Miles 1972 Saliva of Hemiptera

The Saliva of Hemiptera
PETER W . MILES
School of Natural Sciences. University of Zambia
I. Introduction . . . . . . . . . . . . . . . . . . 183
I1. Methods of Investigation . . . . . . . . . . . . . . 185
111. Modes of Feeding . . . . . . . . . . . . . . . . 191
IV . Stylet-Sheath Feeding . . . . . . . . . . . . . . . 194
A. Sampling the Surface . . . . . . . . . . . . . 194
B. Secretion of the Flange . . . . . . . . . . . . . 195
C. Formation of the Sheath . . . . . . . . . . . . 196
D. Discharge of Watery Saliva . . . . . . . . . . . . . 197
E. Ingestion . . . . . . . . . . . . . . . . . 200
F . Withdrawal of the Stylets . . . . . . . . . . . . 201
V . Lacerate-and-Flush Feeding . . . . . . . . . . . . . 202
VI . Feeding by Carnivores . . . . . . . . . . . . . . . 203
VII . Chemical Composition and Function of the Saliva . . . . . . 205
A. Sheath Material . . . . . . . . . . . . . . . 205
B. Watery Saliva . . . . . . . . . . . . . . . . 208
VIII . Phytopathogenicity . . . . . . . . . . . . . . . . 217
IX . Salivary Glands and Ducts . . . . . . . . . . . . . . 225
A . Aphidoidea . . . . . . . . . . . . . . . . 226
B . Jassomorpha . . . . . . . . . . . . . . . . 229
C. Fulguromorpha . . . . . . . . . . . . . . . 232
D. Other Auchenorrhyncha . . . . . . . . . . . . 233
E. Heteroptera . . . . . . . . . . . . . . . . 234
X. Origins of the Saliva . . . . . . . . . . . . . . . . 236
A. Functions of the Accessory Gland . . . . . . . . . 236
B . Functions of the Principal Gland . . . . . . . . . 237
C. Sources of Oxidases . . . . . . . . . . . . . . 238
D. Sources in the Homoptera . . . . . . . . . . . . 239
E . Salivary Carbohydrate and Lipid . . . . . . . . . . 240
XI . The Saliva as a Vehicle for Pathogens . . . . . . . . . . 241
XI1. Evolution of Salivary Function in the Hemiptera: a Summary . . 244
XI11. A Survey of Problems . . . . . . . . . . . . . . . 247
References . . . . . . . . . . . . . . . . . . . . . . 250
I . INTRODUCTION
Salivary function is especially interesting in Hemiptera because of
the effects the saliva has on the living and surviving organisms on
183
184 PETER W. MILES
which many of these insects feed. Some of the exclusively

phytophagous suborder Homoptera cause “phytotoxaemias”
including galls in their food plants; some Homoptera and a few
phytophagous Heteroptera transmit diseases to plants in their saliva
and some of the blood-sucking Heteroptera similarly transmit
diseases to their hosts. Even when Hemiptera transmit diseases
apparently by contamination of their mouthparts, they do not
function as mere “flying pins”; there is evidence that the saliva can
modify the effectiveness of transmission.
The saliva of Hemiptera is by no means a simple secretion: in
addition to the usual salivary functions of moistening food and
mixing it with hydrolytic enzymes before ingestion, the saliva of
phytophagous species plays an important physiochemical role during
the mechanical penetration of plant tissues by the piercing and
sucking mouthparts and, in accomplishing this task, the saliva may
vary in its chemical composition and physical consistency from one
moment to the next. Moreover, deposits of solidifying components
of the saliva of many species persist in the food plants, modifying the
long term effects of feeding by the insects. At the same time, other
salivary components dissolve solid materials during gustatory
exploration of substrates and it seems highly probable that the saliva
thus acts as a carrier of gustatory stimuli to sensilla remote from the
“functional mouth” at the tip of the stylet-like mouthparts. Finally,
there is evidence that the saliva may subserve an excretory function
in some species, varying in composition in relation to the
compositim of the haemolymph-indeed it would appear to provide
the only means of excretion in those few, highly specialized
Homoptera that lack an anus.
In relation to the complex composition and varied functions of
the saliva, the salivary glands of Hemiptera are themselves complex
and in the suborder Homoptera may present a seemingly bewildering
array of cell types that appear to secrete different products and to
undergo individual cycles of secretory activity. Identification of the
products of individual types of cells with externally recognizable
salivary functions is difficult in the Homoptera, in which the main
secretory parts of the salivary apparatus are without a distinct lumen;
but in the Heteroptera the salivary glands take the form of sac-like
lobes, and accumulations of the salivary secretions can be identified
and even collected from the salivary glands of the larger species.
The history of investigations of salivary functions in Hemiptera is
largely one of independent studies: on the one hand of economically
THE SALIVA O F HEMIPTERA 185
significant Homoptera, in which research on the saliva is beset with

problems connected with the small size of the insect; and on the
other of the larger Heteroptera which are easier to deal with but have
evoked less interest because of their lesser economic importance.
Only recently has a measure of similarity in salivary functions in the
two taxa been recognized and explored. It is the intention of this
article to bring together the various types of investigation on salivary
functions in the Homoptera and Heteroptera, and to suggest
profitable lines of future investigation based on analogous functions
in different taxonomic groups.
11. METHODS OF INVESTIGATION
The effects of the feeding of phytophagous Hemiptera were first

investigated by histological study of plants on which these insects
had fed. Histochemical analyses were made of the tissues surrounding
feeding punctures and physiological inferences drawn as long ago as
Busgen (1 89 1); although the usefulness of such interpretations was
limited by the uncertainty of whether observable effects were caused
by the insects directly or were due to reactions on the part of the
plant (Petri, 1909). A refinement in histological studies was the
examination of tissues on which the insects had fed for a known
length of time and in which the insects’ stylets remained in situ. This
was achieved by rapid killing of the insects with drops of very hot
wax (Smith, 1920), electric shocks or by snipping or shaving off the
stylet bundle while the insect was still feeding (Mittler, 1957).
Major advances in the determination of the nature of the salivary
secretions of Hemiptera and of their possible roles during feeding
became possible when it was found that the insects could be induced
to feed on transparent media such as agar gels or solutions enclosed
by membranes. McLean and Kinsey (1 967) brilliantly exploited the
ability of aphids to probe through parafilm by passing a small electric
current through the aphid and substrate and correlating changes in
the current with observable feeding activities involving salivation and
ingestion. By this means, McLean and Kinsey (1 968) were then able
to determine the sequence of salivation and ingestion in opaque,
natural substrates. Refinements and details of the method have been
published by McLean and Weigt (1 968): electrical contact is made
with the aphid by cementing a gold wire of 15.0 p thickness to the
dorsum with a quick drying silver conducting paint. An example of
the circuitry is outlined in Fig. 1. Patterns of change in the
..
Fig. 1. Block and schematic diagram of the various devices and components used in a system to record pea aphid salivation and
ingestion. (From McLean and We&, 1968.)
Rl-IOK; R2-150-500K; R3-99M; R4-47K; R5-16; R6-1M; R7-1M; R8-470K; R9-8; R10-1M; Rll-16; D1 to D4-1N1614;
M-high impedance A-C voltmeter; T-Triad F-16X filament transformer; S1A,B-DPDT toggle switch; S2A,B-DPDT toggle switch.
Fig. 2. Strip chart recordings showing sequences of feeding activity by the pea aphid. To be read from right to left:
base line at the bottom of chart Omv. S-salivation waveform associated with penetration of tissues by the stylets and the secretion
of a stylet sheath; X-waveform associated with penetration of phloem sieve tube; t-probably a period of brief ingestion between
unblocking of food canal by discharge of saliva; Y-waveform of unknown significance; I-prolonged ingestion. (From McLean and Kinsey,
1967.)
188 PETER W. MILES
conductance of the system can be recorded on a cathode ray

oscilloscope, through a loud-speaker or on a chart recorder or any
combination; although the chart recorder is probably the most useful
as a means of recording data permanently (Fig. 2).
A similar system has been used by Smith and Friend (1971) to
record the feeding of the blood-sucking bug Rhodnius prolixus.
These authors inserted a platinum electrode through the cuticle and
fixed it in place with beeswax and colophony (2: 1). The insects were
permitted to feed through a rubber membrane on artificial diets
containing 0.15 M NaCl with or without M ATP sodium salt.
Flows in the liquid were observed by adding washed frog
erythrocytes. The authors used DC current rather than AC and added
the refinement of television monitoring of the activity of the
mouthparts (Fig. 3).
Saliva has been obtained for chemical analysis by a number of
means. Salivary deposits have been collected from solid surfaces or
recovered from inert gels or membranes (Edwards, 1961; Miles,
1959b, 1965). Saliva has also been collected directly from the
mouthparts (Anders, 196 1 ; Miles, 1967b; Strong, 1970), sometimes
after the insects have been stimulated to salivate by placing them in a
humid environment or by injecting them with solutions containing
10% pilocarpine (Miles and Slowiak, 1970). Saliva has also been
collected by allowing the insects to probe inert absorbent materials.
Feir and Beck (1961) collected the saliva of the milkweed bug
(Lygaeidae) by allowing the insect to probe through the testa of a
0
milkweed seed into powdered cellulose. Schaller ( 1968a) collected
Oscilloscope
P recwder
47,
recorder
Monitor
Fig. 3. System for simultaneously recording and displaying optical and electrical data
from a feeding insect. (From Smith and Friend, 1971).
the saliva of several hundred aphids at a time by placing them in

successive batches on the undersurface of a piece of damp filter
paper, illuminated from above with yellow-green light. The aphids
were first deprived of food and water so that they no longer
produced honeydew as a contaminant. The saliva was eventually
eluted from the paper for analysis.
Adams and McAllan (1958) analysed saliva for one particular
enzyme by enclosing the insects directly over a spot of the substrate
on a strip of filter paper. A membrane was interposed between the
insects and substrate and the exploratory probes of the insects
through e.g. parafilm caused their saliva to be directly applied to the
substrate. Subsequent chromatography of the spot then revealed
whether any enzymic hydrolysis of the substrate had occurred.
In the larger Heteroptera particularly, recourse has been made to
analysis of enzymic activity of the whole glands or of the contents of
particular lobes (Miles, 1967a; Hori, 1968b). Chromatographic
separation of components of the secretions of the glands can be
conveniently carried out by using the whole glands themselves as the
“spot” at the origin of the chromatogram (Miles, 1967b).
Radioisotopes have been used both as a means of determining the
extent of salivary deposition in substrates (Fig. 4)and as a method of
tracing metabolites into the saliva and thus identifying salivary
components. Kloft et al. (1968) reviewed the methods used for
labelling the saliva of aphids by incorporating radioisotopes, 32P in
particular, into host plants or “sachets” of artificial diet enclosed in
parafilm. Onion leaves which had their cut stems placed in a solution
containing one or two mCi/ml Na2 32P04became radioactive within
three or more hours and aphids or Thysanoptera placed on the
labelled leaves acquired sufficient radioactivity over 24 h to make
their saliva traceable by autoradiography when the insects were
transferred to non-radioactive hosts (Kloft and Ehrhardt 1959a, b;
Kloft, 1960). Hennig (1 963) similarly placed the cut stalks of Vicia
faba leaves in solution containing 16pCi/ml for 5 to 20 h to label the
leaves in preparation for transfer of the label to Aphis fabae Scop.
Injection of from 0.5 to 10 pCi of radioisotope-labelled
metabolites directly into the haemolymph of Heteroptera has been
used to trace the transport of materials from the haemolymph into
the saliva and to demonstrate metabolic pathways leading to the
occurrence of individual compounds or classes of compounds in the
saliva (Miles, 1967b, 1969a). It became apparent that any compound
injected into the haemolymph was likely to appear in the saliva
190 PETER W. MILES
Fig. 4. Autoradiograph: Distriibytion of saliva labelled with '*P 'discharged by Myzus

ascolonicus in leaf of violet. (From Kloft, 1960).
within a few minutes unless it was first rapidly metabolized in the

haemolymph; but by injecting a labelled metabolite already known
to occur in the haemolymph, it was possible to demonstrate the
normal presence in the saliva of those compounds of which the
labelled metabolite was a precursor.
111. MODES OF FEEDING

I. Scratch-and-suck Feeding
The Hemiptera, according to Goodchild (1 966), probably arose
from insects that scratched the surfaces of growing plants, sucking
out the cell contents (Fig. 5). Such an architypal scratch-and-suck
mode of feeding is practised by the Thysanoptera, and probably also
by the Tingidae within the Heteroptera. Little is known about the
feeding of the tingids, however, except that these small insects feed
on cells immediately below the epidermis, for the most part causing
insignificant lesions. They are specialized Hemiptera nevertheless,
and if their mode of feeding should indeed prove primitive, it is
likely that it arose as a simplification of a more complex mode such
as the stylet-sheath feeding described below.
Even during the scratch-and-suck feeding of Thysanoptera,
radioisotopic labelling of the saliva indicates that some of it is
deposited in the cells on which the insects have fed (Kloft and
Ehrhardt, 1959b) and species of both Thysanoptera and Tingidae are
known to cause galls. Discharge of saliva into food sources is
characteristic of the Hemiptera and it is convenient to distinguish
between at least four major modes of feeding among the Hemiptera
based partly on food source and partly on the function of the saliva.
2. Stylet-sheath feeding
All the Homoptera and the Heter0ptera:Pentatomorpha are able
to discharge at least two different kinds of saliva; one that solidifies
rapidly on ejection and another that always remains watery and that
leaves only a trace of solid matter evaporation.
During the normal course of feeding on growing plant tissues, the
solidifying kind of saliva is ejected wherever the stylets penetrate and
is moulded by the action of the stylets to form a tubular lining to the
path taken by them, thus forming the so-called “stylet-sheath”. The
watery saliva is also secreted before and during penetration of the
substrate, as well as on withdrawal of the stylets and the functions of
these secretions will be discussed in detail in Section VII.
3. Lacerate-and-gush feeding
Some members of the Pentatomorpha, particularly the Lygaeidae
and Pyrrhocoridae, feed on seeds. When they do so they secrete only
a surface “flange” of sheath material, that is not continued as a
stylet-sheath into the seed. Instead, the stylets and watery saliva are
Reduviidae Miriabe
Cimicidae etc. Tingidae Y
v,
predatory return to h)
forms plant-feeding carnivorous Geocorinae

\ / Asopinae Coreoidea
Hydrocorisae Amphibicorisae Cimicomorpha \
\ - -- - Pen tatornoidea
\ surface Saldidae
\
subaquatic
/ skating litoral Pen tatornorpha
Corixidae habit
algophagous shbre stylet-sheath feeding on sap,
litter \? lacerate-and-flush on seeds or prey
/
abhity to secrete a cornplite ability to secrete a stylzsheath
stylet sheath lost: mostly carnivorous retained: phytophagous
/
I I /
Dipso corimorpha
Jassomorpha other
/Geocorisae Cicadomorpha Sternorrhyncha
\? /
litter-inhabiting OmniVOrOUS forms, Fulguromorpha Malpighian tubules
lacerate-and-flush feeding evolved
I / reduced ;
\ \
posterior junctidn antehor junition tubules lost
Coleorrhyncha - >
of mid and hind gut of mid and hind gut
stblet-sheath fehing
evolved; mesophyll-
\
A phidoidea
feeding, true Hemiptera

I
scratch-and-suck
pre-Hemipterans -THYSANOPTERA
Fig. 5 . Evohtionary interrelationshipsbetween divisions of Hernipternbased on physiology of feeding. OVIodifi from Goodchild. 1966.)
THE SALIVA OF HEMIPTERA 193
used to lacerate and macerate a pocket of cells or the entire contents

of the seed according to its size. The contents are finally flushed out
with a copious flow of dilute saliva.
Elsewhere among the Heteroptera, phytophagous forms are found
within the Cimicomorpha: namely the Tingidae and many species of
Miridae. These insects produce no stylet-sheath, yet they feed on the
roots and shoots of growing plants. The tingids are mostly very small
and probably feed on individual cells or small numbers of them near
the epidermis, but the phytophagous mirids apparently use a
lacerate-and-flush method of feeding on pockets of cells in a manner
very much like that of the Pentatomorpha when they feed on seeds.
Thus the derivation of lacerate-and-flush feeding on plant tissues by
the Cimicomorpha is perhaps to be seen as a necessary consequence
of their loss of ability to secrete a stylet-sheath.
4. Predation
Many Heteroptera feed on small prey and they employ what is in
effect lacerate-and-flush feeding. Indeed, some of the mirids among
the Cimicomorpha are carnivorous as larvae and phytophagous as
adults. In the Pentatomorpha too, cannibalism is practised and
undoubtedly the seed-feeding forms employ much the same
technique whether feeding on seeds or individuals of their own kind.
The main difference between phytophagous lacerate-and-flush
feeding and predation proper lies in the composition of the saliva; for
the saliva of the predators causes rapid immobilization of their prey,
while the phytophagous bugs can practise cannibalism only on
incapacitated individuals or on eggs. Further, the true predators are
not known to produce a stylet-sheath.
5. Blood-sucking
Blood-sucking Hemiptera are found within the Cimicomorpha
only. Despite the observation that the phytophagous Cimicomorpha
secrete no sheath material, in at least one of the blood-sucking
Reduvioidea, Rhodnius prolixus Stbl, traces of a solidifying secretion
are deposited at the point on the surface of the skin about to be
penetrated (Friend and Smith, 197 1). No stylet-sheath is formed,
however. The mandibles force their way a short distance into the
skin and the maxillae alone penetrate deeper, thrusting first one way
and then another until a blood vessel is penetrated (Lavoipierre et al.,
1959; Smith and Friend, 1971). Little or no histolysis of the tissues
of the host occurs. Indeed, the success of feeding depends on
avoidance of sensory reaction on the part of the host.
Alp-9
194 PETER W. MILES
IV. STYLET-SHEATH FEEDING

A . SAMPLING THE SURFACE
All phytophagous Hemiptera, Homoptera as well as Heteroptera,

often touch a surface several times with the labium before settling
down to feed. It has been suggested (Miles, 1959b) that during this
initial period, gustatory stimuli are picked up by watery saliva that is
ejected and almost immediately sucked back into contact with the
gustatory receptors that form the epipharyngeal organ (Wensler and
Filshie, 1969). Exploration of surfaces with the mouthparts by
aphids may or may not be accompanied by actual penetration.
Hennig ( 1963) observed that when the black bean aphid, Aphis fabae
Scop. touched leaf surfaces several times with the labium, each touch
could last between 5 and 60 s and that the epidermis was sometimes
penetrated, sometimes not. Often sheath material was deposited to
form an external flange (Fig. 6) and when the stylets penetrated the
surface, more sheath material was sometimes secreted and formed a
short canal through the surface. At other times, however, deposits of
sheath material were almost imperceptible or non-existent.
I
200p
d
Fig. 6. Flanges of sheath material. a: aphid probes into a leaf surface; a short sheath
accompanies the probe into a mid-lamella. (After Hennig, 1963). b: aphid penetrating
parafilm membrane and building a sheath in a solution-showing formation of the flange
within the tip of the labium and the bead-like appearance of the sheath. (After Miles,
1968b). c: formation of flange by Rhodnius on rubber membrane. (After Friend and Smith,
1971). d: flange formed on testa of milkweed seed by Oncopeltus. (After Miles, 1967a). e:
formation of flange external to labium by Dysdercus feeding on cotton seed. (After Saxena,
1963).
Such observations make it important to distinguish between an

actual penetration of a surface-a true probe-and a mere touching of
the surface-a dab. Hennig ( 1963) was unable to obtain any evidence
that during these dabs and probes, any radioactivity was taken up
from plants labelled with 32P; on the other hand, his results indicate
only that aphids had not taken up quantities of radioactivity large
enough to be measured; it is also possible that the sucking back of
watery saliva brought into very brief contact with the surface of a
leaf plant labelled with 3? would not pick up the label at all.
Miles (1 959a) observed that aphids with their stylets exposed and
in contact with glass ejected and sucked back minute quantities of
watery saliva quite distinct from the solidifying sheath material;
while McLean and Kinsey ( 1964), during the electronic recording of
feeding by aphids, also obtained evidence that some fluid was ejected
and sucked back on impenetrable surfaces. Heteroptera will spend a
considerable time dabbing surfaces that contain soluble food
materials, while at the same time ejecting. and sucking back watery
saliva (Miles, 1959b; Saxena, 1963; Bongers, 1969).
B. SECRETION OF THE FLANGE
When Homoptera and Heteroptera : Pentatomorpha feed on plant

tissues, typically a small amount of sheath material is first secreted on
the surface and the stylets then push through the solidifying material
and begin to penetrate the substrate. This external sheath material
has been termed a “flange” (Nault and Gyrisco, 1966).
Exceptions have been noted. Saxena (1963) stated that the
pyrrhocorid Dysdercus koenigii ( F . ) produced a flange on the hard
testa of a cotton seed or on the intact cuticle of stems and leaves, but
no sheath material was secreted at the surface of slices of cottonseed
kernel. Hori (1968a) claimed that when the pentatomid Eurydema
rugosa Motschulsky fed on cabbage leaves, it did not always secrete a
flange or any other sheath material when the stylets subsequently
remained solely within the mesophyll; but the insect did produce
both flange and sheath when the destination of the stylets was a
phloem vessel. Hennig (1 963) indicated that short probes by Aphis
fubae Scop. into epidermal cells were not necessarily accompanied by
a flange or sheath.
Saxena’s observation on Dysdercus can be interpreted as indicating
that this insect secretes a sheath only when its stylets encounter a
hard substrate during attempts at penetration. But there is no simple
196 PETER W. MILES
explanation for the observations of Hori and Hennig. They would

seem to imply that, at the moment of penetration, the subsequent
pattern of feeding is already determined-i.e. if no flange has been
secreted, subsequent feeding will be on mesophyll cells (and not on
vascular tissue) or only a short “exploratory” probe will be made
(and the stylets will not penetrate further). Presumably such
predetermination of stylet activity would have t o be due to the
physiological state of the individual. One possibility is that
subsequent feeding behaviour depends on the ability of the insect to
produce sheath material when it first attempts penetration of the
substrate. Nevertheless, McLean and Kinsey (1 969) found no loss of
ability of an aphid to secrete sheath material with starvation and
further investigation of this problem is clearly required.
Despite the few reports to the contrary noted above, the usual
course of events during feeding by Homoptera and Heteroptera:
Pentatomorpha is the secretion of a drop of solidifying saliva on the
surface at the point where penetration of the stylets will begin; and
this now seems to be true even of a blood-sucking reduviid Rhodnius
prolixus Stll (Friend and Smith, 1971) that until recently was
thought unable to produce any secretion similar to the stylet sheath
of the phytophagous bugs.
The initial secretion of sheath material on to a surface results in a
flange of more or less circular cross section surrounding the point of
penetration. The flange extends either around the labium or into the
labial groove (Fig. 6).
C. FORMATION OF THE SHEATH
A flange is not necessarily continued as a stylet-sheath into the

substrate below. When the seed-feeding lygaeids and pyrrhocorids
penetrate a hard surface, the flange is continued only a short way
beyond the surface (Miles, 1959a, 1967a; Saxena, 1963). When
Aphis fubae probes the body of an epidermal cell, further sheath
material is unlikely to be secreted; whereas if the stylets have struck
an intercellular groove, secretion of a stylet sheath is more likely,
whether or not the penetration continues further into the plant
(Hennig, 1963).
Mostly, however, when Homoptera and Heter0ptera:Pentato-
morpha feed on the roots or shoots of plants, it is found that
a flange of sheath material is secreted on the surface and is
continuous with a stylet-sheath laid down wherever the tips of the

stylets penetrate (Fig. 7).
Precise details of the way in which a stylet-sheath is formed have
been furnished by McLean and Kinsey (1965, 1968). The stylets
characteristically move into tissues by a series of backward and
forward movements. When the stylets are at the end of a backward
sequence, a drop of sheath material is secreted; watery saliva is
ejected into this, making it balloon out; the stylets then push
forward through the material and pierce the end of it (McLean and
Kinsey, 1968). At this stage, the substrate may be sampled by
sucking. The stylets then move back again and sheath material is
again secreted. In this way, each new drop of sheath material is
secreted in contact with the last piece and becomes part of a
coherent sheath. In a soft, uniform medium, the stylet-sheaths of
aphids thus have a typically beaded structure (Fig. 6); but in
materials of varied structure and texture, the sheath may flow into
the space surrounding the stylets or be squeezed into a space so
narrow that it almost disappears. When stylet-sheaths pass through
solid materials (e.g. when an aphid’s stylets pass through unstretched
parafilm) it would seem that the insect is sensitive to the
backpressure caused by the medium and that less material is secreted.
Even so, it is under these circumstances that some aphids begin to
suck back some of the sheath material before it has completely
solidified and it then remains as an indigestible deposit in the
mid-gut. (Moericke and Mittler, 1965). Possibly the thinness of the
sheath when it is secreted within narrow confines in relatively rigid
structures accounts for some confusion on whether stylet sheaths are
continuous within plant tissues or not (Miles, 1968b).
D. DISCHARGE OF WATERY SALIVA
Some watery saliva is ejected by aphids as part of the process of

formation of the sheath (McLean and Kinsey, 1965); and as the
stylets push through each new drop of sheath material, this watery
saliva is released. When the secretions of aphids have been labelled
with 3?, diffusible components of the saliva can be traced for some
distance beyond the stylet-sheath in, for instance, leaves (Fig. 4).In
aphids and some other Hemiptera the diffusing secretion contains
enzymes such as pectinase and cellulase (see Section VI1,B) that
presumably aid penetration of the plant tissues.
The phytophagous Hemiptera continually sample any substrate
198 PETER W. MILES
THE SALIVA OF HEMIPTERA
Fig. 7. The feeding of Aulacaspis tetalensis (Zhnt.), Coccidoidea, in sugar-cane stems. a-c: stylets and stylet-sheaths in cortical cells:
199
.-c
c: pierced cell that has collapsed; d: barbed tip of stylet (scale = 5 0 ~ )(From
. Williams, 1970.) \o
200 PETER W. MILES
through which the stylets are passing by sucking back small amounts
of liquid. Aphids periodically suck whatever fluids are present when
the stylets have just emerged from the last drop of sheath material
secreted; this has been indicated by the electronic methods of
McLean and Kinsey (1967), the uptake of radioactivity from very
heavily labelled plants (Garrett, personal communication) and from
the sucking back of sheath material that has been unable to solidify
when aphids probe unstretched parafilm (Moericke and Mittler,
1965).
All Hemiptera would seem to react to an inability to suck fluids
when they attempt to do so by alternately discharging small
quantities of watery saliva and sucking back (Miles, 1959b; Saxena,
1963; McLean and Kinsey, 1967). In this way insoluble materials are
brought into solution (Saxena, 1963) or viscous solutions diluted
(Miles, 1959b).
E. INGESTION
Once the stylets have penetrated a source of ingestible food (e.g. a

phloem seive tube), no more saliva is ejected (Kloft, 1960) unless the
food canal should subsequently become blocked. Rapid movements
of the tips of the stylets then occur, and if this does not dislodge the
Dendrites b
Fig. 8. Stylets of Myzus persicae. a: tip of left maxilla. b: cross section of maxillae. c:
cross section of whole bundle. fc-food canal; md-mandible; mx-maxillae; sc-salivary
canal. (After Forbes, 1969).
THE SALIVA OF HEMIPTERA 20 1
particle, a small amount of sheath material is secreted (McLean and

Kinsey, 1965). This last technique is effective because the functional
opening of the salivary canal lies a short distance behind the
functional opening of the food canal (Fig. 8). McLean and Kinsey
(1967) ascribe a characteristic sequence of change of electrical
resistance between aphid and substrate (the “X-waveform” Fig. 2) to
the accumulation of callose slime around the tips of the stylets when
they have been inserted into phloem sieve tubes and the clearing of
the slime by short bursts of salivation.
Those insects that feed on mesophyll tissue by the stylet-sheath
method eject watery saliva continually (Kloft, 1960). Presumably
they eject saliva into each cell on which they feed and suck out the
contents before the secretion of the sheath is continued and the
stylets move on to another cell.
F. WITHDRAWAL OF THE STYLETS
The watery saliva has immediate effects on plant cells into which
it diffuses, causing increased respiration and streaming of the
protoplasm (Kloft, 1960); effects very likely caused primarily by an
increase in the permeability of the cell membranes.
Hemiptera may withdraw their stylets through the stylet-sheath
completely, or they may draw back the tips of the stylets for a short
distance before the stylet bundle is thrust through the side of the
sheath to produce a branch in the sheath. Whenever the stylets
retreat, even during the final withdrawal of the stylets, the
surrounding cells again show transient increases in respiration, as
though once more affected by the emission of saliva (Kloft, 1960). It
has in fact been shown by Kinsey and McLean (1967) that when
aphids withdraw their stylets voluntarily from plants, the end of the
stylet sheath is sealed and the central canal filled up with secretion.
It seems likely that any effects on the plant tissues that occur
during withdrawal of the stylets are due to the saliva emitted at the
moment withdrawal begins, as it is improbable that mechanical
stimulation of the plants’ cells during withdrawal of the stylets
would be significant and Kinsey and McLean (1967) have demon-
strated that once the end of the sheath is sealed by the insect, dyes
will not diffuse from the central canal to the exterior of the sheath.
They conclude therefore that all ingestion by aphids is through the
open end of the sheath and not from materials diffusing through its
walls; at the same time it follows that saliva would be unlikely to
diffuse outwards through the walls of the sheath.
202 PETER W. MILES
These observations are a clear indication of the sealing properties

of the sheath. Since the central canal of the sheath is moulded by the
stylets themselves, the insect may be forced to fill the canal of the
sheath with saliva during withdrawal of the stylets by the suction
that would occur otherwise. What kind of saliva remains in the
central canal of the sheath has not been determined with certainty.
The photographic evidence produced by Kinsey and McLean (1 967)
would seem to indicate that it is sheath material itself; although
observations on lygaeids (Miles, 1959b) were that the central canal of
the sheath is filled with watery saliva on voluntary withdrawal of the
stylets.
V. LACERATE-AND-FLUSH FEEDING
Lygaeids, pyrrhocorids and some pentatomids will feed either on
seeds or on the growing tissues of plants. When feeding on phloem
sap, the lygaeid Oncopeltus fusciutus (Dall.) secretes a complete
stylet-sheath, but when feeding on seeds, it secretes a flange of
sheath material which is continued as an abbreviated tubular
structure within the seed (Miles, 1967a; Bongers, 1969), be it a
milkweed seed on which the insect normally feeds or a peanut (Miles,
1959b). Saxena (1963) points out that Dysdercus secretes such a
flange only when the surface covering the food material is
non-porous and insoluble: the cut surface of a seed kernel does not
induce the secretion of sheath material.
Once the stylets of a seed-feeder are within the kernel, the feeding
activity is very different from typical stylet-sheath feeding. The
stylets are pushed first one way and then another for periods of up
to two hours when Oncopeltus feeds on milkweed-seeds or
Dysdercus on cotton seeds (Saxena, 1963). During this period, the
whole contents of a small seed (Miles, 1969b) or a pocket of cells in
a larger seed (Miles, 1959b; Saxena, 1963) will be rendered fluid and
removed. How this is achieved may differ, however, with different
species.
Oncopeltus when feeding on a milkweed seed, reduces the solid
contents to a thin juice which can be squirted out of the seed, the
liquid being derived from the watery saliva. The insect finally sucks
out this juice, leaving the testa practically empty. Bongers (1 969)
calculated that an individual Oncopeltus injected some 1.14 mg of
salivary solids into a milkweed seed during the process of digesting
and flushing out its contents. How great a volume of saliva this
represented was difficult to estimate, since Bongers found almost no

solids at all in the watery saliva he was able to collect. This apparent
anomaly is probably explicable in terms of the ability of Hemiptera
to vary the dilution of the watery saliva they secrete (see
Section VI1,B)
Dysdercus appears to suck back its watery saliva immediately after
it is discharged and thus significant quantities of watery saliva do not
accumulate within the cotton seed kernels on which it feeds.
External digestion of, for instance, starch grains too large to be
sucked into the salivary food canal of the stylets can easily occur
when Oncopeltus is feeding, but Saxena (1 963) concluded that this
was impossible when Dysdercus fed and that disintegration of larger
particles was due mainly to mechanical action aided, at the most, by
physical solution in the watery saliva. Nevertheless, all seed feeders
seem to require relatively large amounts of water to drink if they
continue to feed exclusively on dry seeds and liquefaction of the
contents of seeds, whether by physical solution and disruption or by
enzymic action, requires the insect to secrete large amounts of
watery saliva during feeding (Saxena, 1963; Bongers, 1969).
The mirids and tingids of the Cimicomorpha secrete no sheath
material in the sense of producing a coherent tubular structure;
although early descriptions of feeding by mirids included accounts of
“granular”, deeply staining material within histological sections
through feeding punctures (Smith, 1926). In the light of recent
reports of a secretion akin to sheath material being secreted by even
blood-sucking reduviids (Friend and Smith, 197 l ) , the categorical
statement that sheath material is not secreted by the Cimicomorpha
(Miles, 1968b) must be revised.
Mirids lacerate and flush out pockets of adjacent cells when they
feed. They do not seem to be adapted to feed on dry seeds, and feed
mostly on growing tissues and fruits. The general process of feeding
is similar to that of lygaeids and pyrrhocorids, however, as indicated
by the water-soaked patches of tissue that they produce, and the
silvery appearance of the air pockets left behind when they have
finished.
VI. FEEDING BY CARNIVORES

Lacerate-and-flush feeding is clearly akin to feeding by predators;
some species of mirids are carnivorous, as are some pentatomids and
lygaeids and even the phytophagous Pentatomorpha are capable of
204 PETER W. MILES
cannibalism and suck eggs. It is interesting to note that when

Oncopeltus feeds on the eggs or other individuals of its own species,
it first secretes a flange of sheath material on the surface; thus seeds
and prey are treated alike. The seed feeders, however, require an
immobile food source and will attack only disabled individuals, while
the true carnivores must rapidly immobilize their prey. The
difference in the feeding process between the two forms thus resides
in the chemical content of the saliva.
Predatory (as opposed to blood-sucking) reduviids inflict painful
bites on man. Some species spit their saliva for distances up to 30 cm
as a defensive mechanism. As Edwards (1 96 1) showed, this spitting is
without effect on the normal invertebrate prey of the insect, for the
saliva is harmless when applied topically to arthropods or even when
ingested by them. The spitting is apparently “aimed” at the sensitive
mucous membranes of the eyes, nose and mouth of potential
vertebrate enemies. Once the saliva is injected into an arthropod,
however, it is highly toxic. The reduviid Platymerus rhadamanthus
Gaerst immobilizes a large Periplanetu americana within two t o five s
by injecting about 10 mg of saliva (Edwards, 1961). The saliva of
predators in the Hydrocorisae and in other Geocorisae similarly
rapidly immobilizes the prey.
The offensive function of spitting by Platymerus probably
explains the concentrated nature of this secretion, which Edwards
used as a source for analysis of the saliva. In sharp contrast, the saliva
ejected by the phytophagous forms outside their food is very dilute
indeed (Strong and Kruitwagen, 1968; Bongers, 1969). Edwards
(1961) compared the saliva of Platymerus to snake venom: both
contain hyaluronidase, proteinase and phospholipase, although the
activity of the salivary phospholipase of the insect was somewhat
weaker than the phospholipase of snake venom. The hyaluronidase
acted as a spreading agent, reducing the viscosity of some body fluids
and attacking the intercellular matrix, thus speeding tissue lysis by
the other enzymes. There was particularly rapid disruption of neural
function, mainly due to lysis of the outer phospholipid membranes
of nerves. The insect did not, however, contain ATP-ase or serotin,
which are commonly present in snake venom, but which are
presumably specifically adapted to vertebrate prey.
By comparison, the saliva of the insects that suck vertebrate blood
seems to contain no venom-indeed the habit depends for its
effectiveness on the absence of immediate reaction on the part of the
host (Table I). Little is known of the composition of the saliva of the
blood-suckers, however.
Table I
Toxicity of Hemiptera salivary gland homogenates as indicated b y effect o n
heart beat of Periplanetaa
Donor species Dilution factorb Action
I. Predators
Naucoris cimicoides 40 Immediate cessation

Platymeris rhadamanthus 40 Immediate cessation
R h in coris carm elita
Reduvius personatus
11. Phytophagous bugs
Pentatoma rufipes 1 Slight increase in rate:
cessation after some
minutes
Oncopeltus fasciatus 1 Slow decrease in
, amplitude
111. Blood-suckers
Rhodnius prolixus
Triatoma protracta i 10 No action
(I Data from Edwards (196 1).

The unit is a pair of glands homogenized in 0.05 ml saline; larger numbers indicate
relative increases in dilution.
VII. CHEMICAL COMPOSITION AND FUNCTION OF THE SALIVA
A. SHEATH MATERIAL
The Homoptera and Heter0ptera:Pentatomorpha produce an oral

secretion that originates from the salivary glands and that solidifies
very rapidly after secretion. Such recent studies as have been done on
this material, whether from aphids, pentatomids or lygaeids, indicate
that it is mainly protein, but contains about 10% phospholipid and
probably some conjugated carbohydrate (Miles, 1964b, 1967b). It is
mainly hydrogen bonded, but is stabilized by disulphide linkages
(Miles, 1967a, 1969a). Once formed it is impermeable (Kinsey and
McLean, 1967). It is also inert, for when aphids ingest their own
sheath material, they are unable to digest it (Moericke and Mittler,
1965, 1966). When first secreted, the precursors of the sheath
material are admixed with soluble amino acids and these diffuse from
206 PETER W. MILES
the sheath during the second or less while it is solidifying (Miles,

1964b).
Oxidizing enzymes are secreted with the sheath material, which in
some species actually appears to be tanned by these enzymes (Miles,
1964b). The sheath can be formed in the absence of oxidizing
enzymes however (Miles, 1967a), and these enzymes are probably
also secreted by Hemiptera that secrete no sheath (Miles, 1964a).
The precursors of the sheath material are secreted by specialized
lobes of the salivary glands and are discharged more or less
independently of the other products of the glands. The secretions of
all parts of the glands are nevertheless freely miscible with one
another and the sheath material shows no signs of beginning to
solidify if for instance the contents of the glands are mixed together
in vitro, as long as oxygen is rigorously excluded (Miles, 1959b,
1967a).
Within the glands, the precursors of the sheath material are
maintained in solution by reducing conditions, probably due to the
presence of free sulphydryl groups (Miles, 1967a). The precursors are
intimately mixed with amino acids that are presumed to prevent the
formation of hydrogen bonds by maintaining a high dielectric
constant (Miles, 1964b). Any other secretions of the salivary glands
that are likely to be mixed with the sheath precursors before they are
ejected are similarly reducing and contain free amino acids, although
the analysis of freely soluble metabolites differs in different parts of
the gland (Miles, 1967a, b).
Once the precursors are secreted, diffusion of amino acids out of
the mixture and the presence of free oxygen rapidly bring about
solidification by hydrogen bonding and disulphide bonding respec-
tively. The oxidizing enzymes present in the saliva undoubtedly assist
in the oxidative part of the process of solidification, although they
do not appear to be essential (Miles, 1967a).
The work of Friend and Smith (1 97 1) indicates that the secretion
of sheath material by Homoptera and Pentatomorpha is matched in
Rhodnius prolixus, a blood-sucking bug within the Cimicomorpha
which secretes a flange at the surfaces it penetrates; but nothing is
yet known of its composition.
The function of the stylet-sheath remains problematical, despite
discussion by several authors (Mittler, 1954; Saxena, 1963; Miles,
1968b; Bongers, 1969). Mittler’s suggestion that it serves t o seal the
stylets of Homoptera into cells (e.g. phloem sieve tubes), the
contents of which are under turgor pressure, still seems sound when
applied to sap-sucking aphids, particularly since recent studies have

confirmed that these insects require a diet under pressure for their
optimum growth (Wearing, 1968).
The claim by Hori (1 968a) that the pentatomid Eurydema secretes
a sheath when feeding on phloem sap, but not when feeding on
mesophyll cells, would seem to be evidence that in the Pentato-
morpha also, the sheath is an adaptation to feeding on pressure
systems. But the foregoing does not explain why no sheath is
produced by Dysdercus when it feeds on phloem sap (Saxena, 1963)
or why Homoptera that feed only on mesophyll tissue do produce a
stylet-sheat h.
Saxena suggested that the flange secreted on to surfaces by
Dysdercus enabled the insect to attach the labium firmly to the
substrate without the danger of the mouthparts slipping sideways
while the stylets were forced into the substrate. This explanation is
supported by the cement-like nature of the sheath material and its
ability to adhere to waxy surfaces of plants by virtue of its
phospholipid content (Miles, 1968b), but such an explanation
ignores the complete stylet-sheath that most phytophagous bugs
secrete within plant tissues.
Miles (1968b) contrasted the relatively small lesions made by
stylet-sheath feeders of the Pentatomorpha with the large lesions
produced by lacerate-and-flush feeders of comparable size in the
Miridae. He suggested that if the stylet-sheath is seen as maximizing
the efficiency of feeding on individual cells by preventing losses into
intercellular spaces, then, in contrast, lacerate-and-flush feeders
probably need to scavenge the contents of ruptured cells with
large quantities of dilute saliva.
Possibly the functional significance of the stylet-sheath can
properly be appreciated only in an evolutionary context. Goodchild
(1966) discussed the evolution of the physiology of the digestive
system of Hemiptera in relation to sources of food. Although he did
not refer to the secretion of sheath material, his ideas are relevant to
it: as already noted in Section 11, he would consider the primitive
mode of feeding in the Hemiptera to be stylet-sheath feeding (that
arose from scratch-and-suck feeding, presumably when the insects
had developed the ability to secrete a solidifying saliva). Secondarily,
the Heteroptera became omnivorous. Even among the Homoptera,
the secretion of a stylet-sheath may not occur automatically
whenever the stylets are used (Hennig, 1963) and presumably some
of the ancestral Heteroptera lost the ability to secrete a stylet-sheath
208 PETER W. MILES
almost entirely when they became predators, using the stylets and
saliva as a lacerate-and-flush system.
Goodchild assumed the mirids to be evolved from such predatory
ancestors. If so, they retained the lacerate-and-flush system perforce
because unable to secrete a stylet-sheath; indeed Goodchild
specifically compares the feeding of the bryocorine mirids with that
of the predatory Heteroptera. At the same time, it would appear that
predators such as the reduviids include species that retain some of
the ancestral ability to secrete sheath material, as the recent
discovery of the salivary flange secreted by Rhodnius prolixus has
demonstrated (Friend and Smith, 197 1 ).
Within this evolutionary interpretation, the Heter0ptera:Pentato-
morpha must be seen as Heteroptera that have retained the
stylet-sheath feeding habit, but that nevertheless display some of the
possible intermediate kinds of feeding between stylet-sheath and
lacerate-and-flush. Thus the seed-feeders use both and also perhaps so
do the pentatomids such as Eurydema which according t o Hori
(1968a), uses the stylet-sheath method when it sucks phloem sap and
the equivalent of a lacerate-and-flush technique when feeding on
mesophyll. According to Saxena’s descriptions, Dysdercus has almost
lost the use of a stylet-sheath, but retains the flange alone-perhaps
because of its value in steadying the stylets during the initial
penetration of a surface which, if a cotton seed, may be particularly
hard to penetrate.
An evolutionary interpretation in this way allows for the retention
of ancestral habits and for changes in function that would be
difficult to envisage in a strictly functional analysis.
B. WATERY SALIVA
Some of the known components of the non-gelling secretions

(watery saliva) of the salivary glands are summarized in Table 11. The
watery saliva is a vehicle for hydrolysing (“digestive”) enzymes.
Many of the Heteroptera can be induced t o secrete a watery liquid
from the free tips of the stylets while these are outside food
substrates; e.g. by manipulation of the labium, especially after
subjecting the insects to a humid atmosphere or after injecting them
with pilocarpine (Miles and Slowiak, 1970) or by amputation of the
antennae (Clarke and Wilde, 1970a). Nevertheless, there is doubt
whether this experimentally induced secretion properly represents
the watery saliva secreted within substrates. Strong and Kruitwagen
Table I1
-$
I
Some recent studies of the soluble contents of the salivary secretions of Hemiptera
0 Compounds Insects studied Features noted References
1. Enzymes
Amylase Oncopeltus fasciatus (Dall) Occurrence Feir and Beck (1 96 1)
(Lygaeidae)
Origin in glands Miles (1 967a)
Heteroptera (various families) Activation by C1- Hori (1969)
and NO3
Lygus disponsi Linnavouri Characteristics Hori (1970a, d)
(Miridae)
Variability in quantity Hori (1 970b)
Role in digestion Hori (1 970c)
Empoasca fabae (Harris) Occurrence Berlin and Hibbs (1 963)
(Jassoidea)
Cellulase Aphididae Occurrence Adams and Drew (1963a)
Heat stability Adams and Drew (1963b)
Oligosaccharases Oncopeltus fasciatus Occurrence . Feir and Beck (1 96 1 )
Dolycoris bascarum L. Occurrence Nuorteva and Laurema ( 1 96 1b)
(Pentatomidae)
Lygus disponsi Absence Hori (1 970c)
Empoasca fabae Occurrence Berlin and Hibbs (1 963)
Pectin- Aphididae Variable occurrence Adams and McAllan (1958)
polyglacturonase
Auchenorrhyncha Absence Laurema and Nuorteva ( 1 96 1)
Heteroptera Occurrence in Miridae Laurema and Nuorteva (1961)
only
Lygus hesperus Knight Role as spreader Strong (1 970) N
(Miridae) in phytotoxicity 0
\D
Table 11-cont.
Compounds Insects studied Features noted References
1. Enzymes
Hyaluronidase Platymeris rhadamanthus Role as spreader in Edwards (1 96 1)

Gaerst. (Reduviidae) toxicity to prey
Proteinase Platymeris rhadamanthus Role in toxicity Edwards (1 96 1)
Oncopeltus fasciatus Occurrence Feir and Beck (1961)
(Lygaeidae)
Empoasca fabae Occurrence Berlin and Hibbs (1963)
(Jassoidea)
Dolycoris baccarum L. Variability in Nuorteva and Laurema (196 1b)
(Pentatomidae) quantity
Lygus disponsi Variability in quantity Hori (1970b)
(Miridae)
Aphididae General properties Hori (1970d)
Occurrence Schaller (1 968a)
EsteraseILipase Oncopeltus fasciatus Occurrence Feir and Beck (1 96 1)
(Lygaeidae)
Origins in glands Miles (1967a)
Phospholipase Platymeris rhadamanthus Role as neurotoxin Edwards (1 96 1)
(Reduviidae)
Acid phosphatase Pyrrhocoris apterus L. Occurrence Kloft (1 960)
(Pyrrhocoridae)
Phosphorylase Pyrrhocoris apterus L. Occurrence Kloft (1960)
(Pyrrhocoridae)
Phenolase/ Hemiptera Presence in glands of Miles (1 964a)
peroxidase phytophagous and
predatory species
Pentatomorpha Miles (1964a) and
(Pentatomidae and Occurrence Miles and Slowiak (1 970)
Lygaeidae)
Oncopeltus fasciatus Origin in glands Miles (1 967a)
(Lygaeidae)
Aphididae Occurrence Miles (1965) and
Miles and Slowiak (1970)
General Discussion of role Miles (1 969b)
2. Metabolites
Amino acids Aphididae Occurrence and Kloft (1960);
phytotoxicity Anders (1961) and
Schaller (1 968b)
Pentatomorpha
(Pentatomidae and Occurrence and Miles (1964a, 1967a, b)
Lygaeidae) transfer to saliva
Phenylalanine/ Pentatomorpha Role in experimental Miles (1964b, 1968a)
Tyrosine/DOPA (Pentatomidae and induction of galls
Lygaeidae)
Cysteine and Aphids Occurrence Schaller (1968a)
derivatives
Eumecopus punctiventris Occurrence and Miles ( 1 969a)
Stil (Pentat omidae) m etab o h m
212 PETER W. MILES
(1968) have shown that the secretion discharged from the free tips of
stylets of Lygus hesperus Knight outside plant tissue lacks detectable
quantities of the enzymes the insects discharge within feeding
punctures. The lygaeid Oncopeltus is known to secrete esterase into
substrates (Feir and Beck, 1961) and the enzyme can be found in its
salivary glands-yet Miles (1967a) was unable t o detect it in saliva
collected directly from the tips of the stylets.
It would thus seem that the watery saliva of phytophagous
Hemiptera is of varying composition. When secreted within plants it
contains hydrolysing enzymes, but it is subject t o varying degrees of
dilution and when discharged outside plants may contain little but
water.
Studies based on the watery saliva collected from the free tips of
the mouthparts are thus of limited use in determining the com-
position of the saliva; yet it is indeed difficult to collect the watery
saliva secreted within plants. Saxena (1 963) managed to collect drops
of saliva discharged by Dysdercus while it was feeding on thin slices
of cotton seed kernel. The best attempts so far t o analyse watery
saliva as actually discharged into plants have been made by allowing
aphids t o probe into damp filter paper (Schaller, 1963); by caging
Homoptera over filter paper covered with plastic membrane or
parafilm (Adams and McAllan, 1958) or by allowing larger insects to
probe through the surface of a normal food material into a pocket of
powdered cellulose (Feir and Beck, 1961).
The results of such experiments are still open to some doubt. One
of the functions of the very dilute saliva discharged by Hemiptera is
probably the bringing back of soluble materials to the gustatory
sensilla of the epipharyngeal organ; thus in the absence of the
gustatory stimuli normally associated with food-for instance in filter
paper or powdered cellulose-the watery saliva discharged might still
lack the normal concentration of salivary enzymes secreted into
food.
The closest approach to determining salivary enzymes under the
natural conditions of their secretion is probably that of Adams and
McAllan (1 958) who have caged insects over filter paper impregnated
with the pure substrates for the enzyme. By determining the
breakdown or otherwise of these substances chromatographically,
they were the first t o demonstrate the secretion of pectin
polygalacturonase by Hemiptera. Other studies of this enzyme are
summarized in Table 111. Salivary polygalacturonases are assumed to
aid the disruption of the midlamellae of the cell walls of plants rather
Table 111
Occurrence of pectinase in the saliva of Hemiptera
~
1. Present
Aphididaea
Aphis abbreviata Patch In both apterae and alatae

Dactynotus sp. In both apterae and alatae
Macrosiphoniella millefolii In both apterae and alatae
(DeGeer)
Myzus persicae (Sulz) In both apterae and alatae
Rhopalosiphum rhois (Monell) In both apterae and alatae
Aphis fabae Scop. In apterae, not always in alatae
Aphis sedi Kltb. In apterae, not always in alatae
Aphis spireacola Patch In apterae, not always in alatae
Eriosoma americanum (Riley) In apterae, not always in alatae
Eriosoma lanigerum (Hausm.) In apterae, not always in alatae
Phorodon humili (Schrank) In apterae, not always in alatae
Aulacorthum solani Known from apterae only
Cinara spp. Known from apterae only
Periphyllus negundinis (Thomas) Known from apterae only
Pterocomma spp. Known from apterae only
Schiz olach n is pin i-radiata (Davidson) Known from apterae only
Thomasiniellula populicola (Thomas) Known from apterae only
Ceruraphis viburnicola (Gill) Known only from immature alatae
Auchenorrhyncha (Cicadellidae)"
Dalbulus maidis (Del and Wohl) Demonstrated in adults
Heteroptera (Miridae)b
~~~ ~ ~ ~~
Adelphocoris seticornis (F) In males and females

Poeciloscytus unifasciatus (F) In males and females
Miris dolabratus (L) In males and females
Stenodema calcaratum (Fall.) In males and females
Capsus ater (L) Demonstrated in female only
Lygus pratensis (L) Demonstrated in female only
Lygus hesperus KnightC In saliva discharged in plants,
but not in saliva discharged
outside plants
214 PETER W. MILES
Table 111-cont.
Heteroptera (Lygaeidae)'
Liocoris lineolaris (Beauv.) Demonstrated in adults
2. Absent
Aphididae:'
Aphis cardui L.
Ceruraphis eriophori (Wlk.)
Melaphis rhois (Fitch)
Myzus cerasi (F)
Prociphilus tessellata (Fitch)
Psyllidae:'
Unidentified spp.
Auchenorrhyncha:b
Various spp. in Fulguroidea (5), Cercopoidea (2) and Jassoidea (10).

Heteroptera:b
~
Various spp. in Lygaeidae ( l ) , Coreidae (2) and Pentatomidae (4)
a In saliva secreted into filter paper (Adams and McAllan, 1958).

In salivary glands (Laurema and Nuorteva, 1961).
(Strong, 1970).
than to function primarily in the digestion of a major nutrient

(Adams and McAllan, 1958; Strong, 1970).
Many workers have contented themselves with analysis of whole
gland homogenates or (from the larger Heteroptera) the secretion
expressed from the sac-like lobes of the principal gland. The main
generalizations that have emerged from such studies can be
summarized as follows:
(1) The saliva of phytophagous Hemiptera most often contains
amylase. Other carbohydrases are sometimes present, but Hori
( 1970c) states that Lygus disponsi Linnavouri secretes a salivary
amylase and no enzymes that hydrolyse oligosaccharides; all further
digestion of carbohydrates occurring in the midgut.
(2) Those insects that suck phloem sap as their principal food
are said not t o have hydrolytic enzymes other than carbohydrases in

their saliva, although among these enzymes may be counted the
pectin polygalacturonases secreted mainly by aphids and mirids
(Adams and McAllan, 1958; Laurema and Nuorteva, 1961).
(3) Those insects that feed on mesophyll tissues or seeds
however, are likely to have both proteinases and esterases (or lipase)
in their saliva (Nuorteva, 1958; Feir and Beck, 196 I ).
Other salivary enzymes have also been found. Kloft (1960)
showed that the mesophyll-feeder Pyrrhocoris upterus L. secreted
acid phosphatase and a phorphorylase among the other enzymes in
its saliva (whereas these enzymes were not secreted by sap-sucking
aphids). Miles (1968b) reported that the saliva of all the Hemiptera
excepting those that suck vertebrate blood secrete a salivary
polyphenol oxidase (PPO). The latter generalization is perhaps too
sweeping, however, for the Jopeicidae in the Cimicomorpha are
predatory bugs that apparently have no .detectable oxidase in the
glands (Davis and Usinger, 1970). In addition t o PPO, Miles and
Slowiak ( 1970) report that the insects also secrete peroxidase and
despite the possible confusion of the two enzymes (van Loon, 1971),
the discovery of insects that secrete the one without the other would
seem to corroborate the finding. The function of the oxidases is
discussed in the concluding section; so far no function for them has
been convincingly demonstrated.
The enzymic content of the saliva of any particular species cannot
be assumed t o be constant. There is considerable evidence for the
variation in content of proteinase especially. Nuorteva ( 1 956b)
found that in the mirid Miris dolubrutus L. salivary proteinases
occurred in the juveniles and in only female adults and Nuorteva and
Laurema ( 196 1b) found that the amount of proteinase in the salivary
glands of the pentatomid Dolycoris buccururn (L) increased when the
amount of protein in the diet increased. Similarly Hori (1970b)
found that not only did both amylase and proteinase content of the
salivary glands of the mirid Lygus disponsi vary with the
physiological state of the insect, but that the proteinase content was
variable even between the two glands of a single individual and that
there was no correlation between the amount of proteinase in the
glands and the less variable amount of amylase present. Similarly,
Adams and McAllan (1 958) found that whether detectable pectinase
occurred in the saliva of aphids depended on the species of plant on
which they were feeding, or whether they were apterous or alate;
sexual differences were also noted in the latter (Table 111).
216 PETER W. MILES
The saliva of Hemiptera is noted for its content of amino acids

and, as indicated in SectionVI1,A the presence of these may be
essential in those species that secrete a stylet-sheath. In the grape
phylloxera, Viteus vitifolii Fitch, Anders (1 96 1) and Schaller (1 960)
have shown that especially large quantities of amino acids are
secreted, no doubt because this insect is without an anus and must
excrete via the salivary glands. A distinctive feature of the saliva of
Viteus is that it contains an unusually high content of the basic
amino acids asparagine and glutamine, which presumably represent
the end points of nitrogenous excretion in the insect. In other species
of aphid, however, there are only trace quantities of the dibasic
amino acids, although aspartic acid and glutamic acid may be present
in significant amounts (Table IV).
Lately, the work of Miles (1967b) with radioisotopes has shown
that any soluble metabolite introduced into the haemolymph will
appear also in the watery saliva. Miles worked mainly with the
watery saliva discharged from the free tips of the mouthparts and
this presumably represented direct excretion of water from the
haemolymph along with traces of any metabolites present in it.
Nevertheless, analysis of the contents of the whole glands (Miles,
1967b, 1969a) suggests that some metabolites are selectively
sequestered from the haemolymph by the salivary glands. Thus a
large part of labelled cysteine injected into a pentatomid subse-
quently appeared in the salivary glands and secretions; Hagley (1 969)
noted a disproportionately large amount of phenylalanine in the
salivary glands of the cercopid Aeneolamia compared with the
composition of the haemolymph. It is therefore safe to conclude that
all the soluble metabolites that occur in the haemolymph, be they
salts, amino acids, sugars or the precursors of lipids (e.g. glycerol),
will occur in the salivary glands and will be secreted (or excreted) in
the very dilute secretion that comes mainly from the accessory gland
(see below); but some metabolites are specifically sequestered in the
principal glands.
Of particular interest in relation to phytopathogenicity is the
possible occurrence of the plant hormone p-indolyl acetic acid (IAA)
in the saliva. Duspiva (1954) and Miles (1968a) claimed to have
demonstrated the in vitro production of IAA from tryptophan by
homogenates of the salivary glands of an aphid and heteropteron
respectively. Nuorteva ( 1962) claimed evidence for the transfer of
IAA and gibberellic acid from diet to saliva of the auchenorrhychan
Calligyponu pellucidu. On the other hand, IAA is a common
endpoint of indole metabolism in animals, and the recent work of

Schaller (1 965, 1968a) has demonstrated conclusively that the saliva
of some aphids contains IAA: whether in sufficient quantity to
account for their phytopathogenicity will be discussed in the next
section.
A possible means of demonstrating the origin of a salivary
secretion is provided if the pH of the secretion can be determined.
Thus the pH of the sheath material is slightly on the acid side of
neutral (Saxena, 1963; Miles, 1965, 1968b); and the pH of the
watery saliva is alkaline, with pH values of up to 9 (Miles, 1965,
1968a). On the other hand, the contents of the principal salivary
gland never have as high a pH as this, and thus the more strongly
alkaline the watery saliva, the more it is likely to be the secretion of
the accessory gland (see Section X) and the less it comes from the
principal gland and thus contains the digestive enzymes and other
compounds secreted by that gland.
VIII. PHYTOPATHOGENICITY
Large numbers of some species of aphids or leafhoppers can

abound on plants and apart from some stunting, or contamination of
the foliage with honeydew, little effect on the growth pattern of the
plant can be observed. Yet individual mirids of some species produce
large lesions or such violent necrosis at the points where they feed
that the fruit will absciss prematurely or grow with characteristic
deformations (Carter, 1962). Although lacerate-and-flush feeding
necessarily results in necrosis, the lesions produced by cocoa capsids
on young stems may become surrounded by a zone of increased
growth, such that in time the lesion becomes occluded (Carter,
1962). Stylet-sheath feeding is usually accompanied by less
immediate damage, and is more likely to cause longer-term
disturbances in growth. Colonies of the woolly aphis, Erisoma
lunigerum (Hausm.) produce intumescences on the part of the stem
or root on which they feed. The grape phylloxera, Viteus vitifolii
Fitch causes similar swellings on roots; by depressing growth at the
point where it feeds and stimulating it further away, this insect
causes characteristic pocket galls on the vine leaves (Fig. 9).
Similarly, many (but not all) sedentary psyllids and coccids produce
galls. Among the scratch-and-suck feeders also, some tingids (and
Thysanoptera) cause pocket galls in which they live colonially.
Table IV
Analyses of aphid saliva for some metabolites
Viteus Eriosoma Aphis Sappaphis Myzus Hyalopterus Crypto- Aphis Myzus Megoura
vitifolii lanigerum pomi mali cerasi pruni myz.us smnbuci ascalo- viciae
rib is nicus
Amino acids
Serine ++ ++ + f
Alanine ++ + +++ f
Aspartic acid ++ + + f *3M
Glutamic acid + f +++ f %
Glycine + + -?
“Under-
asparagine”
+ i -
Leucine + f ?
Valine f f +
Asparagine +++
Glutamine ++
Arginine f
Lysine f
Histidine f
Cysteine/Cystine -
Tyrosine i
PAlanine -
Threonine i -
a-Aminobutyric - f
acid
Methionine - f
Phenolics
Naringenin + ? + ? f +
Phloridzin? + + + +
Quercitrin f ++
Quercetin - f +
Chlorogenic acid? - + f +
Rutin? - f + f
Hyperin? - + +
Robinetin- - f
aglycone? 4
Protocatechuic
acid?
- ? ? E
Ferrulic acid? - - ? Bt:
pCumaric acid? - f ? <
Indole acetic
acid
* * + + -
Proteinase + ? - ? - - - - - - E
s
M
Results for some unidentified amino acids and phenolics not included: Number of ++ indicates strength of reaction, * indicates trace p
only, and ? an uncertain result. Results for Viteus vitifolii represent the pooled results for seven biotypes of the species. (From Schiiller,
>
1968a).
220 PETER W. MILES
a
a. Dreyfusia spp. b. Eriosma lanigerum c. Cocoa capsids
Increase in cell protein Simple surface gall. Cause occluded necrosis on
but not cell growth young shoots by stimulating
a
(from Kloft, 1960). peripheral growth.
d. Wteus vitifolii
At root tip of vine causes swelling
surrounding feeding puncture
(from Anders,1961).
e. Viteus vitifoii
on foliage causes occluded
gall and with daughters
o calonial gall forms
(adapted from AndersJ961).
Fig. 9. Formation of galls: a: “physiological gall”. b: surface gall; c: occluded necrosis;

d: root gall; e: pocket gall on leaf.
Such localized effects of feeding must be differentiated from

systemic stunting or deformation that are caused by viruses or by
mycoplasmas (Raine and Forbes, 1969; Whitcomb and Davis, 1970).
Localized effects, whether or not they take the form of necrotic
lesions or galls, can usually be shown to be independent of any
disease organism and to be due to the toxic effects of the saliva
discharged by the insects into the plants during feeding.
The identity of the salivary toxins responsible has elicited much
interest. In recent work on the causal agents of galls, a major
controversy has been whether phytopathogenicity resides in free
amino acids present in the saliva of plant bugs (Anders, 1961 ; Kloft,
1960) or in the IAA that is either secreted in the saliva (Schaller,
1968a) or may be formed from tryptophan by oxidative deamination
brought about by salivary oxidases (Miles, 1968a, b). Recently an
explanation of the formation of lesions by mirids has been advanced
as a separate hypothesis; namely that pectin polygalacturonase in the
saliva causes a rapid spread of other salivary enzymes into the tissues
of plants during the lacerate-and-flush type of feeding of these
insects (Strong, 1970).
Kloft (1 960) showed that the amino acids secreted by aphids in
their saliva caused increases in the permeability of plant cells and
THE SALIVA O F HEMIPTERA 22 1
probably thereby increased respiration, transpiration and proto-

plasmic streaming. Insects that suck phloem sap release their saliva
only while penetrating to the phloem or at the moment of
withdrawal of the stylets and the pathological effects of an insect
such as the onion aphid, Myzus ascalonicus Donc. are thus not
pronounced. In contrast, the Dreyfusi spp. (Adelgidae) that multiply
on silver fir, feed on the parenchyma and secrete saliva continually;
the net result of their feeding is similarly progressive, resulting in the
accumulation of proteins in the bark just under the points of feeding
of the insects. Such an accumulation of nutrient materials without
any obvious hypertrophy of the plant tissues Kloft called a
“physiological gall” and ascribed it principally to a stimulation of
protein synthesis brought about by the amino acids discharged by
the insect in its saliva.
Anders in a series of papers ( 1960a, by 196 1) described his analysis
of the saliva of larvae of phylloxera that were producing galls on
vines. As has been discussed in Section VI1,B the unusually high
concentrations of amino acids that this species has in its saliva have
been considered excretory in nature. Anders claimed t o have
identified three amino acids in particularly high concentrations
namely lysine, histidine and tryptophan, with significant quantities
also of glutamic acid and valine. When germinated in solutions of
these amino acids (but not others), the roots of grape seedlings
produced subapical swellings that Anders compared to the subapical
galls produced by phylloxera feeding just behind the root cap
(Fig. 9d).
On the other hand, similar results have been described when vine
roots are grown in potassium phosphate solution (Miles, 1968a) and
perhaps solutions of other compounds that affect the permeability of
the cells in the meristematic subapical region of the rootlet would
cause similar growth disturbances.
Careful analysis of the saliva of phylloxera and several other
species of aphids with varying degrees of phytopathogenicity led
Schaller ( 1 968a) to conclude that in fact the amino acids named by
Anders were not typical of the saliva of phylloxera, in which he
found the principal amino acids to be glutamine, serine, alanine and
aspartic acid. The saliva analysed by Schaller was collected from
dampened filter paper and there is thus the problem of whether the
saliva discharged in what were presumably exploratory probes was of
the normal strength and composition secreted by the insects when
they feed on plants.
222 PETER W. MILES
Nevertheless, that amino acids were found at all gives a good

indication of those that feature most prominently in the salivary
secretions of the various species. Schaller also found IAA and several
phenolic compounds in the saliva of aphids. The average quantities of
compounds collected from an individual aphid during the 6 to 8 h
when it was permitted to probe the filter paper were up to a
maximum of 2 x 10-Fg each of the major amino acids present in the
saliva. Eriosomu Zunigerum secreted a similar quantity of IAA in its
saliva and somewhat less IAA was retrieved from the saliva of Viteus
vitifolii and of Myzus cerusi (Table IV).
Schaller concluded that although the analysis of the saliva of
aphids showed each to have a specific composition qualitatively and
quantitatively, certain generalizations emerged. The greater the
ability to cause hypertropy of tissues in their host plants, the
greater the overall concentration of amino acids, the greater the
concentration of IAA and the lower the concentration of phenolics.
He concluded that IAA must work together with free amino acids to
produce galls while the phenolic compounds, by producing quinones
that reacted with amino acids and destroyed IAA, reduced the
likelihood of gall formation.
In a series of brilliant experiments, Schaller (1968b) tested his
conclusions by introducing solutions that simulated the saliva of
aphids into the petioles of developing vine leaves. To do this he filled
hollow glass microneedles with the solution and allowed the needles
to remain permanently in place while the leaf grew (Fig. 10). He
found he could imitate the galls of phylloxera with remarkable
felicity and the nearer the solution approached the actual
composition of phylloxera saliva with respect to amino acids and
IAA, the more “perfect” the gall produced.
Strong ( 1970), meanwhile, has investigated the destructive lesions
produced by Lygus hesperus Knight. He concluded that the saliva
contained no IAA and lacked any physiological system by which
IAA could be synthesized by the saliva released within plants. He
ascribed the large lesions produced by individual bugs to the salivary
pectin polygalacturonase which, by greatly increasing the effective
spread of the digestive enzymes in the saliva during the lacerate-and-
flush feeding practised by this and other mirids, caused a much larger
lesion than would be produced by a sap-sucking insect of comparable
size. Presumably the effects of the feeding of the mirids that attack
cocoa must involve more than the destructive processes in the
feeding of Lygus, since Strong’s explanation does not dispose of the
Fig. 10. Formation of “histoid” gall on petiole of vine leaf by a mixture of amino acids
and IAA simulating the saliva of the grape phylloxera, V . vitifolii. (After Schiller, 1968b).
observation that hypertrophy of cells can occur at the edge of the

lesions produced by the “cocoa capsids” (Carter, 1962). In fact,
Scott (1 970) showed that the feeding both of L. hesperus and of L.
elisus Van Duzee on either carrot seeds or beans, while depressing
initial growth of the seedlings after germination, actually increased
their eventual growth compared with plants grown from seeds on
which the insects had not fed.
A third approach to the phytotoxicity of the saliva of Hemiptera
is the proposal that the salivary phenols and phenolases of Hemiptera
directly interfere with the growth-controlling mechanisms of
meristematic cells. As Gordon and Paleg (1 96 1) demonstrated in
vitro, quinones produced by a system such as dihydroxy phenyl-
alanine (DOPA) plus polyphenol oxidase (PPO) will transform
tryptophan by oxidative deamination to IAA. On this basis, Miles
(1969b) proposed that an increase in IAA content of cells
surrounding the feeding punctures of Hemiptera would be likely. The
PPO would seem to be provided in the saliva of all the phytophagous
forms; phenylalanine is transformed in the salivary glands to DOPA
and the tryptophan, although present in small amounts only, would
224 PETER W. MILES
nevertheless occur in the haemolymph and therefore saliva as the free

metabolite. Miles thus considered all phytophagous Hemiptera as
possessing the potential for forming galls on their food plants and he
considered they would do so provided the precursors of the
IAA-producing reaction were present in sufficient concentration and
the insect injected enough of its saliva in a place where the plant’s
cells were still sufficiently meristematic. As a demonstration of this
hypothesis, he made a non-cecidogenic lygaeid temporarily produce
galls on cotyledons of a sunflower seedling by implanting into the
bug flakes of agar containing phenylalanine and tryptophan (Miles,
1968a). Scott (1970) similarly suggested that the potential of the
saliva to form IAA was a likely explanation for the enhanced growth
of plants grown from seeds that had been attacked by Lygus spp.
A number of problems arise from the hypothesis that salivary
phenols and phenolases cause increases in IAA concentrations in the
tissues of plants. Phenolases have also been implicated in the
breakdown of IAA (Pilet et al., 1970); Schaller (1 968a) correlated an
increase in salivary phenolics with decreases in both IAA-content and
phytopathogenicity of the saliva. Moreover, as Schaller ( 1968b) has
pointed out, the total amounts of known metabolites injected by the
insects into plant tissues are small compared with the amounts
already present within the tissues themselves. Indeed the amino acids
in the saliva of a sap-sucking aphid represent merely a small
proportion of the amino acids obtained by the insect from the
plant’s own phloem sieve tubes and the galls induced by phylloxera
are much richer in IAA than the saliva injected into them by the
insects.
The question thus arises whether the observations so far made on
possible gall-inducing substances have in fact been observations of
secondary effects: the amino acids and IAA in the saliva of
cecidogenic species being derived from the metabolites already
present in rich supply in the galls, rather than the galls being due to
the substances introduced in the saliva of the aphids. Nuorteva’s
(1962) work on the transfer of dietary amino acids t o the saliva of
Calligypona and the evidence that even enzymes are readily
transported unaltered from haemolymph to the saliva of plant bugs
(Miles and Slowiak, 1970) would add weight to such an interpreta-
tion.
Schaller’s successful demonstration that the injection of amino
acids and IAA does cause galls must tip the balance in favour of the
explanation that cecidogenesis indeed lies in the presence of these
compounds in the saliva of the insects, even though the apparent

anomaly that they are already present in higher quantities in the
plant remains.
A definitive explanation of cecidogenesis is likely to be concerned
with the precise location and movement of physiologically active
substances, rather than overall concentrations. A sap-sucking insect
in effect removes amino acids from sieve tubes and subsequently
reinjects them elsewhere in the plant. The hypertrophy that occurs at
the edges of the lesions of cocoa-capsids must be due either to a
gradient in concentration of substances that cause necrosis at higher
concentration and increased growth at lower or to differential rates
of diffusion of necrosis-causing metabolites and growth-promoting
ones. And it is possible to reconcile the in vitro production of IAA
by a phenol-phenolase system, with demonstrations that the same
system causes the destruction of IAA, by assuming that the end
point of the reaction is dependent on a precise relation between the
concentrations of the reactants.
IX. SALIVARY GLANDS AND DUCTS
The salivary glands of Hemiptera are labial glands, lying mainly in

the anterior region of the thorax, alongside and partly above the gut.
Typically, there is on each side a principal gland and an accessory
gland. The duct of the accessory gland unites with the duct of the
principal gland near where the latter duct leaves the principal gland
(Fig. 1 l), and the principal ducts unite to form a common salivary
duct that discharges into the salivary pump. From the pump there is
a short meatus leading to the salivary canal, the posterior of the
canals formed by the opposition of the maxillae (Fig. 8).
There is usually a high degree of uniformity of structure in the
glands of members of the same family and a degree of likeness is also
apparent within higher taxa. At the same time, considerable
differences exist between the glands of such taxa as the Sternor-
rhyncha and Auchenorrhyncha in the Homoptera and between the
superfamilies of the Auchenorrhyncha. In contrast, the glands of all
the Heteroptera show a remarkable similarity of anatomical pattern,
seemingly derived from the relatively simple pattern within the
Coleorrhyncha, a small unspecialized group once regarded as
heteropteran, but now usually placed in a separate division of the
Homoptera.
226 PETER W. MILES
Fig. 1 1. Salivary glands of Hemiodoecus veitchi Hawker (Co1eorrhyncha:Peloridiidae).

(From Prendergast, 1962). A nerve (not shown) also innervates the principal gland.
A. APHIDOIDEA
The salivary glands, although apparently simple, have been shown

by Weidemann (1968, 1970) to be composed of a number of
different kinds of cells (Fig. 12) that show very different cycles of
activity and produce visibly different kinds of secretion (Moericke
and Wohlfarth-Bottermann, 1960a). At least nine histological types
of cell occur in the principal gland apart from the canal cells.
Weidemann arranged them into four functional groups, at least three
of which produce components of the saliva. Using the electron
microscope, Moericke and Wohlfarth-Bottermann ( 1960b) have
shown that the secretory products accumulate in vesicles that are
extruded from the cell border, and the membrane surrounding the
vesicle then breaks down.
The principal salivary glands of Aphididae exhibit a partial
bilateral division into two symmetrical halves. Down each half runs a
stout walled central canal, formed intracellularly by the “canal cells”
through which it runs. In the principal glands there is a region of at
least seven kinds of “Main Cells”, and at its proximal end, the region
of main cells fits into a region of “Cover Cells” rather as an acorn fits
into its cup. Both main and cover cells are secretory and small
canalulae ramify among the cover cells from the central canals.
gland
Fig. 12. Salivary glands ofMyzus persicae. a: principal gland; left side showing cell types
and numbers (on each side), right side showing nuclei; canal cells and their nuclei not
shown; cross-hatching indicates histochemical grouping: A and F are rich in cysteine; B, C,
and I in hyaluronic acid; D and E in carbohydrate. (After Weidemann; 1968, 1970). b:
principal and accessory gland showing ducts. c: schematic diagram of the structure of the
salivary ducts, showing the canal wall surrounded by intercellular spaces and the
interdigitating processes of the canal cells which form the corona sinuosa (Faltenkranz).
(Redrawn from Moericke and Wohlfarth-Bottermann, 1960b).
228 PETER W. MILES
According to Moericke and Wohlfarth-Bottermann ( 1 960b) the cells

of the principal gland discharge vesicles containing their secretory
products into the intercellular spaces that surround and indent the
canal cells.
The surface area of the cells of the central canal is increased by
numerous radiating folds, forming the corona sinuosa (Moericke and
Wohlfarth-Bottermann, 1 960b) and this is particularly well
developed in the region of the cover cells. The secretion of the main
cells appears to be relatively electron transparent, while in the region
of the cover cells the contents of the canal become electron dense. It
is not certain, however, whether this can be ascribed solely to the
secretory products of the cover cells or to changes occurring to the
products within the canal, possibly mediated by activity of the canal
cells themselves.
The accessory gland of Aphids is usually a small structure with a
few cells producing a very electron transparent secretion. Its canal is
continuous with numerous intracellular canalulae that ramify into
the secretory cells-an arrangement consistent with the rapid
discharge of a dilute secretion. In the phylloxera, Viteus vitifolii, as
Rilling (1 966) has shown, the accessory gland is enormously
increased in size and is much larger than the principal gland (Fig. 13).
The cells of the accessory gland form a syncytium and appear to be
greatly enlarged canal cells. Surrounding the intracellular accessory
canal is a system of radial, laminar vacuoles and surrounding these
again vesicular vacuoles that occupy most of the bulk of the cells.
Rilling relates this development of the accessory gland to the
gall-forming propensities of the insects, but it is more probable that
the hypertrophy of the accessory gland is related primarily to its
assumption of the main excretory role in the insects, which not only
lack Malpighian tubes, in common with the other Aphidoidea, but
also have no anus and must therefore excrete, if at all, through their
salivary glands.
Viteus show other interesting phenomena. The partial division of
the principal glands of aphids into bilaterally symmetrical halves has
apparently become complete in Viteus for the principal gland is now
completely bilobed, although each lobe has a histologically similar
structure. Each is composed of four “giant cells” and two
“eosinophilous cells”, and a further group of cells that Rilling
homologizes with cover cells, although they are arranged centrally in
a “hilus”. The giant cells, the eosinophilous cells, and the cover cells
all show secretory activity. In addition there are the presumably
Fig. 13. Salivary glands of Viteus vitifolii (Phylloxeridae), semidiagrammatic. a: bilobed

principal gland and multilobular (semisyncytial) accessory gland. b: one lobe of the
principal gland, showing the four “giant” cells, the branched, double nuclei and the hilus
cells. c: cross section through one lobe of the principal gland, principal duct and part of the
accessory gland. I to 1V-giant cells; e-one of the two eosinophilous cells; hilus cells in c
cross hatched. (Adapted from Rilling, 1966).
non-secreting canal cells. The secretory cells are typically binucleate,

and the nuclei of the giant cells are greatly enlarged and branched
structures.
€3. JASSOMORPHA
In the superfamilies Jassoidea and Cercopoidea, the various kinds

of secretory cells of the principal salivary glands are grouped
230 PETER W. MILES
separately into distinct lobes or regions, while the accessory gland

takes on a more or less elongated, vesicular appearance. In Empoasca
fabae (Hausm.), the four separate lobes of the principal gland remain
a solid mass of cells (Fig. 14a), although between the cells at the
centre of the lobe there is an intercellular space, sometimes
extending as indentations (“intracellular canniculae”) into the
Fig. 14. Salivary glands of Jassoidea, semidiagrammatic. a: Empoasca fabae (Harris)

(Typhlocybidae). (After Berlin and Hibbs, 1963). b: Erythroneura limbatu Matsumura
(Cicadellidae). (After Sogawa, 1965). c: Nephotetrix cincticeps Uhler (Deltocephalidae).
(After Sogawa, 1965).
secretory cells (Fig. 15). This space communicates at the origin of

the lobe with a chitin-lined duct. The accessory gland is typically
elongated with at least one portion having a distinct lumen and
looking similar in structure to a Malpighian tube. The glandular cells
of the salivary apparatus are typically binucleate and the nuclei of
the large secretory cells may be ramified (Berlin and Hibbs, 1963).
In other Jassoidea, the cells in each lobe tend to remain separated
Fig. 15. Lumen of glands. a: Xenophyes cuscus Bergroth (Coleorrhyncha), with

canniculae only. (After Prendergast, 1962). b: Empwscu f a h e (Harris) (Jassoidea), with
confluent intracellular vesicles. (After Berlin and Hibbs, 1963). c: Notonectu glaucu L.
(Hydrocorisae), with true but poorly developed lumen approximating the condition in
Empouscu. (After Baptist, 1941).
from one another (Fig. 14b) and in the principal glands of some
families, Sogawa (1965) described up to seven kinds of secretory
cells, arranged not into distinct lobes, but as rosettes of cells
(Fig. 14c). He nevertheless distinguished two groups of these cells:
the principal salivary duct branches just as it enters the gland into
two “ducteoles”; about the end of the one (“posterior”) branch,
four kinds of cells form a concentric rosette, while two other kinds
of cells are arranged in radial layers along the “anterior” branch. The
anterior ducteole remains short in some species, but becomes more
elongate in others and may end in a terminal appendage formed from
a cluster of small cells of yet another type.
The accessory gland of the Jassoidea is typically elongated and
may be differentiated into a tubular distal (“tail”) region and a more
232 PETER W. MILES
bulbous proximal (“head” or “cephalic”) region in which the lumen

becomes less evident. Sogawa believes the bulbous region t o be
secretory or resorptive, possibly increasing the analogy between the
accessory gland and an excretory organ.
Very little information is available about the glands of the
Cercopoidea. Nuorteva ( 1956a) provided illustrations of some glands
(Fig. 16), indicating that there occur in them compact groups of cells
Fig. 16. Salivary glands of Cercopidae. a: Aphrophora alni (Fall.) b: Philaenus spumarius
(L.) (After Nuorteva, 1956a).
corresponding to Sogawa’s “anterior” lobe, and a “crown” of

sometimes tubular acini corresponding to the rosettes of the
posterior lobe of some Jassoidea.
C . FULGUROMORPHA
The principal gland in the Delphacidae is composed of a large

number of multicellular acini, each with its separate ducteole
(Fig. 17). It differs from the gland of Empoasca (Fig. 14) chiefly in
the larger number of acini and in the absence of a tubular accessory
gland. Sogawa (1 965) describes nine kinds of acini, one of which he
designates an accessory gland, although it is reniform and not always
well separated from the other acini. Balasubramanian and Davies
(1968) also distinguish nine commonly occurring acini in the family
Delphacidae and a tenth type occurring in some species. Miles
( 1 964a) similarly described ten lobes in the glands of a flatid. Neither
Balasubramanian and Davies nor Miles distinguished an accessory
gland. Sogawa lists the numbers of cells in each type of acinus as
I
d
loop
Fig. 17. Salivary gland of Laodelphax striatellus (Fu1guromorpha:Delphacidae). a to

h-distinguishable acini of the principal gland; Ag-accessory gland. (After Sogawa, 1965).
varying between two and eight, while Balasubramanian and Davis list
two kinds of acinus as unicellular. The latter authors point out that
all cells are binucleate; a feature they appear to share with the
Jassomorpha. The ducts in the Fulguromorpha are similar to those of
the Cicadellidae in the Jassomorpha: intracellular spaces in the cells
of the acini finally join up with ducteoles that have their own
characteristic small cells with compact ovoid nuclei. The ducteoles
join up with one another and eventually a common salivary duct is
formed on each side of the body; these join to form a very short
median duct just before this enters the salivary syringe.
D.OTHERAUCHENORRHYNCHA
Very little work has been done on the other groups within the
Homoptera. The Cicadomorpha are described by Nuorteva ( 1956a)
as having bilobed principal glands and a tubular accessory gland, but
this account was based on early studies and, as Balasubramanian and
Davies (1 968) point out, many past generalizations may need careful
revision as more information on the comparative morphology of the
salivary glands of Homoptera begins to accumulate.
The salivary glands of the small family Peloridiidae, now placed in
the taxon Coleorrhyncha separate from the other Hornoptera, are of
especial interest. These glands bear a superficial resemblance to the
glands of many of the relatively unspeciaIized, carnivorous
234 THE SALIVA OF HEMIPTERA
Heteroptera. Balasubramanian and Davies object that this similarity

is more apparent than real, quoting as the major difference between
the glands of the heteroptera and Homoptera the presence or absence
of a lumen. The glands of the Peloridiidae have no distinct lumen and
therefore are typically Homopteran , according to these authors. But
the distinction is not necessarily valid, for the salivary glands of
many of the Heteroptera Cryptocerata, as Baptist (1941) has shown,
have no more lumen than those of the Cicadellidae (Fig. 15).
E. HETEROPTERA
Most of the Heteroptera have principal salivary glands that are

clearly differentiated into an anterior and a posterior lobe, each of
which has a distinct lumen. In most, also, the accessory gland is
vesicular. In the Cimicomorpha the accessory gland is a thin-walled
bladder, whereas in the Pentatomorpha, the terminal vesicle is
completely lost, but the cells at the distal end of the elongated
accessory duct take on a swollen, glandular appearance. The nerve
supply in the lygaeid Oncopeltus (Bronskill et al., 1958; Miles, 1960b)
is two-fold, one nerve supplying the anterior lobe and the other,
which travels alongside the principal salivary duct, supplying the
posterior lobe and accessory gland and duct (Fig. 18).
Although Baptist ( 1 941) illustrated only a single nerve supplying
the gland of any one species of heteropteran, that nerve might
variously appear to be the homologue of either of those described in
Oncopeltus. It is therefore possible that the double nerve supply is
typical throughout. According to Miles, this arrangement provides
for the discharges either of the anterior and related lobes of the
principal gland or of the posterior lobe and accessory gland, thus
accounting for the independent discharge of the two kinds of saliva
secreted by the Pentatomorpha.
In the Cimicomorpha, blood-sucking forms tend to lose the
division between the anterior and posterior lobes of the principal
gland (Rhodnius) or lose the anterior lobe entirely as in Cimex.
Whereas, in the Pentatomorpha, only the Pentatomidae retain the
simple bilobed condition; in all other families, the glands are
multilobed. Baptist (1941) claimed that such proliferation of lobes
was due to subdivisions of the posterior lobe, but studies of
innervation and of physico-chemical composition of the secretions
could indicate that, on the contrary, the subdivisions are of the
PETER W. MILES 235
Fig. 18. Salivary glands of Heteroptera. a: a predator, Notonecta glauca L.

(Hydrocorisae) b: a blood-sucker, Rhodnius prolixus Stal (Reduviidae). c: a blood-sucker,
Cimex lectularius L. (Cimicidae). d: a phytophagous lacerateand-flush feeder, Lygus
pratensis L. (Miridae). e: a stylet-sheath feeder, Pentatoma rufipes L. (Pentatomidae). f a
stylet-sheath feeder, Oncopeltus fusciatus (Dall.) (Lygaeidae). Ag-accessory gland;
anterior-anterior lobe; lateral-lateral lobe; n, ,na -nerves; posterior-posterior lobe. (a to e
from Baptist, 1941; f from Miles, 1960b). All drawings approximately to scale.
anterior lobe and are concerned with the secretion of sheath material
(Miles, 1967a). If, as Goodchild (1 966) has suggested, all Heteroptera
are to be derived from phytophagous Hemiptera through omnivorous
forms in which the number of lobes was reduced or primitively small
as in the aquatic Heteroptera, then the return to a phytophagous
condition in the Pentatomorpha has apparently required a more
complex division of labour in the salivary secretions and a convergent
elaboration of the salivary glands in the Homoptera on the one hand
and Heteroptera : Pentatomorpha on the other.
236 THE SALIVA OF HEMIPTERA
X. ORIGINS OF THE SALIVA

Tracing the origins of the salivary components within the salivary
glands is easiest in the Heteroptera because the great majority have
glands that are morphologically simple and each lobe of the gland has
its own lumen in which the secretory products of the lobe collect.
Little is known of the contents of the salivary glands of Heteroptera
other than the Geocorisae, however. Work has been done mainly on
the glands of Pentatomorpha; but amongst these, only the
Pentatomidae retain a simple two-lobed principal gland and in the
other families the problem of identifying the origins of any specific
salivary secretion has proved more difficult because of secondary
multiplication of the lobes.
A. FUNCTION OF THE ACCESSORY GLAND

As a result of the work of Goodchild (1966) it can be accepted
that, throughout the Hemiptera, the function of the accessory gland
is the production of the copious flows of very dilute secretion that
the insects employ when they “taste” surfaces with which the stylets
come into contact, as a means of flushing out food sources or as a
means of excreting excess water. In all Hemiptera, with only the
possible exception of the Fulguromorpha, that part of the salivary
apparatus identifiable as the accessory gland is either vesicular or
tubular. When the accessory gland is a compact organ, it often has
greatly enlarged intracellular vesicles or extensive canniculae; i.e.
ways of increasing the surface area of the functional ducts. In the
Fulguromorpha, Sogawa ( 1965) identified the lobe in which the duct
had a distinctive “corona sinuosa” as the accessory gland.
Where it has been specifically identified, the secretion of the
accessory gland is alkaline (Miles, 1968b) and presumably the
accessory gland thus functions as the first stage of a typical diuretic
organ, producing a dilute ultrafiltrate of the circulatory fluid by the
active secretion of cations. In a complete excretory organ, there
would follow a part that served to resorb useful metabolites such as
amino acids and sugars, while exchanging the cations for hydroxo-
nium ions, thus “acidifying” the original secretion. Clearly, however,
in the Heteroptera at least, such a resorptive region of the accessory
gland does not occur (or is at best only partially effective).
PETER W . MILES 237
B. FUNCTIONS OF THE PRINCIPAL GLAND
In the two-lobed gland of pentatomids, the contents of the

anterior lobe rapidly gel on exposure to gaseous or dissolved air or to
hypotonic liquids, whereas the contents of the posterior lobe do not.
The anterior lobe has thus been identified as the origin of the sheath
material. The contents of the anterior lobe gel particularly rapidly in
water, in which the free amino acids that are presumed to keep the
solution of sheath precursors (Section VI1,A) stable, can rapidly
diffuse from the secretion (Miles, 1964b); whereas under paraffin oil,
the contents remain fluid. Nevertheless, paraffin oil readily dissolves
oxygen and a skin of solidified material forms at the interface of the
secretion and the oil.
The cells of the anterior lobe in pentatomids do not show uniform
chemical activity, however. The cells that contribute most of the
sulphydryl groups of the sheath precursors are located at the anterior
end of the lobe. In lygaeids, both anterior and lateral lobe of the
three-lobed principal gland produce sheath precursors, but the
secretion of the lateral lobe contains less sulphydryl groups than does
that of the anterior lobe. Thus Miles (1 967a) concluded that the two
lobes (anterior and lateral) of lygaeids represent a secondarily bifid
anterior lobe (of pentatomids) with a division of function between
the two; the lateral lobe providing a protein that readily forms
hydrogen bonds and that provides the bulk of the protein (or
lipoprotein) of the sheath, while the anterior lobe provides the
sulphydryl groups that give the sheath chemical stability and initiate
particularly rapid gelling in oxidizing conditions.
In the Pyrrhocoridae, the principal gland is four-lobed and the
contents of all the lobes except the posterior can form irreversible
gels; thus Miles (1960b, 1967a) considered that in the Pentatomorpha
as a whole, any more than two distinct lobes (not counting
digitations) in the principal gland represented subdivisions of the
anterior lobe. This point of view is at variance with that of Baptist
(1941) who believed any subdivision to belong morphologically to
the posterior lobe. But so little is known of the functions of the
various lobes in the multilobed glands of some families of
Pentatomorpha, that any conclusion must be considered conjectural
at the present time.
The posterior lobe of the salivary glands of Heter0ptera:Pentato-
morpha secretes salivary enzymes. Miles (1 967a, 1968b) stated that
the digestive enzymes occur only in the posterior lobe of the lygaeid
238 PETER W. MILES
Oncopeltus, but other authors claim the occurrence of such enzymes

in other lobes of the salivary glands of Heteroptera (Baptist, 1941;
Bronskill et al., 1958; Salkeld, 1960). In Heteroptera that secrete no
sheath, the division of function between anterior and posterior lobes
is almost unknown. Edwards (1961) found that in the carnivorous
bug Plutymerus, extracts of both anterior and posterior lobes were
proteolytic and zootoxic, whereas the contents of the accessory
gland were neither. Hori (1968b) stated that the main source of
salivary amylase in the mirid Lygus disponsi was the posterior lobe
and that only traces of activity occurred in the anterior lobe and
accessory gland; but it has also been pointed out (Miles, 1960b) that
very careful separation of the lobes and removal of contaminants
from the haemolymph is necessary to pinpoint the origin especially
of amylase in view of its rapid activity and the sensitivity of tests for
it.
In the blood-sucking bugs, the distinction between the lobes in the
principal gland tends to disappear and Cimex lacks an anterior lobe
entirely. This secondary reduction of structure is presumably
ascribable to a reduction in the number of functions performed by
the saliva and comparative investigation of salivary function in the
Cimicomorpha, phytophagous, predatory and blood-sucking, should
be most rewarding, especially in the light of the discovery by Friend
and Smith (197 1) of the secretion of traces of a sheath-like material
by Rhodnius.
C. SOURCES OF OXIDASES
In most Hemiptera, some part of the salivary glands secrete

polyphenol oxidase (Miles, 1965) and perhaps peroxidase as well
(Miles and Slowiak, 1970). In the Homoptera it is cells of the
principal glands and in Heteroptera it is the cells of the accessory
gland or its ducts and often those of the principal salivary duct also
that secrete polyphenol oxidase. Within the phytophagous
Hemiptera, these secretions could be expected to aid the oxidative
process accompanying sheath formation; but experiments in which
the oxidase of the accessory gland was effectively isolated from the
feeding mechanism failed to prevent the normal formation of a stylet
sheath within plant tissues (Miles, 1967a). At the same time,
carnivorous bugs which are presumed to secrete no stylet-sheath also
secrete a polyphenol oxidase in the accessory glands or ducts (Miles,
1964a).
It is noteworthy that the cells reacting with DOPA in the

Heteroptera are those surrounding the ducts, all of which have a
chitinous intima: the oxidase could thus be part of the normal
cuticle-producing mechanism of epidermal cells, except in those
insects in which there is definite evidence of secretion of the enzyme
in the saliva itself. Locke ( 1969) has recently shown that peroxidase
too is involved in the oxidative processes carried out by the
epidermal cells when they produce cuticle, and peroxidase is the
latest enzyme to join the list of those secreted in the saliva of
Hemiptera (Miles and Slowiak, 1970).
One puzzling feature of the secretion of salivary oxidases by
Hemiptera is that the enzymes are secreted in high concentration
along with the sheath of aphids (Miles, 1965) and Pentatomorpha,
and they can be found in high concentration in secretions remaining
within the lumen of the sheath (Miles, 1967a); yet in the
Pentatomorpha these enzymes are secreted by the accessory gland
and this produces so dilute a secretion that .it is often impossible to
detect any solutes in it. Possibly it is always secreted by the cells of
some parts of the accessory gland or duct (Miles, 1964a) and is
subject to varying degrees of dilution by water discharged by other
parts.
D. SOURCES IN THE HOMOPTERA
In the Homoptera, discovery of the origin of salivary components

is considerably more difficult than in the Heteroptera, and recourse
has mainly been had to histochemistry. It is not always easy to
differentiate between the secretory products and the synthetic
processes that give rise to them, however, and although prosecretory
granules are separately identifiable by electron microscopy in the
cells of the salivary glands of Homoptera (Moericke and Wohlfarth-
Bottermann, 1960a) the composition of the secretion cannot be
determined by this means.
Comparison between the work of different authors on the
histochemistry of the salivary glands of Homoptera is also
complicated by their use of different dyes and reagents. Another
difficulty, pointed out by Weidemann (1970) is that in Myzus
persicae the cells do not react consistently with reagents-a likely
result in view of the cycles of activity which the cells undergo
(Moericke and Wohlfarth-Bottermann, 1960a).
Miles (1964a) published a comparison of the cells that produce
240 PETER W. MILES
PPO in the salivary glands of Homoptera; Sogawa ( 1 965, 1967) made

a histochemical comparison of the glands of delphacids (Fulguro-
morpha) and deltophacids (Jassomorpha) and Weidemann (1 970)
made a histochemical study of the glands of the aphid Myzus
persicae. Since the sheath material secreted by Hornoptera, like that
secreted by Heteroptera, most probably contains sulphydryl groups
(Miles, 1965), attempts have been made to trace the origins of the
sheath material by looking for a major source of the sulphydryl
compounds, for example cysteine/cystine in the glands. Results have
tended to depend very much on the particular reagent chosen,
however. Perhaps the most specific test for sulphydryl groups is the
nitroprusside reaction, but it is insensitive and unsuitable for small
sections; a highly sensitive method, said to be specific, is with DDD
(dihydroxy dinaphthyldisulphide), but this test gave no clearly
positive results with the salivary glands of leaf hoppers (Sogawa,
1967). Other methods, found more likely to react positively, were of
less certain chemical protocol-e.g. the alkaline tetrazolium reaction
(Sogawa, 1967) and performic acid-alcian blue (Weidemann, 1970).
Finally, quite apart from the occurrence nt sulphydryl groups in the
sheath, any other secretion with which the sheath precursors are
likely to come into contact within the conducting system of the
glands are also likely to contain reducing groups (Miles, 1967a).
Other properties of sheath material that may be of use in
identifying its origins in the glands of Homoptera are its content of
phospholipid and its periodic acid-Schiff (PAS) reaction. Using tests
for lipids and the PAS-reaction, Sogawa homologized some lobes of
the salivary glands of the jassomorph N. cincticeps and the
fulguromorph L. striatellus (Figs 14, 17). These cells gave somewhat
different combinations of reactions, but Sogawa concluded that two
or three sets of cells were responsible for the secretion of the sheath
precursors out of the six kinds of cells in the principal glands of N.
cincticeps and out of eight kinds in the glands of L. striatellus. The
strongest homologies according to Sogawa are between the IV cells
of N. cinticeps and the A cells of L. striatellus (main secretion of
protein); the I11 cells and the H and G cells (main secretion of lipids)
and the V cells and the Ag cells (secretion of conjugated
carbohydrate).
E. SALIVARY CARBOHYDRATE AND LIPID
One histochemical peculiarity of sheath material and of some cells

in the salivary glands may be of use in future studies of its glandular
origins. The PAS-reaction is usually given by carbohydrates, but also

by some lipids: these sources can be differentiated by either treating
with an acetylating agent, which blocks the groups in carbohydrates
that are PAS-positive or by extraction with solvents that remove the
source of the reaction when it is due to lipids. One or both of these
pre-treatments should prevent the PAS-reaction, thus indicating the
identity of the PAS-positive source. Sheath material (Miles, 1960a)
and certain cells of the Homoptera (Sogawa, 1967) and Heteroptera
(Miles, 1960b) remain PAS-positive despite prior blocking of
carbohydrates or extraction of lipids. Sogawa (1 967) suggested this
was due to the presence of both sources of reactivity in a conjugated
form. His hypothesis received some support from experiments with
injected radioactive glucose and glycerol (Miles, 1967b), both of
which are incorporated into the sheath precursors of the pentatomid
Eumecopus, the glycerol presumably being metabolized into the 10%
or so lipid moiety.
According to Hori (1968b), the mirid Lygus also has a strongly
PAS-reacting secretion in the anterior lobe (compared with the
posterior) of the principal gland. This insect produces no sheath
material and the anterior lobe secretes relatively little protein. In the
Pentatomorpha, by comparison, the anterior lobe, which does secrete
sheath precursors, produces a secretion that is strongly PAS-positive
and also contains a large amount of protein. These results, taken with
the finding that the blood-sucking reduviid, Rhodnius produces a
salivary material akin to sheath material, may mean that in all
Heteroptera the anterior lobe retains an ability to secrete protein
conjugated with carbohydrate and lipid, although in the forms that
secrete no sheath the amount of protein secreted is reduced. Even in
the Pentatomorpha, there is apparently a tendency for the most
anterior part of the anterior lobe to lose its ability to secrete a large
bulk of protein (Miles, 1967b), this function being taken over by
another part of the glands or perhaps by the hind region of the
anterior lobe, which becomes separated off as a distinct lateral lobe.
XI. THE SALIVA AS A VEHICLE FOR PATHOGENS

The pentatomid Acrosternum hilare (Say) acquires and transmits
the fungus Nematospora coryli Peglion when it feeds on lima or soy
beans or the berries of dogwood, Cornus drummondi Meyer; and
Dysdercus transmits N. gossypii to cotton bolls similarly (Clarke and
Wilde, 1970a, b). The spores contaminate the stylets and salivary
syringe and infectivity is lost during moulting. Clarke and Wilde
AIP- 11
242 PETER W. MILES
(1970a) were unable to recover the fungus from watery saliva

secreted outside plants (the insect was induced to salivate by
amputation of its antennae). Even so, the authors did not discard
salivary transmission as the most likely and they had not entertained
the possibility that this secretion might have been atypical of those
normally secreted within plant tissues (see Section VI1,B)-perhaps a
more viscous secretion, such as the sheath material, is normally
required to dislodge the contaminating spores.
By far the most significant instances of transmission of plant
pathogens by Hemiptera are the virus diseases carried by Homoptera.
The “non-persistent” viruses are transmitted immediately after they
have been acquired by the insects and the latter very rapidly lose
their infectivity; the “persistent” viruses are transmitted only after a
period of hours to weeks, the latent period, and usually the insect
then continues to be infectious until it dies. The non-persistent
viruses are not ingested before transmission and they are somehow
contaminants of the stylets or food canal of the feeding mechanism;
whereas the persistent viruses are ingested, transferred first to the
haemolymph and thence to the saliva.
The non-persistent viruses are typically transmitted by aphids and
are acquired from and transmitted to the subepidermal tissues of
plants. The persistent viruses are typically transmitted by the
jassomorph Homoptera and are acquired from and transmitted to the
vascular tissues of the plant. A number of authors have suggested
that the saliva is by no means an inert carrier of the viral particles
and may either inactivate them or modify the plant cells in such a
way that they become more or less susceptible (Sylvester, 1962;
Miles, 1968b).
Of most recent interest in the field of salivary transmission of
plant diseases is the finding of mycoplasma-like bodies (Fig. 19) in
the salivary syringe and ducts of the jassomorph leafhopper
Mucrosteles fascifrons (Raine and Forbes, 197 1) and in its ejected
saliva (Raine and Forbes, 1969), and the evidence that such bodies
are normally associated with individuals carrying the Aster Yellows
disease of China Aster and annual Chrysanthemum (Davis and
Whitcomb, 1970). Moreover, both the disease and the organisms
within the insect are alike attacked by certain antibiotics, according
to Whitcomb and Davis (1970), who nevertheless warn that some
non-infective individuals also carried the mycoplasma-like bodies and
that an absolute link of organism with disease had thus not been
established beyond all possible doubt.
m
c
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E
P
3
z
244 PETER W. MILES
Observations on identifiable infective organisms in the salivary

glands are of especial interest in the light of the report by
Ossiannilsson ( 196 1) and Moericke and Wohlfarth-Bottermann
(1960a, b) that the wall of the gut and the basement membrane of
the salivary glands respectively have no pores in them large enough to
allow viral particles (e.g. 32 x 300 mp in size) to move through.
Moericke (1961) found large viral bodies up to 50 x 400 mp in the
cells of the salivary glands of Myzus persicue infected with potato
leaf-roll disease; he reasoned that the infective unit must be very
much smaller and was probably molecular nucleic acid. The
mycoplasma-like bodies described by Raine and Forbes in the
salivary glands and ducts of Mucrosteles were up to 400 mp across.
Even larger particles, up to 800 mp across, have been described in the
cells of the glands themselves by Hirumi and Maramarosch (1 969);
Raine and Forbes (1 97 1) concluded that these must produce small
intermediate bodies that leave the cells and develop into the
organisms found in the saliva. On the other hand, Moericke and
Wolfarth-Bottermann ( 1960a) describe the discharge of secretory
granules up to 260 mp across from the cells of the salivary glands of
Myzus persicae by a membrane flow mechanism-i.e. a prosecretory
granule bulges out from the secretory cell into a canal cell, a part of
the cell membrane surrounding the granule detaches itself from the
parent membrane and the granule is eventually liberated when the
membrane dissolves.
Just how large a particle can pass all the way through the glands is
now known, however. Slama (personal communication) found that
the concentration of enzymes in the saliva of the phyrrocorid
Pyrrhocon's apterus was much the same as their concentration in the
haemolymph and the possibility must therefore be considered that
the enzymes merely found their way into the saliva by transport
from the haemolymph. In the only known check of this possibility
(Miles and Slowiak, 1970), peroxidase, with a molecular weight of
40,000, was shown to pass into the saliva of a pentatomid after
injection into the haemolymph, but this is a relatively small molecule
for a protein.
XII. EVOLUTION OF SALIVARY FUNCTION IN THE

HEMIPTERA: A SUMMARY
The salivary glands of Hemiptera can be thought of as having two
kinds of function:
(1) those of excretory organs due to their origin as the

segmental nephridia of the labial segment and
(2) those of epidermal cells due to their ectodermal origin.
The excretory function resides mainly in the accessory gland and
this is seen very clearly indeed in the Phylloxeridae. Whereas, in the
related aphids, the main excretion occurs into the midgut and the
accessory gland is small, in Viteus there is no anus and the accessory
gland is enormously increased in size. Characteristically, the cells
concerned with salivary excretion contain either large intracellular
vacuoles or an elaborate system of intracellular canals as in the
Aphidoidea or much of the accessory gland takes on the
characteristics of a Malpighian tube, as in the Jassoidea and the
He terop tera.
Epidermal cells, as Locke (1 970) has shown, can carry out a series
of functions simultaneously : they secrete the carbohydrate and
protein of the cuticle, pass on the lipid elements that are eventually
incorporated in the exocuticle and epicuticle, secrete the polyphenol
oxidase and peroxidase involved in the oxidative bonding that
stabilizes the cuticle, at the same time they secrete the hydrolysing
enzymes that digest the untanned parts of the old cuticle and they
assimilate the products. The cells of the principal salivary gland and
ducts of the salivary glands of Hemiptera similarly secrete the
precursors of the sheath material, as well as oxidizing enzymes and
hydrolysing enzymes, although there would seem to be a con-
siderable separation of specialized functions between the various
parts of the glands.
It is noteworthy that the ducts of the salivary glands have
chitinous linings. Miles (1 960a) drew attention t o the histochemical
and histological similarity of newly secreted sheath material and
newly secreted cockroach cuticle. It was found later that gelling of
the sheath material involved the formation of disulphide linkages, at
a time when it was widely reported that the cuticle of insects
contained no sulphydryl amino acids. Recently, however, this
generalization has been shown to be incorrect (Hackmann and
Goldberg, 197 1) and perhaps in the cuticle, as in sheath material, the
oxidative bonding of sulphydryl groups plays a part in the gelling and
stabilization of the precursor proteins.
If all the Hemiptera are to be derived from forms similar to the
Peloridiidae (Coleorrhyncha), then the salivary glands of the
Heteroptera are the more primitive in shape and form within the
Hemiptera as a whole. In both Homoptera and Heteroptera the
246 PETER W. MILES
accessory gland has retained a diuretic function, although there is

doubt whether a true accessory gland persists in the Fulguromorpha
(Balasubramanian and Davies, 1968). In the Heteroptera, the
accessory gland assumes a definitive form as a chitin-lined duct
surrounded towards its distal end by more or less glandular cells. In
all but the Pentatomorpha, the accessory gland has a thin walled
vesicle at its distal extremity. This vesicle, far from being a reservoir
for secretory products (Baptist, 1941), appears to be a bladder that
collects a dilute ultrafiltrate of the haemolymph. It is probably an
adaptation to predatory and other lacerate-and-flush feeding, in
which a copious flow of water is finally required to flush out the
food source. In the Pentatomorpha, although lacerate-and-flush can
be practised by the seed-feeders, the absence of a vesicle on the
accessory gland is possibly associated with a reduced need for large
quantities of watery secretion by insects adapted to the more
conservative stylet-sheath feeding.
Within all the Hemiptera, there is a clear division of labour
between the different lobes or types of lobe of the principal gland.
Even in the Peloridiidae, the poorly developed principal gland is
composed of an anterior and posterior lobe that have different
staining reactions (Prendergast, 1962). In the Heteroptera, the
posterior lobe is probably the main source of the hydrolysing
enzymes of the saliva. All the secretions of the principal gland are
relatively concentrated and it is likely that the posterior lobe in
particular produces a secretion that in normal function requires
dilution by the secretion of the accessory gland.
Although the anterior lobe in the Heter0ptera:Pentatomorpha
produces components of the sheath material, its primary function
throughout the Heteroptera may be the production of mucoid
substances and conjugated lipids that both lubricate the stylets and
are sufficiently viscous to dislodge particles at their tips; for, as
McLean and Kinsey (1965) have shown, this is one of the functions
of the sheath material of aphids. At the very beginning of the
evolution of the Hemiptera, some species must have begun to utilize
the solidification of this viscous secretion, brought about perhaps by
the release into the saliva of oxidases secreted by the ectodermal cells
of the ducts, perhaps by the increased content of sulphydryl groups
within the protein moiety of the secretion, perhaps by a combination
of both.
However evolved, this “sheath material” may originally have been
used to fix the stylets at one point on a hard or slippery surface
during its initial penetration (Saxena, 1963): but for all those species
that fed on phloem sap, the evolution of stylet-sheath feeding has
clearly become the most unique and characteristic of their salivary
functions. It also seems likely that evolution of the production of
sheath material has tended to result in a further division of labour
and proliferation of morphological divisions in those parts of the
glands responsible for its secretion; a convergent tendency in both
Homo p tera and Heteroptera :Penta tomorpha despite their p hy letic
separation.
XIII. A SURVEY OF PROBLEMS

Of the problems concerned with salivary function in the
Hemiptera that remain t o be solved, perhaps one of the most
intriguing is the function of the salivary oxidases. Little is known
about their secretion by Hemiptera other than that they can be
readily demonstrated in the stylet-sheaths of aphids and Pentato-
morpha in concentrations that must be physiologically active.
Miles (1969b) has attempted to rationalize the occurrence of
oxidase in the salivary glands and saliva of Hemiptera by suggesting
that the enzymes when first secreted may have subserved a
detoxifying function. This suggestion was based on the facts that:
(1) many of the toxic and repellant substances produced by
insects are based on phenolic compounds (their production no doubt
also being derived from the abilities of ectodermal cells to secrete
substances that tan the cuticle) and
(2) the reaction of plants t o wounding also involves the
secretion of toxic phenols.
Thus for insects that feed either on plants or other arthropods, the
possession of an antidote against toxic phenols and quinones, by
oxidizing them all the way to insoluble polymers, would be an
advantage.
It would seem t o be possible t o test this hypothesis by
experimental inactivation of the salivary phenolase system, either by
surgery on the salivary gland (Miles, 1967a) or by the use of reducing
compounds in artificial diets. It could then be determined whether
the insects’ sensitivity t o toxins was increased. A related problem is
the occurrence and function of salivary peroxidases and their
interaction with the phenol/phenolase system.
A further line of investigation of a possible detoxicant function of
248 PETER W. MILES
the saliva of phytophagous Hemiptera is indicated by a recent

investigation of the degree of resistance of various tissues from apple
trees to attack by the woolly aphis, Eriosoma Zanigerum (Sen Gupta
and Miles, unpublished). These insects will begin to colonize a variety
of seedlings germinated on wet filter paper, but survive on only apple
as the seedlings grow. In the field and greenhouse, a relation existed
between how readily the insect attacked different varieties of
apple-or different parts of any one tree-and the chemical
composition of the tissues. High amino acid content predisposed
tissues to attack, but phenolics appeared t o protect them; thus the
ratio of phenolics t o amino acids provided a rough means of
prediction of the resistance of any particular tissue t o attack
(Table V). Of further interest was the discovery that the galls
produced by the insects were more readily colonizable than
surrounding tissues.
A number of contingent questions are raised by these observations
and as yet remain unanswered. Is host specificity due to the presence
of specific phagostimulants (e.g. in apple and not in other plants) or
absence of repellents (in young as opposed to older seedlings)? Is
Table V
The susceptibility of tissues of the apple to attack by E. lanigerum in relation to
their chemical composition
Susceptibility
ratin& a-amino Nb phenolics (8)" @/N
Shoot
tip + 0.126f0.002 14.5f0.04 115

base ++ 0.096f0.002 lO.lf0.04 105
gall +++ 0.143fO.007 8.5f0.12 59
Root
8mm +++ 0.493f0.02 2 1 .OfO.1 1 43
4mm ++++ 0.806f0.02 16.3f0.11 20
gall *U+ 1.069f0.05 13.2f0.33 12
0 Based on measurement of rate of development of colonies, expressed semiquantitatively

because of incomplete equivalence of, for instance, physical conditions.
b mg N/g wet weight: colorimetric determination with ninhydrin against a D-alanine
*
standard, standard deviation.
mg/g wet weight: colorimetric determination with Folin and Denis reagent against a
*
catechin standard, standard deviation.
ability to feed on apple due to the possession by the insect of a

specific detoxicant for repellent (e.g. phenolic) substances present in
apple? Is the reduced toxicity of galls a direct result of salivary
action or an indirect result of the stimulation of cells to grow at a
rate greater than they can accumulate phenolics?
The problem of cecidogenesis itself is still far from closed. Despite
the elegant way in which Schaller (1 968b) has shown that the amino
acids and IAA injected by some aphids cause galls in plant
tissues-how the IAA comes to be present is an interesting problem
in insect physiology, while the roles of the salivary IAA and the
specific amino acids said to determine gall morphogenesis represent
an even more challenging problem in plant physiology.
The possible functions of the stylet-sheath and the salivary
oxidases in moderating the effect of feeding on the plants also
requires investigation. It has been suggested that the sheath, besides
increasing the efficiency of feeding by the phytophagous Hemiptera,
may also reduce those interactions between insect and plant that
cause necrosis in the latter (Miles, 1969b) with an obvious advantage
to both. According to Hille Ris Lambers (personal communication),
however, the aphid Aulucorthum soluni is a stylet-sheath feeder that
causes necrosis as a result of a single feed and this possible
exception should be especially worthy of investigation.
The problem of the role of the phenolic compounds as distinct
from the phenolases in the saliva of phytophagous insects also
require elucidation. Schaller ( 1 968a) has demonstrated that phenolic
compounds occur in the saliva of aphids and, at the same time, has
correlated their presence with a lack of pathogenicity of the insect.
Although some of these phenolics could well have been transferred
directly from the diet, Miles (1964a) demonstrated that one of the
phenolics present in the saliva of the phytophagous Heteroptera is
DOPA and that it is the end product of a specific metabolic pathway
in the salivary glands. Thus any investigation of the salivary oxidases
should take into account the complete phenol/phenolase system and
its eventual products.
The functions of the salivary glands and saliva of Heteroptera
other than the Pentatomorpha are still almost unknown. The division
of labour between the various lobes of their salivary glands remains
undetermined; the way in which Rhodnius produces its flange of
sheath material and in what way the loss of the anterior lobe has
affected the salivary physiology of the Cimicids remain further
intriguing problems.
250 PETER W. MILES
How viral or mycoplasmal particles find their way seemingly from

the gut to the saliva of Homoptera and details of the transmission of
rickettsia1 diseases by reduviids are further aspects of the salivary
physiology of Hemiptera that remain undetermined. Indeed, the
degree to which salivary composition is normally due to transport of
whole molecules including proteins from the haemolymph to the
saliva is largely unknown.
Finally, the control of salivary discharge and composition-
whether entirely by neural pathways or partly subject to hormonal
influences-remains apparently unexplored. Yet this knowledge will
be necessary to integrate what is known of salivary function into the
broader, but still unique, subject of the physiology of feeding of
these highly specialized and economically important insects.
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Miles 1972 Saliva of Hemiptera

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Miles 1972 Saliva of Hemiptera

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The Saliva of Hemiptera

which many of these insects feed. Some of the exclusively

significant Homoptera, in which research on the saliva is beset with

11. METHODS OF INVESTIGATION

The effects of the feeding of phytophagous Hemiptera were first

conductance of the system can be recorded on a cathode ray

the saliva of several hundred aphids at a time by placing them in

Fig. 4. Autoradiograph: Distriibytion of saliva labelled with '*P 'discharged by Myzus

within a few minutes unless it was first rapidly metabolized in the

111. MODES OF FEEDING

forms plant-feeding carnivorous Geocorinae

feeding, true Hemiptera

used to lacerate and macerate a pocket of cells or the entire contents

IV. STYLET-SHEATH FEEDING

All phytophagous Hemiptera, Homoptera as well as Heteroptera,

Such observations make it important to distinguish between an

B. SECRETION OF THE FLANGE

When Homoptera and Heteroptera : Pentatomorpha feed on plant

explanation for the observations of Hori and Hennig. They would

C. FORMATION OF THE SHEATH

A flange is not necessarily continued as a stylet-sheath into the

continuous with a stylet-sheath laid down wherever the tips of the

D. DISCHARGE OF WATERY SALIVA

Some watery saliva is ejected by aphids as part of the process of

Once the stylets have penetrated a source of ingestible food (e.g. a

particle, a small amount of sheath material is secreted (McLean and

These observations are a clear indication of the sealing properties

represented was difficult to estimate, since Bongers found almost no

VI. FEEDING BY CARNIVORES

cannibalism and suck eggs. It is interesting to note that when

Naucoris cimicoides 40 Immediate cessation

(I Data from Edwards (196 1).

VII. CHEMICAL COMPOSITION AND FUNCTION OF THE SALIVA

The Homoptera and Heter0ptera:Pentatomorpha produce an oral

the sheath during the second or less while it is solidifying (Miles,

applied to sap-sucking aphids, particularly since recent studies have

Some of the known components of the non-gelling secretions

0 Compounds Insects studied Features noted References

Compounds Insects studied Features noted References

Hyaluronidase Platymeris rhadamanthus Role as spreader in Edwards (1 96 1)

Aphis abbreviata Patch In both apterae and alatae

Dalbulus maidis (Del and Wohl) Demonstrated in adults

Adelphocoris seticornis (F) In males and females

Various spp. in Fulguroidea (5), Cercopoidea (2) and Jassoidea (10).

Various spp. in Lygaeidae ( l ) , Coreidae (2) and Pentatomidae (4)

a In saliva secreted into filter paper (Adams and McAllan, 1958).

than to function primarily in the digestion of a major nutrient

are said not t o have hydrolytic enzymes other than carbohydrases in

The saliva of Hemiptera is noted for its content of amino acids

endpoint of indole metabolism in animals, and the recent work of

Large numbers of some species of aphids or leafhoppers can

Fig. 9. Formation of galls: a: “physiological gall”. b: surface gall; c: occluded necrosis;

Such localized effects of feeding must be differentiated from

probably thereby increased respiration, transpiration and proto-

Nevertheless, that amino acids were found at all gives a good

observation that hypertrophy of cells can occur at the edge of the

nevertheless occur in the haemolymph and therefore saliva as the free

compounds in the saliva of the insects, even though the apparent

IX. SALIVARY GLANDS AND DUCTS

The salivary glands of Hemiptera are labial glands, lying mainly in

Fig. 1 1. Salivary glands of Hemiodoecus veitchi Hawker (Co1eorrhyncha:Peloridiidae).

The salivary glands, although apparently simple, have been shown

According to Moericke and Wohlfarth-Bottermann ( 1 960b) the cells

Fig. 13. Salivary glands of Viteus vitifolii (Phylloxeridae), semidiagrammatic. a: bilobed