568 Invasive Stink Bugs and Related Species (Pentatomoidea)
12.2.1 The Endogenously Controlled Univoltine Seasonal Cycle
This seasonal cycle is characterized by obligate diapause starting invariably in each generation of the
species or population, regardless of the external conditions. In the temperate latitudes, the formation of
winter diapause occurs well before the drop of temperature in autumn. If a species has obligate diapause,
only one generation can develop in all its populations across the entire distribution range. This is the
distinctive feature of this type of seasonal cycle.
However, heterogeneity of voltinism pattern has been recorded within some species. In such cases, a
population consists of two fractions, one of which has obligate diapause and produces only one genera-
tion per year under any conditions, whereas the second fraction of the same population has facultative
diapause, induction of which is controlled by external conditions (Hodek 1977, Zaslavski 1988; Chapter
11 ). As a result, the first fraction of the population produces only one generation per year, whereas the
second fraction might also produce a second generation if the conditions of a particular year permit this
to occur.
Diapause can occur at any ontogenetic stage, but that stage is strictly species-specific (Chapter 11). In
particular, among the various pentatomoids that have been studied, obligate embryonic diapause has
been found in Picromerus bidens (L.) and Apoecilus cynicus (Say) (subfamily Asopinae); obligate
nymphal diapause in Pentatoma rufipes (L.) (Pentatominae); and obligate adult diapause in Menida
disjecta (Uhler) (= Menida scotti Puton), Palomena angulosa (Motschulsky), Palomena prasina ( L .)
(Pentatominae) and many species from Acanthosomatidae, Scutelleridae, and Cydnidae (see Chapter 11).
The apparent simplicity of the univoltine seasonal cycle often is combined with various adaptations,
which not only help to maintain such a cycle but also ensure the proper timing of individual developmen-
tal stages with certain periods of the year that are most favorable for active development or dormancy.
Such adaptations can be revealed only by special experiments. In the following sections, we review the
most studied examples of the different causes and mechanisms of the univoltine cycle in pentatomoids as
well as the role of additional seasonal adaptations in maintaining this cycle.
12.2.1.1 The Univoltine Seasonal Cycle Based on Obligate Embryonic Diapause
Picromerus bidens. Most authors consider the seasonal cycle of this predatory pentatomid as univoltine
with obligate diapause at the embryonic stage (Leston 1955, Southwood and Leston 1959, Putshkov 1961,
Javahery 1986, Larivière and Larochelle 1989). However, there are a few reports in the literature of living
adult bugs being found in early spring (Schumacher 1910–1911, Butler 1923), which would be impossible
if all the adults died soon after mating and oviposition in late summer or early autumn. To explain the
findings of these adults in spring, a hypothesis has been proposed that assumes simultaneous realization
of two patterns of seasonal development: a primary one, with overwintering in the embryonic stage; and
a rarer secondary one, with overwintering in the adult stage (Larivière and Larochelle 1989).
Our analysis of the collections in the Zoological Institute (the Russian Academy of Sciences,
Saint Petersburg) confirmed the early season findings of adult Picromerus bidens in various regions of
Russia in April–May (Figure 12.1).
Phenological records demonstrate that in the temperate belt of Russia and in Ukraine, the great
majority of Picromerus bidens pass through the final molt in July (Putshkov 1961); in Great Britain, the
final molt occurs mostly in August–September (Southwood and Leston 1959, Hawkins 2003; Figure
12.1). Because the findings of adults in spring (Figure 12.1) do not fit into the phenological pattern
with overwintering in the embryonic stage, Leston (1955) assumed that the overwintering adults were
those infested in the late summer with tachinid flies of the subfamily Phasiinae (Diptera: Tachinidae).
The possibility of overwintering in an unusual stage later was confirmed for other species of insects
(Viktorov 1976, Tauber et al. 1986, Danks 1987). The presence of endoparasitoids greatly affects the
seasonal development of their hosts by modifying their physiological state. Phasiinine flies infest adult
bugs that appear in the late summer or autumn. Their larvae suppress development of the host’s repro-
ductive system. The infested bugs do not participate in reproduction but live longer and overwinter;
thus, the parasitic tachinid larvae can overwinter inside the hosts and complete their development in the
spring of the subsequent year.