588 Invasive Stink Bugs and Related Species (Pentatomoidea)
of Japan, from whence it spread to the north and reached the environs of Osaka (34.7°N) by the end of
the 20th century. At the beginning of the 21st century, it advanced still further northward (Tomokuni et
al. 1993; Musolin 2007, 2012; Yukawa et al. 2007, 2009; Musolin and Saulich 2011; Geshi and Fujisaki
2013; see Chapter 7 for details).
In the warm temperate climate of central Japan, Nezara viridula usually has three annual generations
(Figure 12.15), although part of its population seems to be able to produce an incomplete fourth genera-
tion (Kiritani and Hokyo 1962).
In February, the overwintered adults start changing color from brown/russet to intermediate and by
March–April, most of them acquire green (or yellow) coloration typical of the reproductive state. Mating
starts in April, and oviposition starts in April–May (Kiritani et al. 1963, Musolin et al. 2010, Takeda et
al. 2010, Musolin 2012). Adults of the first generation appear in July and soon give rise to the second
generation, which reaches the adult stage in the second half of August. Adults of the third generation
appear at the end of September. Most of them enter winter diapause and only a minor fraction of adults
reproduces in autumn (Figure 12.18; Kiritani et al. 1963, Musolin 2012).
Induction of the facultative winter adult diapause in Nezara viridula is controlled by a long-day PhPR
with a critical photoperiod of about 12 hours 30 minutes at temperatures of 20°C and 25°C (Musolin and
Numata 2003a). Considering the fact that this species has reached the environs of Osaka only recently,
Musolin and Numata (2003b) carried out a field experiment to determine how well its population has
adapted to the local climatic conditions. Attention was focused on the dates of emergence of adults and
formation of facultative winter adult diapause because these phases of the seasonal cycle often determine
the possibility of naturalization of invasive insects in temperate regions.
The natural day length in Osaka (without the civil twilights) is 12 hours 53 minutes on September 1,
12 hours 27 minutes on September 15, and 11 hours 48 minutes on October 1. All females of Nezara
viridula that emerged before September 1 were reproductively active and laid eggs. Among females
that emerged in the second half of September, approximately 60% entered facultative winter diapause
(Figure 12.18; series 2 and 3). The remaining approximately 40% of females were reproductive but up
to 60% of their progeny were destined to die during winter because of low temperature (Musolin and
Numata 2003b). In females that emerged in the first half of October (Figure 12.18, series 4), incidence
of diapause reached 100%. Thus, in the outdoor experiment, diapause was induced very late in the
season, but it was in a good agreement with the critical photoperiod (12 hours 30 minutes) estimated in
the laboratory. If compared to several native true bug species studied earlier (Figure 12.19), N. viridula
had a somewhat lower critical photoperiod and, correspondingly, the majority of females of this species
formed diapause somewhat later in the season (e.g., only ≈75% at the beginning of October).
According to experimental data (Musolin and Numata 2003b), the fate of the nymphs of Nezara virid-
ula hatching from the eggs laid in autumn varied. Only the nymphs that hatched before mid-September
could successfully complete preadult development, whereas those that hatched after that time died dur-
ing winter; the later they hatched, the earlier the stage at which they encountered the lethal low winter
temperatures. From the eggs laid in mid-September, adults emerged only in November. Because they
developed under late-autumn short-day conditions, these adults did not reproduce. Although these adults
had some chance of surviving until spring, they could not get properly prepared for overwintering: they
did not have enough time to change their body color and to accumulate sufficient energy resources
(Musolin and Numata 2004). The formation of a complete diapause state in true bugs usually takes
considerable time. For example, according to our observations, preparation for diapause in another pen-
tatomid Podisus maculiventris requires at least 17–19 days at a moderate temperature of about 20°C
(Saulich and Musolin 2011, 2012).
Adults of Nezara viridula entering diapause are known to turn brown or russet soon after the final
molt (Figure 12.18; Musolin and Numata 2003a, Musolin 2012; see Chapters 7 and 11) and to remain
brown/russet until the complete termination of winter diapause in the spring. The change of body color-
ation is controlled by day length and correlated with the physiological state of the individual (Harris et al.
1984, Musolin and Numata 2003a, Musolin 2012; see Chapters 7 and 11). However, the change of body
color in the adults that emerged in another field experiment in November proceeded slowly during winter
and ended as late as the end of March (Musolin and Numata 2003b; see Chapter 11). Moreover, 20%
of individuals still remained green even at that time. The temperature during the period of emergence