Diapause in Pentatomoidea 531
Polyphenism covers cases when environmental conditions determine which phenotype will be
realized. Phenotypic plasticity can result from variation in developmental, physiological, biochemi-
cal, and behavioral processes that are sensitive to environmental variables (Nijhout and Davidowitz
2009, Simpson et al. 2011). If changes in frequencies of phenotypes are regular (annual) and con-
trolled by environmental conditions, then such cases of polymorphism can be called seasonal
polyphenism.
In Heteroptera, cases of seasonal changes of wing size and degree of development of wing muscles
or other organs are good examples of seasonal polyphenism. They allow many true bug species to sur-
vive unfavorable seasons, migrate or disperse, and effectively use available resources. However, whereas
wing size/wing muscle seasonal polyphenism is widely represented in some ecological and taxonomic
groups of Heteroptera (e.g., aquatic and semi-aquatic bugs [Gerromorpha and Nepomorpha]; Saulich and
Musolin 2007a), it remains basically unknown in Pentatomoidea. The only known exception is possibly
a burrower bug, Scaptocoris carvalhoi Becker, distributed in Brazil (Nardi et al. 2008) and represented
by two distinct wing forms. Long-winged (i.e., macropterous) individuals demonstrate a greater loco-
motion capacity than short-winged (i.e., brachypterous) individuals, and only long-winged adults can
fly. The exact mechanism of control of this wing polyphenism is not known, but a significant increase in
the frequency of long-winged adults has been noticed during the swarming season suggesting that the
wing polyphenism is seasonal and highly functional. Furthermore, this seasonality may be related to
the scarceness of rain during the developmental period of the nymphs. In this case, the lack of rain can
result in a decrease in the moisture content of the soil and act as an inducing factor for wing development
mechanisms (Nardi et al. 2008).
Another category of seasonal polyphenism is seasonal body color polyphenism or seasonal body
color change, widely represented in the Pentatomoidea. There are numerous examples of this phenom-
enon where seasonal body color polyphenism often is linked to changes in the physiological state of
individuals, namely formation of winter diapause, and often is under photoperiodic control (Musolin and
Saulich 1996b, 1999; Saulich and Musolin 2007b).
There are two forms of adults of the dusky stink bug, Euschistus tristigmus tristigmus, which differ in
morphology and body color. For many years, the two forms were considered different species or subspe-
cies, but it was discovered they were seasonal forms of the same species (McPherson 1975a). The two
forms could be produced under experimental conditions by manipulation of the rearing photoperiods
(long-day versus short-day; McPherson 1974, 1975a,b, 1979). Subsequently, similar patterns of photo-
periodic control of adult body coloration were reported in a few other pentatomids: Thyanta calceata
(McPherson 1977, 1978), Plautia stali (Kotaki and Yagi 1987), Oebalus ypsilongriseus (Vecchio et al.
1994, Panizzi 2015), Euschistus servus (Borges et al. 2001), Euschistus conspersus (Cullen and Zalom
2006), Nezara viridula (Musolin and Numata 2003a, Musolin 2012), Piezodorus guildinii (Zerbino et al.
2014, 2015), and others. In even more pentatomoids, seasonal body color polyphenism has been reported,
but its control mechanism remains unknown (e.g., Halys fabricii [as Halys dentatus] and Erthesina fullo;
Dhiman et al. 2004).
In Halyomorpha halys, seasonal polyphenism of body color and other morphological characters mani-
fests itself in both nymphal and adult stages (Niva and Takeda 2002). For example, the red color on the
sternum of adults is more common in nondiapausing adults and may be related to reproductive matu-
rity. The pronotum of fifth instars reared from hatching under short-day conditions (L:D 11:13) shows
a darker, brown-marbled color pattern with less creamy-yellowish speckles, than that of the nymphs
reared under long-day conditions (L:D 16:8). Temperature also influences body coloration of nymphs,
and higher temperature enhances the long-day effect. The fifth instars reared under short-day conditions,
which are destined to diapause when they become adults, have shorter white stripes on the pronotum,
smaller body size, less frequent feeding, and more lipid accumulation than the long-day reared nymphs.
In another experiment, cohorts of nymphs were transferred from long-day and high temperature condi-
tions (L:D 16:8 at 25°C) to short-day and low temperature conditions (L:D 11:13 at 20°C) for the dura-
tions of the second–fifth and fourth–fifth stadia and for the fifth stadium. It was found that the longer the
exposure to short-day and low temperature conditions during the nymphal stage, the greater the expres-
sion of short-day-associated characteristics observed in the fifth instars and adults (Niva and Takeda
2002, 2003).