Diapause in Pentatomoidea 529
In most species, aggregations are formed by adults, but cases are known where nymphs aggregate (e.g.,
overwintering aggregations of plataspid Coptosoma scutellatum; Davidová-Vilimová and Štys 1982) or
both adults and nymphs do so (Caternaultiella rugosa Schouteden; Gibernau and Dejean 2001).
In large aggregations, individuals of different categories (hibernating, estivating, or nondiapausing)
can have advantages over nonaggregated individuals including enhanced mating opportunities (Hibino
1985); shelter from adverse environmental conditions (Kiritani 2006) or parasitoids (Caternaultiella
rugosa Schouteden; Gibernau and Dejean 2001); reduced desiccation (Lockwood and Storey 1986,
Vulinec 1990); and combined chemical defense against predators (Cocroft 2001). However, there are
possible negative effects too, because large aggregations are likely to attract predators and parasitoids
or stimulate development of pathogens. This has been shown in the case of Nezara viridula and its para-
sitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in Hawaii (Nishida 1966, Jones and
Westcot 2002).
Ecological importance of seasonal aggregations during diapause has been studied in the subsocial
shield bug Parastrachia japonensis in East Asia. This subsocial species is monophagous and feeds only
on seeds of Schoepfia jasminodora Siebold et Zuccarini (Olacaceae). The fruits and seeds of the shrub
are available only for a couple of weeks per year and to synchronize its seasonal cycle with that of the
shrub, P. japonensis spends about 10 months annually in adult diapause and forms large aggregations
(Tachikawa and Schaefer 1985; Tsukamoto and Tojo 1992; Nomakuchi et al. 1998; Filippi et al. 2000b;
Tojo et al. 2005a,b). Formation of these aggregations decreases the metabolic rate in diapausing bugs
which, in turn, increases their survival rate during long dormancy over hot summer or cold winter peri-
ods when food is not available. Elegant laboratory experiments demonstrated that oxygen consumption
was twice as low in bugs in aggregations compared to isolated individuals. Interestingly, group size was
not important if compared to the physical contacts with other individuals of the same species. It was
suggested that such contacts stimulate excretion of a chemical compound functioning as an aggregation
pheromone and promoting formation of aggregations (Tojo et al. 2005b). A few other eco-physiological
adaptations allow the species to survive for an extended period when food resources are unreliable (Tojo
et al. 2005a,b).
Pentatomoids also produce aggregation pheromones for either food or mate location or to identify
overwintering habitats. Thus, males of the stink bug Halyomorpha halys produce a recently identified
two-component aggregation pheromone (Khrimian 2005; Khrimian et al. 2008, 2014). The species also
responds to a kairomone, which is an aggregation pheromone of a sympatric Asian pentatomid Plautia
stali, although this stimulus is only attractive beginning in early August (Aldrich et al. 2009, Nielsen et
al. 2011, Weber et al. 2014).
In autumn, during a period of preparation for winter diapause, many pentatomoids (e.g.,
Halyomorpha halys, Menida disjecta, Urochela quadrinotata) search for hibernation quarters and,
in so doing, can enter houses and other buildings in large numbers, often becoming a serious nui-
sance (Kobayashi and Kimura 1969, Inaoka et al. 1993, Watanabe et al. 1995, Hoebeke and Carter
2003, Inkley 2012, Lee et al. 2014).
11.7.3 Photoperiodic Control of Nymphal Growth Rate
The growth rate of nymphs and, correspondingly, the duration of the nymphal stadia in Pentatomoidea
are affected largely by ambient temperatures; an increase in temperature within the temperature opti-
mum range hastens development, and a decrease hinders it. However, the developmental rate depends
on other factors and cues as well. In particular, one of the important seasonal adaptations in insects is
photoperiodic control (i.e., regulation) of the nymphal growth rate; nymphs may develop faster under
certain photoperiodic conditions and slower under others. Such adaptation is a quantitative PhPR (see
Section 11.3.1.1). In several species, under low to moderate temperatures, development is accelerated
by short-day conditions. As day length decreases in autumn, the nymphal growth rate increases so as to
reach the overwintering stage before environmental conditions get worse. Such an adaptation first was
described in fire bug, Pyrrhocoris apterus (Pyrrhocoridae; Saunders 1983, Numata et al. 1993, Saulich
et al. 1993), and later found in the predatory stink bug Arma custos (Volkovich and Saulich 1995),
green shield bug, Palomena prasina (Saulich and Musolin 1996, Musolin and Saulich 1999), and many