570 Invasive Stink Bugs and Related Species (Pentatomoidea)
regimes of 12 and 14 hours of light per day at a temperature of 24.5°C, all the females started ovipositing
synchronously about day 15, on average, following the final molt, whereas under the long-day labora-
tory conditions and under the outdoor conditions in July (when natural day is still long), the bugs did
not reproduce but entered estivation (Figure 12.3A), which was manifested as a significantly prolonged
preoviposition period (Figure 12.3B; Musolin and Saulich 2000).
The adaptive significance of these long-day-stimulated delays in the nymphal growth and adults’
gonad development of Picromerus bidens were understood only after the properties of the obligate win-
ter embryonic diapause were studied. This diapause was not deep; at 25°C, nymphs started to hatch from
the diapausing eggs 2–3 weeks after oviposition (Musolin and Saulich 2000). This means that in the
field, eggs laid in the middle of summer would develop into nymphs in the summer of the same year;
however, such nymphs would inevitably perish in winter because they cannot enter winter diapause and
survive the cold season. Because of a 1.5–2.0-month long adult estivation period induced by the long
day preceding reproduction, oviposition is shifted to the end of summer or beginning of autumn. At this
time, the late-season drop of temperature suppresses embryogenesis, thus preventing the nymphs from
hatching in autumn, which would be fatal for them (Figure 12.2).
Based on these results, we hypothesized that the weakness of the obligate winter embryonic diapause
in Picromerus bidens (which starts irrespective of the external conditions) required the formation of an
eco-physiological mechanism that would ensure a delay in oviposition until the autumn drop of tempera-
ture that, in turn, would arrest embryonic development and prevent the nymphs from hatching in autumn.
This mechanism would be established in the form of facultative summer adult diapause induced by the
long day. In the field, females of P. bidens terminate estivation and start reproducing after only 2 months
of dormancy and under the conditions of naturally decreasing day length (see Figure 12.2; Musolin and
Saulich 2000).
The univoltine seasonal cycle with winter embryonic diapause also has been described in North
American species of the genus Apoecilus (formerly Apateticus) (also of the same pentatomid subfam-
ily Asopinae): A. cynicus and A. bracteatus (Fitch) (as A. crocatus Uhler) (Whitmarsh 1916, Downes
1920, Jones and Coppel 1963, Evans and Root 1980, Javahery 1994). The winter embryonic diapause
occurs in these species at the stage of the developed blastoderm and is terminated only by the action
100 20 days40 days60 days806040200
12 14 16 18
Photoperiod, hIncidence of summer diapause,%Preoviposition period, daysPhotoperiod, h20 Field1 21416182 0Field70A B6050403020100FIGURE 12.3 Photoperiodic induction of facultative summer adult diapause in females of the predatory pentatomid
Picromerus bidens. A, Photoperiodic response of summer diapause induction under laboratory (24.5°C) and field condi-
tions in Belgorod Province, Russia (50°N; the preoviposition period was between July 6 and August 23; the photoperiodic
response was determined on days 20, 40, and 60 after the final molt); B, Duration of the preoviposition period under
the same conditions (mean ± SE; min–max). (From D. L. Musolin and A. Kh. Saulich, Entomologia Experimentalis et
Applicata 95: 259–267, 2000, with permission.)