360 Invasive Stink Bugs and Related Species (Pentatomoidea)
An analysis of historical climatic data (Tougou et al. 2009) suggests that the shift in distribution of
Nezara viridula in Japan most likely has been promoted by the milder overwintering conditions in the
region during the last few decades. The mean temperatures in the region from January to February were
1.03–1.91°C higher during 1998–2007 than during 1960–1969. The number of cold days in January and
February (with mean daily temperatures below 5°C) also has decreased significantly, whereas the annual
lowest temperature has risen significantly from 1960–1969 to 1998–2007 (Tougou et al. 2009). In central
Japan, N. viridula is found predominantly near locations where the mean January temperature exceeds
5°C, the mean cumulative number of cold days (with daily mean below 5°C) does not exceed 26 dur-
ing January and February, and the mean annual lowest temperature does not drop below –3.0°C. This
analysis also shows that the mean January temperature and the number of cold days are the most criti-
cal factors that determine the northern distribution limit of N. viridula. All of the climatic data suggest
that over the last 45 years, environmental conditions have become more favorable for overwintering of
N. viridula at many locations in central Japan. This likely has promoted the northward spread of the spe-
cies and represents a direct response of this species to climate warming (Tougou et al. 2009). Subsequent
field collections in colder and more elevated locations documented a more rapid range shift towards the
north (about 5 km per year; Figure 7.3C,E), thus suggesting that not only temperature but also other
abiotic and, perhaps, biotic and anthropogenic factors are involved (Geshi and Fujisaki 2013).
Adults of Nezara viridula are strong fliers and able to disperse over long distances in the wild, presum-
ably before and after diapause (Gu and Walter 1989). Adults of the species also are known to be carried
over long distances by hurricanes (up to 750 km; Aldrich 1990) and probably also by typhoons. It is
highly probable that every year, the population range limits in the northern temperate zone move further
north and reproduction occurs in new areas in summer. The trend of winter warming, with both natural
and anthropogenic components (e.g., in a form of the “heat islands”; see Tougou et al. 2009), improves
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Mean January temperature, °CWinter mortality, %FIGURE 7.4 The effect of mean January temperature on winter mortality of Nezara viridula adults in central Japan.
Field experiments in Asso in 1961–1967 (open circles): mean (and range of) mortality (in different types of hibernacula) in
adults of both sexes (n = 284–1197 per winter) (Data from K. Kiritani, N. Hokyo, and K. Kimura, Annales de la Société
Entomologique de France, Nouvelle Série 2: 199–207, 1966, and K. Kiritani, Proceedings of the Symposium on Rice
Insects, Tropical Agricultural Research Center, Tokyo, Japan, pp. 235–248, 1971); a linear regression trend line refers to the
mean mortality (F1, 5 = 6.81, P = 0.06). Additional outdoor experiments in Osaka in 1999–2000 and in Kyoto in 2006–2007
and 2007–2008 (all other symbols): mean mortality in adults of both sexes and range (mortality in two sexes); n = 23–138
per cohort (Data from D. L. Musolin and H. Numata, Ecological Entomology 28: 694–703, 2003b; D. L. Musolin and
H. Numata, Entomologia Experimentalis et Applicata 11: 1–6, 2004; D. L. Musolin, D. Tougou, and K. Fujisaki, Global
Change Biology 16: 73–87, 2010; and K. Takeda, D. L. Musolin, and K. Fujisaki, Physiological Entomology 35: 343–353,
2010). Note that Kiritani et al. (1966) and Kiritani (1971) measured mortality during the hibernation only and did so in
the wild, whereas in all other experiments we also included prewinter mortality and reared the insects in containers, thus
providing protection from predators and parasites. (From D. L. Musolin, Physiological Entomology 37: 309–322, 2012,
with permission.)