Diapause in Pentatomoidea 521
As shown above, insects differ in their strategies to cope with cold, but most species, including all
heteropterans studied thus far, follow the strategy of freeze intolerance. Even under harsh winter condi-
tions (e.g., in Alaska), the freeze intolerant parent bug Elasmostethus interstinctus survives winter by
supercooling (i.e., the physical phenomenon by which water and aqueous solutions remain unfrozen
below their melting point if ice nucleating agents are absent; Barnes et al. 1996, Duman et al. 2004).
The relation between winter diapause and cold hardiness has been considered in numerous special
publications (e.g., Denlinger 1991, Leather et al. 1993, Danks 2000, Bale 2002, Denlinger and Lee
2010). In general, winter diapause is thought to be necessary for increasing cold hardiness and suc-
cessful overwintering of insects living in the Temperate Zone. However, there are several exceptions to
this rule, where insects can survive winter without deep diapause, apparently using other specific eco-
physiological strategies (Denlinger 1991, Šlachta et al. 2002).
The cold hardiness of insects under experimental conditions usually is estimated by the supercool-
ing point (SCP) (i.e., the temperature at which spontaneous freezing occurs in a supercooled liquid,
also referred to as the crystallization temperature). In several species, the SCP value is not constant
throughout the year. For example, the SCP value of the Italian striped bug, Graphosoma lineatum,
during 2000–2001 in the Czech Republic was about –7°C in May–June, decreased to –14 to –12°C in
August–October, dropped to –18°C in December–January, and then increased again by spring (Šlachta
et al. 2002). A similar pattern of SCP dynamics was observed in the stink bugs Scotinophara lurida in
Korea (Cho et al. 2007) and Halyomorpha halys in the United States (Cira et al. 2016).
Seasonal trends are not always so distinct, however. For example, in a laboratory culture of the preda-
ceous stink bug Podisus maculiventris originating from the United States of America (38°N), the SCP
values of nondiapausing eggs and first instars were –34.1 ± 0.28°C and –29.0 ± 0.40°C, respectively,
despite the fact that this species overwinters as adults. At the same time, the SCP values of diapausing
and nondiapausing females were similar: –17.8 ± 0.46°C and – 15.0 ± 0.60°C, respectively (Borisenko
1987). The diapausing (–11.7 ± 0.7°C) and nondiapausing (–10.4 ± 0.8°C) adults of Nezara viridula from
South Carolina (USA) also showed almost no difference in this parameter (Elsey 1993). These data
testify to a weak relation or no relation at all between cold hardiness and diapause in the above species.
11.5 Diapause Development and Termination of Winter Diapause
The gradual changes that occur during the central diapause phase and finally result in its ending (i.e.,
termination) are usually referred to as diapause development. The term reflects the fact that diapause is
not only a specific physiological state but also a dynamic process whose ending is followed by resump-
tion of active development and often morphogenesis. Termination of diapause is achieved by resumption
of activity of neurosecretory centers as a result of spontaneous or induced processes.
The specific features of the state of winter diapause and the processes taking place during diapause
are still insufficiently studied. Based on the research of the gradual changes that occur during winter
diapause development, Hodek (1983) distinguished two processes: horotelic (slow and spontaneous) and
tachytelic (fast and induced; evolving at a rate faster than in the case of horotelic process).
Horotelic processes represent slow and internally regulated diapause development under more or less
stable conditions (i.e., those under which diapause was induced). In this case, spontaneous diapause
termination is free of external influence and does not require any stimuli. In contrast, the tachytelic pro-
cesses take place when diapause development is influenced and accelerated by environmental conditions
and diapause is externally and prematurely terminated by action of, for example, low temperatures (cold
termination of diapause) or changes in the day length (photoperiodic termination of diapause). In
other words, slow horotelic processes result in spontaneous diapause termination, whereas fast tachytelic
processes accelerate diapause development and finally end up with externally induced diapause termina-
tion (Hodek 1983, 1996, 2002; Zaslavski 1988). These two processes are explained here separately and
can be studied separately in the laboratory, but, in nature, stable conditions almost never exist and, thus,
the tachytelic process (caused by, for example, cold in winter) is likely to override the slow horotelic
process.