Pentatomoids as Vectors of Plant Pathogens 613
the attachment to the head, the innervation of the stylets and labium, the movement of the stylets in
relation to one another, the composition of the saliva, and the manner in which these structures are used
to obtain food vary among the three suborders (i.e., Heteroptera, Auchenorrhyncha, Sternorrhyncha)
(Backus 1988), affecting their behaviors and, consequently, their role as vectors.
In Heteroptera, the rostrum connects flexibly near the front of the head and the maxillary and man-
dibular stylets move together when inserted in food or prey, with the apices of mandibular stylets slightly
ahead. One or both sets of stylets may be barbed or serrated (Cobben 1978). Watery saliva is produced
by all true bugs, but only the phytophagous Pentatomomorpha are capable of producing the gelling
saliva, which also is found in Auchenorrhyncha and Sternorrhyncha (Miles 1968, Cobben 1978, Backus
1988). Chemosensilla are found on the antennae and labium and within the precibarium, allowing both
contact chemoreception and tasting of sampled fluid drawn up the stylets (Backus 1988). Labial dabbing
(tapping the plant surface [with or without exuding watery saliva onto the plant] to sample the surface
chemicals) has been reported for both Cimicomorpha and Pentatomomorpha (Cook and Neal 1999, Cline
and Backus 2002). The path of stylet insertion is intracellular, in vivid contrast to the delicate meander-
ing of some aphid stylets between the palisade cells (Pollard 1973). In addition to damage along the
entry path, damage to the target tissue also may be extensive. This may occur simply because the stylet
bundle is large, or ingestion may be preceded by mechanical laceration and/or enzymatic activity from
watery saliva. If pathogens must be delivered to uninjured, functional plant host cells (e.g., phloem
sieve tube cells [Pollard 1977]), it is difficult to understand how larger bugs can effectively inoculate
phloem-limited phytoplasmas or fastidious bacteria. The diameter of the stylets, and hence the food and
salivary canals, also affects the ability to acquire and inoculate infective particles. The maxillary stylet
canals of some pentatomids, for example, permit entry of the ascospores of Eremothecium (formerly
Nematospora) coryli (Peglion) Kurtzman (Ragsdale et al. 1979), likely facilitating the close association
between this fungus and the larger pentatomids and coreids.
Four modes of feeding, or feeding strategies, were described for Hemiptera by Miles and Taylor
(1994): stylet sheath, lacerate and flush, macerate and flush, and osmotic pump. Stylet sheath (or sali-
vary sheath) feeding involves a complete sheath of gelling saliva extending from the plant surface to
the target vascular tissue and sealing the stylets into the cell of choice (sieve tube or xylem vessel).
Lacerate and flush feeders use the stylets to physically rip open plant cells. Watery saliva then flushes
out the cell contents and the mix is ingested. A partial salivary sheath may be produced within plant
tissue, or a deposit (flange) of gelling saliva may be secreted on the plant surface without any internal
deposition. Macerate and flush, associated with plant bugs (Miridae), employs enzymes in watery
saliva to chemically macerate the cells rather than through physical laceration. Enzymatic activity
also characterizes osmotic-pump feeding in which salivary sucrase alters the osmotic balance in the
intercellular spaces, inducing parenchyma cells to leak their contents and phloem sieve tube cells to
unload. This feeding method is associated with several tribes of Coreidae. The salivary enzymes of
hemipteroids recently have been reviewed by Sharma et al. (2013), with a discussion of their role in
pathogen transmission.
Miles and Taylor’s (1994) organizational scheme was simplified by Backus et al. (2005) who identi-
fied just two basic strategies, sheath feeding and cell-rupture feeding, with other behaviors (lacerate and
flush, macerate and flush, lacerate and sip, lance and ingest) relegated to the status of “tactics” within
cell-rupture feeding. Sharma et al. (2013) presented a similar arrangement, but with osmotic-pump feed-
ing included as a strategy. However, it is essential to realize that despite the confusing nomenclature,
the various strategies are not mutually exclusive. That is, sheath-producing Heteroptera often employ
other strategies and in some species, a salivary sheath may accompany the stylets for some distance as
they approach the target tissue to be ruptured. Obviously, the cimicomorphs (unable to produce gelling
saliva) must by definition be cell-rupture feeders, but Pentatomomorpha are exceptionally plastic in their
feeding behaviors. Some species alter their strategy as development proceeds (e.g., Eurydema rugosa
Motschulsky [Hori 1968]) or may switch from cell-rupture feeding to sheath feeding as the target tissue
changes. Oncopeltus fasciatus (Dallas) uses the salivary-sheath strategy on phloem but employs lacer-
ate and flush tactics (i.e., cell-rupture feeding) on seeds (Miles 1959). Similarly, Nezara viridula ( L .)
produces a complete salivary sheath when hydrating from xylem but feeds via cell rupture on developing
seeds of soybean (Cooke 2014). Pentatomid species vary in their preferences for plant structures as well;