The Invasive Caucasian Populations of the Brown Marmorated Stink Bug Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae) Rapidly Adapt Their Ecophysiological Traits to the Local Environmental Conditions.

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.

Extremely rapid maternal photoperiodic response in Trichogramma telengai: A fine-scale study.

Timing of maternal photoperiodic response of Trichogramma telengai to a single long night was studied in laboratory experiments. Adult females reared under diapause-averting short night conditions (L:D = 18:6) experienced one diapause-inducing prolonged night (12 h) and then were allowed to lay eggs (to parasitize the host, Sitotroga cerealella, eggs) during 3 days. The progeny was incubated under moderately diapause-inducing conditions (14 °C in the dark). The maternal photoperiodic response was extremely rapid: a slight but statistically significant increase in the incidence of diapause was already observed in the progeny hatched from the eggs laid 8 h after the beginning of the 'additional' part of night. Such a quick photoperiodic response, as far as we know, has not been reported for any insect. Then the proportion of diapausing progeny gradually increased over 30-50 h reaching 85-95%. Control females developed and were kept as adults under short night (L:D = 18:6) conditions; diapause was induced in <10% of their progeny. Analysis of individual variations showed that the proportion of diapausing progeny of experimental females increased with time gradually (not abruptly). These data enriches our knowledge of insect photoperiodic response and can be used for the planning of further (in particular, molecular) studies.

To Every Thing There Is a Season: Phenology and Photoperiodic Control of Seasonal Development in the Invasive Caucasian Population of the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae).

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.

Storage Potential of the Predatory Ladybird Cheilomenes propinqua in Relation to Temperature, Humidity, and Factitious Food.

The ability of the females of the predatory ladybird Cheilomenes propinqua to survive and to retain reproductive potential in the absence of natural food (aphids) was estimated under various hydrothermal (temperatures of 7, 12, 17, 22, and 27 °C; air humidities of 50% and 80-90%) and trophic (starved vs. fed on the frozen eggs of the grain moth Sitotroga cerealella) conditions. The post-storage reproductive potential was estimated using the mean number of eggs laid over 20 days. The experiments showed that fed females can be stored at temperatures of 15-17 °C for 20 days with a rather low (about 20%) and for up to 80 days with an acceptable (not more than 50%) loss of the reproductive potential. The successful short-term (up to 3 days) storage or transportation of fed and starved females can occur at temperatures from 12 to 27 °C. However, storage for more than 10 days at temperatures of 7 °C and lower results in the 100% mortality of both the starved and fed beetles. These data suggest that (1) in greenhouses, C. propinqua can be used for the biological control of aphids by preventing colonization, although this would require the regular supplementation of factitious food, and (2) escaped individuals would not survive the winter even in the south of the temperate zone.

Flying over Eurasia: Geographic Variation of Photoperiodic Control of Nymphal Development and Adult Diapause Induction in Native and Invasive Populations of the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae).

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.

Influence of temperature on the restoration of the ability of Trichogramma principium to undergo diapause.

It is known that the progeny of post-diapause females of some insects are insensitive to diapause-inducing stimuli. In aphids the duration of the 'interval timer' (the restoration of the ability to diapause) decreases with temperature. However, the parameters of this temperature dependence are unknown. We investigated the restoration of the ability to undergo diapause in 9-16 sequential post-diapause generations of the egg parasitoid Trichogramma principium Sug. et Sor. (Hymenoptera: Trichogrammatidae) over a period of 120-150 days at different constant and variable temperatures. This revealed a strong linear correlation between mean temperature and the rate of the restoration of the ability to diapause. The lower temperature threshold of this dependence was not significantly different from that of the thermal dependence of the rate of preimaginal development. The restoration rate depended on the mean temperature for the whole period of development rather than on the temperature conditions during the development of the thermosensitive stages determining the incidence of diapause in the progeny. The results of this study indicate that the duration of the interval timer is determined by the rate of development (or, more generally, by the rate of metabolism) rather than by the mechanisms controlling the photothermal regulation of diapause.

Grandmaternal temperature effect on diapause induction in Trichogramma telengai (Hymenoptera: Trichogrammatidae).

Adaptive grandmaternal thermal effect, wherein the grandmaternal thermal environment affects the induction of progeny diapause two generations later, has not been studied in any insect system. We have studied this effect in the parthenogenetic egg parasitoid Trichogramma telengai Sor. (Hymenoptera: Trichogrammatidae) under laboratory conditions. The grandmaternal generation developed at temperatures from 18 to 30 °C combined with short (L:D = 12:12) or long (L:D = 18:6) photoperiod. The maternal generation developed at the same two photoperiods combined with low (20 °C) or high (30 °C) temperature. The progeny generation developed at 14 °C and L:D = 12:12. The grandmaternal temperature response was consistent with an adaptive response (low temperature induces facultative prepupal winter diapause two generations later) and rather strong (ranged up to 20-25%). The experiments suggested that both grandmaternal and maternal thermal effects are based on the influence of temperature on photoperiodic induction of diapause. However, experiments also revealed substantial differences between the grandmaternal and maternal thermal responses. In particular, the grandmaternal thermal response was observed only at short-day grandmaternal photoperiod, whereas the maternal thermal response was independent both of maternal and grandmaternal photoperiods. Although under natural conditions the adaptive value of the grandmaternal thermal response in T. telengai is most probably low, this effect should be considered in physiological models of diapause induction and can be important for mass rearing of Trichogramma species.

Multigenerational maternal inhibition of prepupal diapause in two Trichogramma species (Hymenoptera: Trichogrammatidae).

It is known that in some insect species the incidence of diapause among the progeny of females that had undergone diapause is relatively low or zero even under strong diapause-inducing conditions. Moreover, the maternal inhibition, preventing the induction of a maladaptive diapause in spring, can persist over several generations. This multigenerational effect based on hypothetical 'interval timer' was thoroughly studied in Aphididae. We first described a similar phenomenon in Hymenoptera: laboratory experiments demonstrated that the proportion of diapausing progeny of Trichogramma females that had undergone diapause was practically zero independently of photoperiodic and temperature conditions used (day lengths of 12 and 18h and temperatures of 12-15°C). Then the ability to enter diapause recovered gradually and returned to the normal level over two (in Trichogramma telengai) or even five (in Trichogramma principium) generations. We conclude that the observed effect may be based on an interval timer similar to that in aphids.