Pentatomoids as Vectors of Plant Pathogens 623
fruit abortion. Feeding through the shell later in the season produces discolored, spongy, sunken regions
in the nutmeat, known as kernel necrosis (Rice et al. 1985). In addition to this direct feeding damage,
coreids and pentatomids have been implicated in the transmission of two fungal diseases, pistachio stig-
matomycosis and panicle and shoot blight (Mitchell 2004).
Stigmatomycosis is an older term for fungal infections caused by Eremothecium coryli and other
yeasts associated with hemipteran feeding damage (Ashby and Nowell 1926). The term still is used
commonly in pistachio for infections by E. coryli and Aureobasidium pullulans (de Bary) G. Arnaud,
although similar fungal infections in other crops have different names (e.g., yeast spot, fruit rot, dry
rot). The disease is found throughout the pistachio-growing areas of California and in Iran, Russia,
and Greece (Michailides and Morgan 1990, 1991, and references therein). In pistachio, the disease may
appear as underdeveloped kernels; wet, rancid, distorted, but full-sized kernels; or white, jelly-like ker-
nels (Michailides 2014). Incidence of this disease in orchards ranges from 0.7 to 29.1%, depending on
mode of irrigation (Michailides and Morgan 1990), and peaks in August and September, which coincides
with a period of kernel feeding by large hemipterans (Michailides and Morgan 1991).
The pentatomid species associated with transmission of these fungal infections in California are
Thyanta pallidovirens (Stål), Chlorochroa uhleri (Stål), and C. ligata (Say); a coreid, Leptoglossus
clypealis (Heidemann), also is a known vector (Michailides and Morgan 1990). Infection was signifi-
cantly enhanced when fruit clusters sprayed with a suspension of A. pullulans were caged in the field
with T. pallidovirens; incidence of stigmatomycosis in this treatment reached 28.6%. When T. palli-
dovirens were allowed to feed on cultures of this yeast and then exposed in field cages to sterilized
fruit clusters, significant transmission levels were also documented (Michailides and Morgan 1991). The
involvement of A. pullulans in stigmatomycosis is unusual; the common causative agents in most crops
are Eremothecium coryli and related yeasts. Experiments with the two Chlorochroa species, L. clypea-
lis, and T. pallidovirens feeding on E. coryli produced similar results, with infection rates ranging from
17.7 to 29.6% for the pentatomids, compared with 43.6% for the coreid (Michailides and Morgan 1990).
These bugs can, therefore, acquire fungal propagules from the plant surface or from infected pistachio
fruits or other crops and transmit directly into the kernel. Sprayed fungicides have no effect on the inci-
dence of stigmatomycosis in pistachio, suggesting that the yeasts may be carried internally (Michailides
and Morgan 1990) as shown for pyrrhocorids (Frazer 1944) and other pentatomids (see Section 13.5.4,
L eg u mes).
Panicle and shoot blight, first noted in California orchards in 1984, is a devastating disease considered
to be a serious threat to California pistachios (Holtz 2002, Michailides and Morgan 2004). Symptoms
begin as necrotic spots on shoots, rachises, and leaves (and later on fruits) that coalesce as the season
progresses. Spots on petioles lead to leaf abscission and defoliation, whereas blight on fruiting structures
causes the rachis to collapse, ultimately destroying whole fruit clusters. Losses may reach 100% (Rice et
al. 1985, Holtz 2002). The causative agent is an ascomycete fungus, Botryosphaeria dothidea (Mougeot)
Cesati and De Notaris, which is ubiquitous in woodlands on trees and shrubs as well as on other culti-
vated tree fruits (Michailides et al. 1998). Conidia are spread by rain, birds, and sprinkler irrigation as
well as insects (Holtz 2002); the latter may transfer the fungus within orchards, between orchards, or
perhaps even from surrounding vegetation to pistachio orchards. The large propagules (pycnidiospores
measure 15–29 × 5–8 μm) are thought to be carried externally on hemipteran mouthparts and legs. Bug
feeding and wounding in general facilitate entry into the rachis or fruits, although infection can occur
via stomata or lenticels (Michailides and Morgan 2004, Daane et al. 2005).
Thyanta pallidovirens, Chlorochroa uhleri and an unidentified Chinavia sp. (as Acrosternum) have
been studied to determine their role in transmission of panicle and shoot blight, along with several core-
oid and mirid species. Feeding punctures correlate significantly with the incidence of infected pistachios.
In a series of field experiments, a significant increase in infection rates occurred when T. pallidovirens,
the unidentified Chinavia sp., or the coreoids were caged on fruit sprayed with Botryosphaeria dothi-
dea; results for C. uhleri showed a similar trend (Michailides et al. 1998). However, subsequent trials
(Daane et al. 2005) showed that mechanical wounding with a pin increased infection rates significantly
more than did stink bug feeding. In addition, these bugs are poor vectors; of a large sample of hemip-
terans collected in infected orchards, <0.2% carried inoculum. Furthermore, spores remained attached
to stink bugs for only 3 days, compared with 10 days for a leaffooted bug. The most important role of