southerly steppe regions.

Climate change (first of all the rise in temperature) is currently considered one of the most serious global challenges facing mankind. Here we review the diversity of insect responses to the current climate warming, with particular focus on true bugs (Heteroptera). Insects as ectotherms are bound to respond to the temperature change, and different species respond differently depending on their specific physiological and ecological traits, seasonal cycle, trophic relations, etc. Insect responses to climate warming can be divided into six categories: changes in (1) ranges, (2) abundance, (3) phenology, (4) voltinism, (5) morphology, physiology, and behavior, and (6) relationships with other species and in the structure of communities. Changes in ranges and phenology are easier to notice and record than other responses. Range shifts have been reported more often in Lepidoptera and Odonata than in other insect orders. We briefly outline the history and eco-physiological background of the recent range limit changes in the Southern green stink bug Nezara viridula (Heteroptera, Pentatomidae) in central Japan. Range expansion in individual species can lead to enrichment of local faunas, especially at high latitudes. Phenological changes include not only advances in development in spring but also shifts in phenology later in the season. The phenophases related to the end of activity usually shift to later dates, thus prolonging the period of active development. This may have both positive and negative consequences for the species and populations. As with any other response, the tendencies in phenological changes may vary among species and climatic zones. The proven cases of change in voltinism are rare, but such examples do exist. Application of models based on thermal parameters of development suggests that a rise in temperature by 2°C will result in an increased number of annual generations in many species from different arthropod taxa (up to three or four additional generations in Thysanoptera, Aphidoidea, and Acarina). The warming-mediated changes in physiology, morphology, or behavior are difficult to detect and prove, first of all because of the absence of reliable comparative data. Nevertheless, there are examples of changes in photoperiodic responses of diapause induction and behavioral responses related to search of shelters for summer diapause (aestivation). Since (1) individual species do not exist in isolation and (2) the direction and magnitude of responses even to the same environmental changes vary between species, it may be expected that in many cases the current stable relationships between species will be affected. Thus, unequal range shifts in insects and their host plants may disrupt their trophic interactions near the species’ range boundaries. Studies of responses to climate warming in more than one interrelated species or in entire communities are extremely rare. The loss of synchronism in seasonal development of community members may indicate inability of the higher trophic levels to adapt fully to climate warming or an attempt of the lower trophic level to escape from the pressure of the higher trophic levels. It is generally supposed that many insect species in the Temperate Climate Zone will benefit in some way from the current climate warming. However, there is some experimental evidence of an opposite or at least much more complex response; the influence of warming might be deleterious for some species or populations. It is suggested that species or populations from the cold or temperate climate have sufficient phenotypic plasticity to survive under the conditions of climate warming, whereas species and populations which already suffer from stress under extreme seasonal temperatures in warmer regions may have a limited “maneuver space” since the current temperatures are close to their upper thermal limits. Without genetic changes, even moderate warming will put these species or populations under serious physiological stress. The accumulated data suggest that responses of insects and the entire biota to climate warming will be complex and will vary depending on the rate of warming and ecological peculiarities of species and regions. Physiological responses will vary in their nature, direction, and magnitude even within one species or population, and especially between seasons. The responses will also differ in different seasons. For example, warming may negatively affect nymphal development during the hot season but at the same time accelerate growth and development during the cold season and/or ensure milder and more favorable overwintering conditions for adults. All these factors will affect population dynamics of particular species and relationships among the members of ecosystems. We should keep in mind that (1) not only selected insect species but almost all the species will be affected, (2) temperature is not the only component of the climatic system that is changing, and (3) responses will be different in different seasons. Host plants, phytophagous insects, their competitors, symbionts, predators, parasites, and pathogens will not only respond separately to climate changes; individual responses will further affect the responses of other species, thus making reliable prediction extremely complicated. Responses are expected to (1) be species- or population-specific, (2) concern basically all the aspects of organism/ species biology and ecology (individual physiology, population structure, abundance, local adaptations, phenology, voltinism, and distribution), and (3) occur at scales ranging from an undetectable cellular level to major distribution range shifts or regional extinctions. The scale of insect responses will depend on the extent and rate of climate warming. Slight to moderate warming may cause responses only in a limited number of species with more flexible life cycles, whereas a substantial increase in temperature may affect a greater number of different species and ecological groups.

The paper reviews the data on diapause and related phenomena in stink bugs (Heteroptera: Pentatomidae). Using stink bugs as examples, the consecutive stages of the complex dynamic process of diapause (such as diapause preparation, induction, initiation, maintenance, termination, post-diapause quiescence, and resumption of direct development) are described and discussed. Out of 43 pentatomid species studied in relation to diapause in the Temperate Zone up to date, the majority (38 species) overwinter as adults, two species—as eggs, and another two species—as nymphs. Pentatoma rufipes is believed to be able to overwinter at different stages of its life cycle. Less than 5 % of pentatomid species are probably able to overwinter twice. Only five species have obligate diapause, others have the facultative one. Day-length and temperature are the main diapause inducing factors in the majority of species. The role of food in the control of seasonal development is essential in the pentatomid species feeding on plant seeds. In different species, different stages are sensitive to day-length. Some pentatomids retain sensitivity to photoperiod even after diapause, others lose it and become photo-refractory (temporarily or permanently). In Pentatomidae, such seasonal adaptations as photoperiodic control of nymphal growth rates, seasonal body colour change, migrations, and summer diapause (aestivation) are widely represented, whereas wing and/or wing muscle polymorphism has not been reported yet. In the subfamily Podopinae, induction of facultative reproductive winter diapause is under the control of photoperiod and temperature. All species feed on seeds and their seasonal development to a great extent reflects availability of food. However, the same food preferences and pattern of seasonal development are also characteristic to many species from the subfamily Pentatominae. All species of the subfamily Asopinae are predators. Among them, Picromerus bidens and Apateticus cynicus have obligate embryonic winter diapause, which is rear among true bugs. At the same time, A. cynicus and Podisus maculiventris belong to the same tribe but have different types of diapause: obligate embryonic diapause in A. cynicus and facultative adult diapause in P. maculiventris. Other Asopinae species studied up to date have facultative adult diapause controlled by photoperiod and temperature with probably only one exception: in Andrallus spinidens, adult diapause is controlled by temperature, and photoperiod plays only a secondary role. Thus, in spite of the similar habits and feeding types among Asopinae, the species of this subfamily have different types of diapause and the latter is controlled by different factors. In the subfamily Pentatominae, most species overwinter as adults and induction of their diapause is controlled by the long-day type photoperiodic response, in spite of the differences in their feeding preferences (within phytophagy). However, there are some exceptions in this subfamily, too: Palomena prasina, P. angulosa and Menida scotti have obligate diapause, which conditions univoltinism in these pentatomids. In M. scotti, only females have obligate adult diapause, whereas males remain physiologically active through the whole winter, this pattern being unusual for Heteroptera. The univoltine seasonal cycle of this species with summer diapause (aestivation) and apparent migrations is similar to that of shield bugs (Scutelleridae). According to the analysis of seasonal development, the evolution of seasonal adaptations in Pentatomidae does not directly reflect their phylogeny. However, individual genera, small tribes or even subfamilies have similar complexes of seasonal adaptations. At the same time, Pentatominae is a large and apparently collected taxon, but most of species in this subfamily have the same facultative adult diapause.

Long life cycles covering more than one year are known for all orders of insects. There are different mechanisms of prolongation of the life cycle: (1) slow larval development; (2) prolongation of the adult stage with several reproduction periods; (3) prolongation of diapause; (4) combination of these mechanisms in one life cycle. Lasting suboptimal conditions (such as low temperature, low quality of food or instability of food resources, natural enemies, etc.) tend to prolong life cycles of all individuals in a population. In this case, the larvae feed and develop for longer than a year, and the active periods are interrupted by dormancy periods. The nature of this dormancy is unknown: in some cases it appears to be simple quiescence, in others it has been experimentally shown to be a true diapause. Induction and termination of these repeated dormancy states are controlled by different environmental cues, the day-length being the principal one as in the case of the annual diapause. The long life cycles resulting from prolonged adult lifespan were experimentally studied mainly in beetles and true bugs. The possibility of repeated diapause and several periods of reproductive activity is related to the fact that the adults remain sensitive to day length, which is the main environmental cue controlling their alternative physiological states (reproduction vs. diapause). Habitats with unpredictable environmental changes stimulate some individuals in a population to extend their life cycles by prolonged diapause. The properties of this diapause are poorly understood, but results of studies of a few species suggest that this physiological state differs from the true annual diapause in deeper suppression of metabolism. Induction and intensity of prolonged diapause in some species appear to be genetically controlled, so that the duration of prolonged diapause varies among individuals in a group, even that of sibles reared under identical conditions. Thus, long life cycles are realized due to the ability of insects to interrupt activity repeatedly and enter dormancy. This provides high resistance to various environmental factors. Regardless of the nature of this dormancy (quiescence, annual or prolonged diapause, or other forms) and the life cycle duration, the adults always appear synchronously after dormancy in the nature. The only feasible explanation of this is the presence of a special synchronizing mechanism, most likely both exo- and endogenous, since the adults appear not only synchronously but also in the period best suited for reproduction. As a whole, the long life cycles resulting from various structural modifications of the annual life cycle, are typical of the species living under stable suboptimal conditions when the pressure of individual environmental factors is close to the tolerance limits of the species, even though it represents its norm of existence. Such life cycles are also typical of the insects living in unstable environments with unpredictable variability of conditions, those developing in cones and galls, feeding on flowers, seeds, or fruits with limited periods of availability, those associated with the plant species with irregular patterns of blossoming and fruiting, and those consuming low-quality food or depending on unpredictable food sources (e.g., predators or parasites). Long cycles are more common in: (1) insect species at high latitudes and mountain landscapes where the vegetation season is short and unstable; (2) species living in deserts or arid areas where precipitation is unstable and often insufficient for survival of food plants; (3) inhabitants of cold and temporary water bodies that are not filled with water every year. At the same time, long life cycles sometimes occur in insects from other climatic zones as well. It is also important to note that while there is a large body of literature dealing with the long life cycles in insects, it mostly focuses on external aspects of the phenomenon. Experimental studies are needed to understand this phenomenon, first of all the nature of dormancy and mechanisms of synchronization of adult emergence.

Seasonal development and ecology of Anthocoridae are reviewed. Most of 500–600 species in the family are predacious or zoo-phytophagous, and a few other species are exclusively phytophagous or myrmecophilous. Some anthocorids are (and many others can potentially be) used as biological control agents in the Integrated Pest Management (IPM). Overwintering at the adult stage is typical of anthocorid bugs from the temperate zone (especially for the subfamily Anthocorinae). The known exceptions are the embryonic diapause in Tetraphleps abdulghanii, Temnostethus pusillus, and T. gracilis (Anthocorinae) and continuous development through all seasons (a homodynamic seasonal cycle) in Lyctocoris campestris and some species of Xylocoris (Lyctocorinae). In a number of species, especially in the genera Anthocoris and Orius, copulation occurs before overwintering and only females survive winter, a feature very unusual for Heteroptera and insects in general. Many anthocorid species are multivoltine in the temperate zone, producing several (up to 8 in some cases) generations per year. The number of generations typically decreases to 1 per year towards the north. Seasonal development of multivoltine species is chiefly controlled by daylength and temperature. All multivoltine anthocorids of the temperate zone studied to date have photoperiodic response of a long-day type: the females reproduce under the long-day conditions, but enter diapause under the short-day conditions. Towards the south, the photoperiodic response gradually becomes weaker: some populations do not enter diapause even under the short-day conditions, especially at higher temperatures. Termination of diapause is poorly understood in anthocorids, but a number of species require low-temperature treatment for a few weeks prior to the start of oviposition. Alary and color polymorphism are rare in the family, and they have never been shown to be seasonal or environmentally controlled. Pronounced seasonal migrations and aggregation behavior also have never been reported in Anthocoridae. Summer diapause appears to be very unusual for the family, having been reported only in Tetraphleps abdulghanii. The seasonal change of host plants, known in some populations of Anthocoris nemorum and A. nemoralis, is also a seasonal adaptation unusual for Heteroptera. Seasonality of tropical and subtropical species is poorly studied, but anthocorids developing without winter diapause are considered promising agents for the biological control of arthropod pests. Further studies of ecophysiology of Anthocoridae will optimize application and mass rearing of these predators in IPM programs.