Diapause in the seasonal cycle of stink bugs (Heteroptera, Pentatomidae) from the Temperate Zone

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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.