520 Invasive Stink Bugs and Related Species (Pentatomoidea)
diapause. This has been demonstrated in the pentatomids Aelia fieberi (Nakamura and Numata 1997b),
Dybowskyia reticulata (Nakamura and Numata 1998), Nezara viridula (Figure 11.12; Musolin and
Numata 2003a, Takeda et al. 2010), and many other species. In many species, the gonads of both sexes
remain inactive until the end of the diapause or even postdiapause quiescence (Takeda et al. 2010).
At the same time, there are species with pronounced difference in physiological state of females and
males during winter diapause. Thus, the well studied sunn pest, Eurygaster integriceps, has a deep obli-
gate winter adult diapause. In diapausing females of this species, all morphogenetic processes stop (or
become deeply suppressed) whereas in diapausing males, spermatogenesis continues and by the end of
diapause males have mature sperm (Shinyaeva 1980).
Some other species copulate in autumn and females store sperm until the next spring. In such case,
males sometimes even do not survive until spring. This strategy is known in various heteropteran families
such as Nabidae (Kott et al. 2000), Anthocoridae (Kobayashi and Osakabe 2009, Saulich and Musolin
2009), and Pyrrhocoridae (Socha 2010). Among the Pentatomoidea, this strategy has been recorded in
Menida disjecta (= M. scotti). The winter adult diapause is obligate in this species, but the males already
have mature sperm in autumn. In the process of mating, which may occur even during winter, the males
supply the females with nutrients and, thus, likely increase the females’ chances of successfully overwin-
tering (Koshiyama et al. 1993, 1994).
Males of the white-spotted stink bug, Eysarcoris ventralis, also have mature testes in autumn, winter,
and spring and are ready to copulate after transfer to high temperature in the laboratory, whereas long-
day conditions are required for the start of ovarian development in females (Noda and Ishii 1981).
In the plataspid Megacopta cribraria, approximately 15% of overwintered females store live sperm
from autumn until as late as mid-March. This trait not only allows them to oviposit without additional cop-
ulation in the spring but also likely increases the invasive potential of this species while it colonizes new
areas because even one fertilized female can establish a new population of the pest (Golec and Hu 2015).
11.4.2 Cold Hardiness
Cold hardiness is an important issue in insect ecology and usually understood as the ability of an organ-
ism to survive at low temperatures (Leather et al. 1993). Diapause provides general nonspecific tolerance
of insects to various adverse environmental conditions, including cold. The survival of insects at low
temperatures recently has attracted considerable attention (e.g., Lee and Denlinger 1991; Bale 1993,
1996; Leather et al. 1993; Hodková and Hodek 2004; Danks 2005; Denlinger and Lee 2010), but the data
for Heteroptera still are scarce.
In general, responses of insects to cold are complex and, as a rule, differ between diapausing and
nondiapausing individuals, at different periods of the year, in different ontogenetic stages, and between
populations. Nevertheless, based on their response to temperatures below the melting point of their body
fluids, it has been suggested that insects can use three different strategies to cope with low temperatures:
(1) freeze intolerance (also called freeze avoidance, freeze susceptibility, or chill intolerance),
(2) freeze tolerance (also called freezing tolerance), and
(3) cryoprotective dehydration.
The freeze intolerant species cannot survive the formation of ice within their bodies and, thus, have
evolved a set of biochemical, physiological, behavioral, and ecological measures/adaptations to prevent
ice formation. In contrast, freeze tolerant insects can withstand ice formation, usually only in the extra-
cellular fluids, and have a set of characteristics that enables them to survive such ice formation. Adoption
of the strategy of cryoprotective dehydration allows the third group of insects to survive subzero tem-
peratures by losing water to the surrounding environment, so resulting in an increase of the concentra-
tion of their body fluids and, thus, a decline in their melting point (to equilibration with the ambient
temperature). As a result, they cannot freeze (Zachariassen 1985, Bale 2002, Sinclair et al. 2003, Chown
and Nicolson 2004, Berman et al. 2013, Storey and Storey 2015).