574 Invasive Stink Bugs and Related Species (Pentatomoidea)
long-day conditions. At higher temperatures, acceleration of development was less pronounced and
often disappeared completely. This fact can probably be explained by the existence of a certain tempera-
ture optimum and limits of this PhPR, which is typical of any biological process (see Chapter 11). It is
at moderate autumn temperatures that short-day acceleration of nymphal development becomes adaptive
because it increases the probability that late-hatching nymphs will reach the diapausing stage (adult) and
prepare for overwintering before the onset of unfavorable cold weather in autumn. The nymphs hatch-
ing in the middle of summer do not face this problem because they have enough time to reach the adult
stage. Besides acceleration of development at the end of the vegetative season, photoperiodic control of
the nymphal growth rate synchronizes the adult molt, shifting the appearance of the overwintering stage
to the period most favorable for diapause formation (Musolin and Saulich 1997). It was fortunate that
photoperiodic control of the nymphal development rate was discovered in a species in which onset of
winter adult diapause was not affected by the day length.
A similar quantitative photoperiodic control of the nymphal growth rate was described in a closely
related congeneric species, Palomena angulosa, in Japan (Hori 1986). The nymphs of this species,
which hatch earlier in the season, have slower growth rates than those hatching later, the difference
reaching 50–60%. On the one hand, such an adaptive strategy is determined by the time of fruiting of
the food plants. Although the species is polyphagous and can feed not only on different species but also
on different parts of plants, its nymphs cannot successfully reach the adult stage without feeding on
fruits (Hori et al. 1985). On the other hand, acceleration of nymphal growth in autumn reflects the need
to complete preadult development before the onset of autumn cold, since P. angulosa, like P. prasina,
can overwinter only in the adult stage.
12.2.2 The Exogenously Controlled Univoltine Seasonal Cycle
Similar to multivoltinism, exogenously controlled univoltinism is a common type of seasonal develop-
ment. Nearly all species having a potentially multivoltine seasonal cycle can (or actually do) switch to
univoltine development in some parts of their ranges, for a variety of reasons.
This type of seasonal cycle is found in the predatory pentatomid Arma custos ( F.), which was studied
in the forest-steppe zone (Belgorod Province, Russia, 50°N) where it always has only one annual genera-
tion (Saulich and Volkovich 1996). According to published data, a single generation per vegetative season
was recorded not only in the northern and central regions of Europe (Chelnokova 1980) and in the forest-
steppe zone of Siberia (Petrova 1975) but also in southern Ukraine (Putshkov 1961), Bulgaria (Iosifov
1981), and Kirghizia (Putshkov 1965). However, this species may have two generations in Abkhazia
because its second instars were found there at the end of July (T.A. Volkovich, personal communication).
In addition, a nondiapausing culture was obtained from the Krasnodar population (45°N) of A. custos by
rearing the nymphs and adults under long-day conditions of L:D 18:6 at 28°C (Ismailov and Oleshchenko
1977). These data indicate that the onset of winter diapause in A. custos is externally controlled.
Indeed, experimental studies of Arma custos showed that induction of winter adult diapause in this spe-
cies was controlled by the PhPR of the long-day type (Volkovich and Saulich 1995): diapause was formed
under the short-day conditions (photophase 14 hours or shorter) at temperature of 29–30°C (Figure
12.6, line 1), whereas female maturation, mating, and oviposition took place under long-day conditions.
However, when temperature was a few degrees lower (24–25°C), which is still relatively high for the origin
of this population, incidence of diapause dramatically increased (Figure 12.6, line 2). In another experi-
ment with the same species, it was shown that the range of temperatures permitting full manifestation of
the PhPR of diapause induction was somewhat expanded in the case of thermorhythm (27°C during the
photophase and 13.5°C during the scotophase). However, at the mean temperature of 20°C, about 60% of
the females still entered diapause under long-day conditions (Volkovich and Saulich 1995).
Thus, Arma custos can realize the multivoltine seasonal cycle only in those regions where the tem-
perature is high enough to prevent formation of winter adult diapause. However, in the greatest part of its
range, temperature of the warmest month (July) does not reach the level at which development without
diapause would be possible.
Shift to univoltinism in Arma custos is supported by one more specific trait that is rare among insects,
namely, sensitivity to day length exclusively (or mostly) at the adult stage (Saulich and Volkovich 1996;