578 Invasive Stink Bugs and Related Species (Pentatomoidea)
Thus, the main factor limiting the number of generations is the absence of suitable food for the southern
population in the later part of the season and the insufficient heat for the northern ones, but the signal
function of day length is preserved in both cases (Nakamura and Numata 1999).
A somewhat more complex case of the univoltine seasonal cycle was described in the North American
stink bug Chinavia hilaris (Say) [as Acrosternum hilare (Say)] in Canada (Javahery 1990). The win-
ter adult diapause of this species is controlled by the long-day PhPR as in many other pentatomoids.
Laboratory experiments showed that bugs actively reproduce at long-day conditions L:D 16:8 and form
diapause at short-day conditions L:D 8:16 (Wilde 1969). Two generations of the species were observed
in the southern part of its distribution in Arkansas (Miner 1966) and in southern Illinois (McPherson
and Tecic 1997). In Canada, overwintered adults emerge when the temperature rises above 20°C in
spring. In late May and early June, the bugs actively feed on leaves and young shoots of buckthorn,
Rhamnus cathartica L.; white basswood, Tilia heteropholia L.; and clammy locust, Robinia viscosa
Vent. (Javahery 1990). The females lay eggs from the third week of June to the beginning of August. The
nymphs molt into adults from the end of August to the third week of October. Thus, in southern Canada,
the species has one generation per vegetative season, and its development is shifted onto the second half
of summer. The young adults feed on buckthorn fruits for 1–3 weeks and then migrate onto the leaves of
deciduous trees in the forests nearby and stay there without feeding from the end of September to the end
of October or beginning of November, flying over short distances in warm sunny days. The physiological
nature of this late-autumn resting period was not studied experimentally, but Javahery (1990) regarded it
as a summer diapause. With the onset of frost at the end of October, the bugs migrate into the litter and
overwinter there until April. The shift of emergence of the new generation towards the second half of
summer is probably related to the need of additional feeding of the adults on buckthorn fruits that ripen
in September.
Comparatively late active seasonal development also was observed in the European representative
congeneric pentatomid Acrosternum heegeri Fieber (Putshkov 1961).
Thus, in the above examples, the main factor determining the number of generations in a given popu-
lation is the availability of food (i.e., a vital factor), whereas temperature and day length act together as
signal factors. This results in a sophisticated mechanism controlling the seasonal development of each
population and ensures tuned adaptation to seasonality of the local environmental conditions.
Transition from multivoltinism to univoltinism based on the presence of two facultative diapauses
(summer and winter) is a rare phenomenon in the stink bug family. This seasonal pattern was discovered
in Carbula humerigera (Uhler) (Kiritani 1985a,b). Adult diapause in this species is formed under the
influence of increasing day length in late spring and early summer. Oviposition is delayed by photope-
riodic conditions and it begins only after the summer solstice, when day length starts to decrease. The
summer delay of oviposition (i.e., summer adult diapause) should be regarded as an adaptive mechanism
that phenologically shifts the nymphal development towards a later part of the season, when the day-
length conditions would stimulate the formation of a facultative winter nymphal diapause. Thus, two
facultative diapauses – the winter nymphal one and the summer adult one – participate in the formation
of the univoltine seasonal cycle in C. humerigera.
12.3 The Multivoltine Seasonal Cycle
As mentioned above, the main distinctive feature of the multivoltine seasonal cycle is that the over-
wintered generation gives rise to consecutive summer generations that are concluded with formation of
diapause and overwintering. Depending on the external conditions (first of all, temperature and the avail-
ability of food), there may be two, three, or more such summer generations. Development of two genera-
tions per season is often designated in the literature as bivoltinism, and development of three generations
as trivoltinism. In addition, there is a fairly common pattern in which at the end of the season, some
part of the population gives rise to the subsequent generation whereas the other part of the population
(usually the one that completes development somewhat later) enters diapause. This case is referred to as
development of a partial generation. It should be noted that all the above examples given earlier in this
paragraph are specific cases of the multivoltine seasonal cycle.