Margarita Yu. Dolgovskaya

Long-term storage is an important component of insect mass-rearing systems, prolonging the shelf life of biocontrol agents during a low-demand period or a temporary lack of suitable food. Macrolophus pygmaeus is a predatory heteropteran, mass-reared and widely used for the biological control of arthropod pests in greenhouses. With the aim to determine the optimal conditions and acceptable duration of cold storage, we evaluated the impact of different periods of storage of fed and starved third instar nymphs of M. pygmaeus at different temperatures on nymphal survival, adult emergence, and female fecundity. Four storage temperatures (3, 6, 9, and 12 °C) were tested. The longevity of starved nymphs decreased with an increase in the storage temperature, with a maximum of about 40 days at 3 °C, whereas the longest lifetime of nymphs fed on eggs of the grain moth Sitotroga cerealella (about 150 days) was observed at 9 °C. Further experiments demonstrated that the third instar nymphs of M. pygmaeus fed with eggs of the grain moth can be stored at 9 °C for 30 days, with a moderate (10–20%) decrease in survival and fecundity, whereas the survival of starved nymphs decreased by half after 10 days of storage at 3 °C.

The ability to rapidly adapt to new environmental conditions is a crucial prerequisite for the wide-scale invasion of pests or intentional introduction of beneficial insects. A photoperiodically induced facultative winter diapause is an important adaptation ensuring synchronization of insect development and reproduction with the local seasonal dynamics of environmental factors. We conducted a laboratory study aimed to compare photoperiodic responses of two invasive Caucasian populations of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), which recently invaded neighboring regions with subtropical (Sukhum, Abkhazia) and temperate (Abinsk, Russia) climates. Under the temperature of 25 °C and the near-critical photoperiods of L:D = 15:9 h and 15.5:8.5 h, the population from Abinsk showed a slower pre-adult development and a stronger tendency to enter winter adult (reproductive) diapause compared to the population from Sukhum. This finding agreed with the difference between the local dynamics of the autumnal temperature decrease. Similar adaptive interpopulation differences in the patterns of diapause-inducing responses are known in other insect species but our finding is distinguished by a very short adaptation time: H. halys was first recorded in Sukhum in 2015 and in Abinsk in 2018. Thus, the differences between the compared populations might have evolved over a relatively short span of several years.

Biological invasions often result from multiple invasion events. In the case of several subsequent invasive episodes, ‘newcomers’ are usually poorly adapted to local environmental conditions in contrast to the representatives of the already-established invasive population of the same species. Therefore, the mode of inheritance of life-history features determining the survival and performance of interpopulation hybrids is an important component of invasiveness. We investigated the mode of inheritance of the photoperiodic response in the brown marmorated stink bug, Halyomorpha halys, by crossing between the native population of South Korea and the invasive population of the Black Sea coast of Russia. The aim of this study was to predict the overwintering potential of the progeny from possible crosses between representatives of the native and invasive populations. The pre-adult development time and the incidence of winter adult diapause in the progeny of the interpopulation crosses were close to the average of the values recorded in ‘pure’ (unmixed) crosses. Female and male genotypes were equally important in the determination of these characters. Such a mode of inheritance is most likely determined by a polygenic control and would only partially promote subsequent invasion events from the native South Asian range of H. halys into Europe.

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, Halyomorpha halys, in the Sochi region (Krasnodar Territory, Russia) from 2018 to 2021 by regular field sampling and dissecting. The results of the sampling suggest that H. halys is at least partially bivoltine in the studied region: the main period of mass oviposition (by the overwintered females) occurs from June to July; the second, much shorter period of egg-laying (by females of the new, i.e., the first generation) occurs in August. Reproductively active individuals (i.e., females with developed ovaries and filled spermatheca and males with filled ectodermal sac) were recorded from the end of May to the beginning of September. Such a seasonal pattern correlated with day length: when the natural photoperiod decreased below the experimentally determined critical day length (15.0–15.5 h), the proportions of females with fully developed ovaries sharply dropped to zero. Both the rate of H. halys pre-adult development and the timing of the induction of winter adult diapause observed under natural conditions fully agreed with the earlier predictions that had been based on the results of laboratory experiments.

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.

Ovipositing females from invasive (Krasnodar Territory of Russia) and native (Far East of Russia) populations of Harmonia axyridis were fed one of a set of diets ranging from 50 Myzus persicae aphids every day to 1 aphid every 10 days and all were also provided with a 10% sugar solution. The experiment was conducted at 20?C under short (12 h) and long (18 h) day conditions. Most of the females from the native population that consumed 50 or 10 aphids per day continued to oviposit under both long and short day conditions. Females that consumed 1 aphid per day or every 2 days practically stopped laying eggs but under long day conditions their ovaries were still active, whereas under short day conditions ca 50% of them were reproductively inactive (only germaria present) and had a well-developed fat body. Further reduction in diet resulted in an increase in the proportion of reproductively inactive females. However, about half of the females that terminated oogenesis under long day conditions had poorly developed fat bodies, which indicates that diapause was not induced. For the females from the invasive population, both photoperiodic and trophic effects were weak: under short day conditions, some females entered diapause when prey was abundant, whereas about 50% (independent of photoperiod) did not enter diapause when starved. This risk-spreading strategy, possibly, facilitates the adaptation of this invasive ladybird to unpredictable environmental conditions.

Short photoperiods often accelerate preimaginal development in insects that overwinter as adults and thus ensure the timely development of the diapausing stage. However, fast development usually results in small adults with few reserves whereas successful overwintering is dependent on sufficient reserves of nutrients. Thus, an insect faces two opposite challenges: increase adult weight or speed up pre-adult development. One solution to this "time-size trade-off" is fast development resulting in relatively light-weight but not too small adults, which are able to survive if there is an early onset to winter and have the possibility of further increasing their weight if conditions in autumn remain favourable for longer than usual. To test this hypothesis, we determined the effect of different photoperiods (day lengths of 12 and 18 h at 20?C) on the duration of preimaginal development, size of emerging adults and dynamics of adult weight in Harmonia axyridis. The larvae reared under short-day conditions tended to develop faster and invest resources in structural growth rather than in increasing weight: the daily rate of increase in size under a 12 h long photoperiod was greater than that under a 18 h long photoperiod, whereas the rate of gain in weight showed the opposite tendency. This resulted in a significant decrease in the weight/size ratio of emerging adults. However, their low initial nutritional status was partly compensated for by adult feeding: the relative gain in adult weight of "short-day individuals" was greater than that of the beetles that developed under long day conditions.