Seasonal Cycles of Pentatomoidea 585
Hokkaido (Tomokuni et al. 2003; Rider 2006; Musolin 2007, 2012; Ferrari et al. 2010). Nezara viridula
has a much wider distribution, almost cosmopolitan, and is continuously expanding its range; in Japan,
it overlaps with the southern part of the range of N. antennata (Kiritani et al. 1963, Tougou et al. 2009,
Musolin 2012; see Chapter 7).
Both species, but especially Nezara viridula, are broad polyphages, feeding on more than 197 spe-
cies from more than 43 families of plants (Todd 1989, Panizzi et al. 2000; see Tables 7.4 and 7.5).
They occupy similar ecological niches and occur sympatrically; in some cases, N. viridula has replaced
Nezara antennata almost completely in a mere several years (Kiritani et al. 1963; Kiritani 1971; Kon et
al. 1994; Musolin 2007, 2012; Yukawa et al. 2007, 2009; Tougou et al. 2009).
Nezara antennata, in central Japan, has only two generations per year and does not form a third
generation (even in exceptionally warm years) unlike N. viridula, which can produce three generations
per year (Figure 12.15). Laboratory experiments (Noda 1984) have shown that adults of N. antennata
maintained at a long or increasing day length did not quickly start oviposition but formed summer dia-
pause: the preoviposition period under such conditions was more than 40 days at 25°C, as compared with
about 20 days in the adults transferred from long-day to short-day conditions. Field experiments also
have demonstrated that induction of estivation in the middle of summer resulted in a delay of oviposition.
The estivating adults did not change their color from green to brown whereas during winter diapause,
the color of adults did change, both in this species and in N. viridula (D. L. Musolin, unpublished data).
After the end of estivation, the adults started to reproduce and gave rise to the second generation, which
formed facultative winter adult diapause under the short-day conditions (Numata and Nakamura 2002).
Thus, N. antennata has one generation in spring and one in autumn; the summer adult diapause allows
the species to avoid exposure to excessive heat. Such pattern might be adaptive as it has been shown that
the species is not heat-tolerant and that up to 68% of the nymphs died even at 30°C (Kariya 1961).
12.3.3 The Partially Bivoltine Seasonal Cycle
A seasonal function of summer diapause is quite different in the clown stink bug, Poecilocoris lewisi
(Distant), another pentatomoid species well studied in Japan (Tanaka et al. 2002). Nymphs of P. lewisi
feed on seeds of the dogwood Cornus controversa Hemsley (Cornaceae), which gain their full weight
and ripen only at the beginning of July.
This shieldbacked bug is partially bivoltine and has two facultative diapauses: winter nymphal dia-
pause and summer adult diapause. Both of them are under photoperiodic control and both have critical
photoperiods of diapause induction close to 14 hours 30 minutes (Figure 12.16). Short day induces
winter diapause in the fifth instar and long day induces fairly short adult summer diapause manifested
Apr. MayJune July Aug. Sep. Oct. Nov.Apr. MayJune July Aug. Sep. Oct. Nov.N. viridulaNymphs
Eggs1st generation2nd generation1st generation 2nd generation3rd generation
Overwintered adultsN. antennataNymphs
EggsOverwintered adultsFIGURE 12.15 Seasonal development of Nezara viridula and N. antennata, in central Japan (Data from K. Kiritani,
N. Hokyo and J. Yukawa, Researches on Population Ecology 5: 11–22, 1963.)