Halyomorpha halys (Stål) 257
reduce the time a female is available to mate prior to oviposition. By comparison, Halyomorpha halys
exhibits short copulation periods, averaging 10 minutes in the laboratory. However, females are polyan-
drous, mating with at least five males per day (Kawada and Kitamura 1983b). Field observations of mat-
ing pairs are common, but the pairs easily disengage if disturbed. Multiple matings in H. halys increase
female fitness, and there is an increase in the hatch rate and duration of oviposition with increased mat-
ings (Kawada and Kitamura 1983b). In the absence of mate guarding, it is hypothesized that males are
assured paternity through sperm mixing and/or the high rate of available females (Sillen-Tullberg 1981,
Roderick et al. 2003).
4.4.4 Overwintering Behavior/Diapause
Halyomorpha halys is well-known for causing nuisance problems, as large numbers of adults often
invade human-made structures to overwinter inside protected environments (Inkley 2012). A detailed
reporting in one house counted >26,000 individuals in a single year. H. halys will overwinter in
almost any structure, between cardboard boxes, vehicles, underneath tarps, wood piles, etc., but are
frequently found in attics and crawlspaces in aggregations (Inkley 2012). Survivorship is improved
within aggregations when antennal contact is made, although the physiological reasoning is unknown
(Toyama et al. 2006).
Anecdotal evidence that Halyomorpha halys will disperse from neighboring woodlots into agricul-
tural crops, such as peach, led to an investigation of natural overwintering habitats. Lee et al. (2014b)
found that adults of H. halys will, in fact, overwinter in the natural landscape. Overwintering adults were
recovered from dry crevices in dead, standing trees with thick bark, particularly oak (Quercus spp.) and
locust (Robinia spp.) that were >19.0 centimeters (cm) diameter at breast height. Of randomly sampled
trees, 5.6% had overwintering H. halys adults. However, when the characteristics of the overwintering
habitat mentioned above were applied, ≈32% of trees surveyed harbored H. halys, albeit at low numbers
with ≈six adults/tree observed (Lee et al. 2014a). Large populations also have been observed in rock
outcroppings in both Maryland and Pennsylvania (T.C. Leskey and Galen P. Dively, personal communi-
cation; see Acknowledgments).
Little is known about the effects on Halyomorpha halys of exposure to low winter temperatures typi-
cally found in North America. Cira et al. (2016) examined the impacts of low and freezing temperatures
on mortality of this bug. They reported that H. halys is chill intolerant and dies before freezing and that
cold tolerance varies by season, sex, and acclimation location. Acclimation site also affected the bugs
supercooling point (i.e., -17.06°C ± 0.13 in Minnesota, -13.90°C ± 0.09 in Virginia).
Adult Halyomorpha halys overwintering in temperate regions are believed to be in facultative repro-
ductive diapause (see Chapter 11). Continual observations of adults in California throughout mild win-
ters (Charles Pickett, personal communication; see Acknowledgments) suggest that it is not. Diapause
initiation and termination cues of most insect species are influenced by the interaction of intrinsic factors
such as genetics as well as extrinsic factors such as temperature and photoperiod (Tauber et al. 1986). For
those species that overwinter as adults, photoperiod is frequently the primarily critical cue (Tauber et al.
1986). Based on the available literature, we cautiously assume that the cues for diapause termination and
induction in H. halys are symmetrical and determined primarily by photoperiod – thus are considered
independent of temperature. Watanabe (1979) reported a 13.5–14h critical photoperiod (daylength) to
terminate diapause for overwintering adults, whereas Yanagi and Hagihara (1980) suggested a longer
14.75h critical photoperiod. However, termination of diapause as indicated by the initiation of repro-
duction does not occur immediately upon leaving overwintering sites as females require an additional
developmental period related to heat accumulation. Although emergence from overwintering sites is
gradual, a peak in activity occurs in West Virginia and Virginia in April around 13.5h daylength (T.C.
Leskey and J. Christopher Bergh, unpublished data; see Acknowledgements). A larger peak in adult
activity (measured by leaving overwintering shelters) occurs in early-mid May, which suggests at that
time emergence is the interaction of increasing daylength and temperature (Wiman et al. 2014). To fur-
ther examine spring emergence, Bergh et al. (2017) placed marked adults in overwintering cages encir-
cled by pheromone-baited and unbaited pyramid traps and followed their emergence from the cages in
2013 and 2014. The observed a small peak in activity in mid-April followed by a larger, more prolonged