Antennal sensilla of some aphidophagous Syrphidae (Diptera): fine structure and

electroantennogramme study

D. E. HOODHENDERSON' AND W. G. WELLINGTON

Institute ofAnimal Resource Ecology, University of British Columbia, Vancouver, B . C . , Canada V6T 1W5
Received June 3, 1982
Can. J. Zool. Downloaded from www.nrcresearchpress.com by Université de Sherbrooke on 11/21/12

HOOD
HENDERSON,
D.E., and W. G. WELLINGTON.
1982. Antennal sensilla of some aphidophagous Syrphidae (Diptera): fine
structure and electroantennogramme study. Can. J. Zool. 60: 3 172-3 186.
Antennal sensilla of Metasyrphus venablesi (Cn.) and Eupeodes volucris 0 .S. (Diptera: Syrphidae) were studied by scanning
and transmission electron microscopy. Males and females both had four types of sensilla. Three of these, two multiporous pitted
(mpp) sensilla (one round-tipped and one pointed) and a multiporous grooved peg sensillum, were also confirmed by scanning
electron microscopy on the following species: Syrphus torvus O.S. ( Q , d ), Syrphus opinator O.S. ( ? , d ), Scaevapyrastri (L.)
( Q , d ) , Dasysyrphus amalopsis 0 . S . ( Q ), Xanthogrammaflavipes Lw . ( d ) , Brachyopa perplexa Cn. ( d ), Pipiza sp. ( Q ), and
Xylota quadrimaculata Lw. ( d ) . The fourth mpp sensillum had thicker walls and fewer pores. All four types were located among
dense noninnervated setae on the antenna1 bulb and are probably olfactory. Electroantennogramme (EAG) study revealed
antennae of female M . venablesi to be sensitive to some components of the aphid-plant oviposition site complex, namely, some
green plant volatile substances (6-carbon alcohols), crushed pea aphids, crushed carnation petals, methylsalicylate and
amylacetate, and to be nonresponsive to honeydew and some of its components (tryptophan, indolealdehyde, and
indoleacetaldehyde).

HOODHENDERSON, D.E., et W. G. WELLINGTON. 1982. Antennal sensilla of some aphidophagous Syrphidae (Diptera): fine
structure and electroantennogramme study. Can. J. Zool. 60: 3 172-31 86.
For personal use only.

Les sensilles antennaires ont CtC examides chez Metasyrphus venablesi (Cn.) et Eupeodes volucris O.S. (Diptera: Syrphidae)
aux microscopes Clectroniques ordinaire et a balayage. Les miiles et les femelles portent quatre types de sensilles. Trois de ces
sensilles, deux sensilles picotCes a plusieurs pores (mpp) (une a bout rond et une pointue) et une sensille en bhtonnet a plusieurs
pores et un sillon, ont CtC observkes Cgalement au microscope Clectronique chez les espkces suivantes: Syrphus torvus O.S. ( Q ,
d ) , Syrphus opinator O.S. ( Q , d ), Scaeva pyrastri (L.) ( Q , d ) , Dasysyrphus amalopsis O.S. ( Q ), Xanthogrammaflavipes
Lw . ( Q ), Brachyopaperplexa Cn. ( d ), Pipiza sp. ( Q ) et Xylota quadrimaculata Lw . ( d ). La quatrikme sensille mpp a une paroi
plus Cpaisse et compte moins de pores. Les quatre types de sensilles sont dispersCs au milieu de soies non innervCes sur le bulbe
antennaire et ont probablement un r61e olfactif. Une Ctude par Clectroantennogramrnie (EAG) a dtmontrk que les antennes de M.
venablesi sont sensibles a certaines substances du complexe aphide-plante qui sert de site de ponte, notamment des substances
vCgCtales volatiles (alcools a six carbones), des pucerons du pois pilCs, des pCtales CcrasCs d'oeillets, le salycilate de mCthyle et
I'acCtate d'amyle; par ailleurs, les antennes ne rkagissent pas au miellat ou a certains de ses composCs, le tryptophane,
I'indolaldChyde ou 1'indolacCtaldChyde.
[Traduit par le journal]

Introduction able to respond to an environment quite distinct from her

Adult syrphids are primarily pollen and nectar feed- own preferred feeding site. Searching for an oviposition
ers although some may also utilize aphid honeydew site involves several sensory modes simultaneously or in
(Schneider 1969; Holloway 1976). They are important sequence, and olfaction is generally believed to be the
pollinators. Larval syrphids have diverse feeding pat- most important mode for syrphids (Bombosch and Volk
terns, but a number are obligate predators of aphids. 1966; Dixon 1959; Schneider 1969).
Both of these stages of the life cycle, then, are beneficial An oviposition plant infested with aphids presents
to agricultural and horticultural interests, and because of olfactory stimuli from two different sources: the plant
their importance, adult and larval behaviour towards and the aphid with its excretion-honeydew. The honey-
aphids has been studied (Dixon 1959; Chandler 1966, dew component of oviposition sites has been shown to
1967, 1968a, 1968b, 1968c, 1968d, 1969; Bombosch be attractive not only to syrphids but also to other aphid
and Volk 1966; Sanders 1979, 1980). Since these predators (Bensaad and Bishop 1976). The green lace-
predatory larvae are blind and move only slowly, an wing Chrysopa carnea, after first being attracted to
adult female must oviposit in or very near an aphid tryptophan in artificial honeydew sprayed on field crops
colony to ensure survival of her offspring. She must be (Hagen et al. 1976), was attracted to this amino acid and
some of its decomposition products in an olfactometer
'present address: Department of Zoology, University of (van Emden and Hagen 1976). Because green lacewings
Toronto, Toronto, Ont., Canada M5S 1A 1. responded to these olfactory attractants, it is not unrea-
0008-4301 /82/123172-15$01 .OO/O
01982 National Research Council of Canada/Conseil national de recherches du Canada
 HOOD HENDERSON AND WELLINGTON
sonable to expect that other aphid predators, including
syrphids, may respond similarly. These chemicals have
been tested in behavioural experiments (Hood Hender-
son 1981) with some positivd results, suggesting elec-
troantennogramme (EAG) study of the syrphid antenna
may be profitable.
Visser's 979) studies On EAG of Colo-
rado potato that the 6-carbon chain
Can. J. Zool. Downloaded from www.nrcresearchpress.com by Université de Sherbrooke on 11/21/12
alcohols and aldehydes, common in green plants and to
which the beetles responded, also elicited EAG re-
sponses from many other phytophagous insects, includ-
ing the tobacco horn worm Manduca sexta, a shoot
borer Hypsipyle grandella, the ermine moth Yponom-
euta sp., the locust Schistocerca gregaria, the beetle
Adoxophyes o r a n a , and the carrot rust fly Psila rosae
(Guerin and Visser 1980). Visser (1979) concluded that
this group of compounds was of importance to the host
selection process among phytophagous insects. Six-
carbon chains have also been shown to be important to at
least one dipteran, the blowfly Calliphora vicina, (Kaib
1974) in which one type of antennal receptor for meat
odours is especially sensitive to 6-carbon aldehydes,
For personal use only.
alcohols, and ketones. Thus, the sensitivity to 6-carbon
chain compounds may be even more widespread than
Visser (1979) suggested. These comprise another group
of compounds that may be utilized by the syrphid and
which could be tested by EAG study.
This paper reports on a fine structural study of the
antenna, the primary organ of olfaction, of two species
of aphidophagous syrphid, Metasyrphus venablesi
(Cn.) and Eupeodes volucris O.S. EAG studies con-
ducted herein result from tests of compounds from two
sources, the host plant itself and the aphid excretory
product, honeydew.
Materials and methods
Rearing syrphids
Metasyrphus venablesi and Eupeodes volucris were reared
by Frazer's method (1972) with some minor changes. In
addition to the large cages with feeding platforms used by
Frazer (1972) we also used slightly smaller cages (70 x 60 x
50 cm) for adult flies. Fresh pollen in the form of flowers was
supplied when available in addition to freeze-dried Corylus sp.
pollen. Acyrthosyphon pisum (Harris) or Aphis fabae Scopoli
were used to induce oviposition. These aphids were reared on
broad bean, Vicia faba major cv. Broad Windsor, planted in
sterile soil. Upon hatching, syrphid larvae were not removed
individually from the oviposition plants. Instead, a whole plant
was placed in a cage with nine pots containing 17-cm high
broad beans infested with A. pisum so that the larvae could
move at random from their original plant. Cannibalism was
never a problem unless aphids were scarce. Rearing-room
temperature ranged between 22 and 25"C, with a relative
humidity of 65%. The cages were illuminated by a combina-
tion of warm and cool fluorescent lights with a 1ight:dark
regime of 16:8 h.
3 173
To avoid problems with a virus that appeared during the first
few months of continuous rearing, all cages were cleaned after
each rearing session with detergent (Bactrex) and 70%
ethanol. An independent colony of A . pisum was kept in a
cooler room, 10-15"C, with 16 h light, specifically to infest
new broad beans with "clean" aphids. The virus ceased to be a
problem with this treatment, so that colonies of M . venablesi
were kept for 10- 12 months at a time, and E. volucris could be
kept for 4-5 months. Syrphid generation time under these
conditions was 5-6 weeks.
Additional species studied here were collected locally
before study or reared to the adult stage from eggs. Some
specimens were supplied by Dr. J . R. Vockeroth, Bio-
systematics Research Institute, Ottawa, and these were a male
Brachyopa perplexa Cn . , a female Dasysyrphus amalopsis
0 . S. , a female Pipiza sp. , a male Xanthogramma Jlavipes
Lw., and a male Xylota quadrimaculata Lw .
Scanning electron microscopy
For scanning electron microscopy (SEM) of antennae,
either whole heads or portions of cuticle containing antennae
were excised from freshly killed syrphids and stored in 70%
ethanol. Antennae were cleaned by sonication first in a 50%
ammonium hydroxide solution for 50 s and then for three
consecutive 30-s periods in pure acetone. The specimens were
air dried, mounted on stubs with rubber cement diluted 5 0 5 0
with chloroform, and gold coated (Eiko Engineering IB-2 Ion
Coater). Two male specimens of each, and five, five, four,
three, and three female specimens of M . venablesi, E.
volucris, Syrphus torvus 0 .S ., Syrphus opinator 0 . S . , and
Scaeva pyrastri L., respectively, were studied with a Hitachi
S500 scanning electron microscope.
Transmission electron microscopy
Specimens were dissected in 5% gluteraldehyde (in phos-
phate buffer, pH 7 .O-7.2) on ice, then left overnight in fixative
in partial vacuum (ca. 16 lb). Postfixation was in 2% osmium
tetroxide (pH 7.0) on ice for 1 h. Specimens were slowly
dehydrated in ethanol to 70% in an ice bath, then at room
temperature from 80% to propylene oxide, all in partial
vacuum. Tissue was infiltrated overnight in 5 0 5 0 propylene
oxide and an embedding medium (Epon 8 12, Spurr 's , Quetol,
or Epon-Araldite) in partial vacuum. The following day,
specimens were embedded in the appropriate pure resin for
polymerization. Most sections were cut with a glass knife and a
few with a diamond knife on a Reichert OM U-2 ultramicro-
tome. Staining was achieved in uranyl acetate and lead citrate,
on collodion, carbon-coated 100-mesh copper grids. A Philips
model 200 or model 300 transmission electron microscope was
used to view sections.
Electroantennogramme recordings
Electroantennograrnrnes were obtained in Dr. B. K. Mit-
chell's laboratory in the Department of Entomology, Univer-
sity of Alberta. Antennae from freshly decapitated laboratory-
reared M . venablesi females were excised at the first antennal
segment. The tip of the third segment was then removed before
the base was inserted in the end of a glass micropipette filled
with 0.0 1 M NaC1. The pipette was placed over a silver - silver
chloride electrode mounted on a Leitz dissecting microscope.
 3 174 CAN. J. ZOOL. VOL. 60. 1982

The second (recording) electrode, in another micropipette
containing 0.01 M NaCl, was then placed within the hole in the
tip of the third antennal segment.
Signals from the recording electrode passed through a
microamplifier and could be viewed on a Tektronix 549
storage oscilloscope or recorded on a Harvard No. 486,
12-speed chart recorder. Responses were recorded on 35-mm
Ektachrome slide film, using the oscilloscope storage func-
tion, and on photographic paper in a Cine-scope recorder
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sensilla could not be accurately counted, but searches for
each type soon showed that they varied in density. The
two most common were typical multiporous sensilla
(mpp) (Fig. ID) with exteriors pitted by numerous
pores. These sensilla differed in size and shape. The
more common type had a rounded tip, a mean length of
7.78 + 0.31pm, n = 2, and a diameter of 1.5 +
0.3 1 pm, n = 9 (Fig. 2A). The less common type had a

connected to a second Tektronix oscilloscope.
Solutions to be tested were applied by micropipette until
they saturated one-half the circle of a 1-cm disc of filter paper.
The wet filter paper was then placed in a 3-rnL syringe
equipped with its needle and 12 cm of plastic tubing having the
same bore as the needle. After the desired quantity of air was
drawn into the syringe, the tube was sealed to allow the test
compound to saturate the air.
An L-shaped glass tube, tapered at both ends and with a
5-mm diameter hole at the elbow, was used to deliver the
stimulus. A small aquarium air pump was connected by soft
rubber tubing to an activated charcoal filter which in turn was
connected to the short arm of the L-shaped tube. The tube was
positioned in a clamp stand so that the tip of the long side of the
L was only a few millimetres from the excised antenna and
pointed directly at it. The air forced over the preparation by the
For personal use only.
pointed tip, with a mean length about half that of the
other type (3.66 + 0.34 pm, n = 3) and a diameter at the
widest point of 1.67 + 0.27 pm, n = 5. At the tip, the
diameter measured 0.17 + 0.01 pm, n = 3 (Fig. ID).
Density of pores was not estimated.
The less common was a grooved peg sensillum (mpg)
of mean length 2.5 + 0.59 pm, n = 9, and width at the
widest point 0.89 + 0.16 pm, n = 11. Each peg had a
collared appearance, as it arose from a shallow pit and
each had 12 grooves in cross section (Fig. 4C). There
were no pores in the distal tip of the peg. The tips in M.
venablesi and E. volucris were blunt (Fig. 4A) but in
some other species, e.g. X. quadrimaculata they have a
more pointed extremity. These three types of sensilla
were found in both males and females of M. venablesi,

pump was carried away by a vacuum line attached to a funnel

on the other side of the microscope. The pump provided a
constant rate of airflow throughout all experiments. Test
substances were introduced into the air stream by inserting the
tubing of the syringe into the hole at the elbow of the delivery
tube and injecting the syringe contents quickly and smoothly.
All equipment, exclusive of the recorders, was enclosed in a
copper mesh cage to eliminate extraneous electrical interfer-
ence. Room temperature was 22°C.
Results
Fine structure of antennal sensilla
Syrphid antennae consist of three segments, a scape
and pedicel and a large terminal bulb. The bulb is oval
shaped in cross section and covered with a dense mat of
noninnervated cuticular setae. A long slender arista
articulates from the laterodorsal margin of the bulb (Fig.
1A). Antenna1 sensory structures (excluding Johnston's
organ) are all located on the antennal bulb.
The most numerous structures on the bulb are the
noninnervated setae (Fig. 1C). They are long (mean,
13.1 + 0.39 pm, n = 4) curved, spirally grooved, and
tapered to a fine point. Interspersed along these setae are
four types of chemoreceptive sensilla, all multiporous.
Because of the dense mat of setae, total numbers of these
E. volucris, S. towus, and S. pyrastri. There was no
appreciable difference in size among sensilla of these
species. Multiporous round-tipped sensilla and grooved
pegs were also found in the following species: a female
D. amalopsis, a female Pipiza sp. , a female X. Jlavipes,
a male X. quadrimaculata, and a male B. perplexa
(Figs. 3D, 3E, 4B).
The fourth sensillum (mppt) was also multiporous but
was shorter and more slender with fewer pores and
thicker walls (Fig. 3B). These sensilla were only
infrequently encountered in the antennal bulb though
they occurred in higher density around the laterodorsal
margin, in the vicinity of the arista. In this area, the other
kinds of mpp sensilla were less frequent. This fourth
type of sensillum arises out of a depression in the cuticle,
as do the grooved pegs.
Some workers have reported apparent "sensory pits"
on the antennal bulbs of syrphids. These pits are much
more prominent in some species than in others. In the
species examined here, "pits" are visible but not
prominent (Fig. lc). Upon examination by SEM, these
structures proved not to be "pits," but areas with
a thinner population of noninnervated setae, which
allowed a clearer view of the underlying sensory

FIG.1. (A) SEM of a whole head preparation of a male B. perplexa showing prominent antennal sensory pits (sp). (B) SEM of
the antennal bulb of a male B. perplexa sensory pit area showing numerous round tipped multiporous sensilla (mpp- I). Note the
absence of noninnervated setae (nis) in the area of the pit. (C) SEM of the antenna of a female E. volucris showing faint "sensory
pit" areas (sp) and a dense covering of noninnervated setae on the bulb (b). Sparser and shorter noninnervated setae and a few
long stout setae cover the pedicel (p). The arista (a) has very few setae. (D) SEM of a female M. venablesi antennal bulb showing
two types of thin-walled perforated multiporous sensilla: rounded (mpp-1) and pointed (mpp-2).
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HOOD HENDERSON AND WELLINGTON

3 175
 3176 CAN. J. ZOOL. VOL. 60, 1982

structures. Sensilla did not apear more numerous in
these "pits. "
A male specimen of B. perplexa was obtained for
SEM study of its very prominent antennal "pit" (Fig.
1A). This round area could be seen to contain a dense
population of round-tipped multiporous sensilla (Fig.
1B). Surface cuticle wa snot visible, because the sensilla
were so dense. These sensilla were not confined to the
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branch (Fig. 2C). The outer sheath or tormogen cell with
its cytoplasmic lamellae lined the outside of the rather
limited receptor lymph cavity (Fig. 2C). Structures
below the cuticle level were not easily distinguishable,
because of crowding together of the cellular portions of
many sensilla and the difficulty in obtaining serial
sections of the very thick hard antennal cuticle. Conse-
quently, the presence of an inner sheath cell was not

"pit," however, but were also scattered over the entire
bulb at a lower density (Fig. 3D).
The two common mpp sensilla, types I and 11, could
not be distinguished in TEM sections, as cross sectional
diameters were very similar and the tip was rarely seen.
They will be described together here. Cuticle in the
external sensillum was thin (0.15 3- 0.04 Fm, n = 10)
with numerous pores. Narrowest pore diameter was
32.8 + 6.8nm, n = 10. Pores flared slightly to the
exterior and opened into bell-shaped cavities to the
interior (Fig. 2B). No pore tubules were seen.
Usually three, sometimes two, dendrites without a
dendritic sheath could be found in the cuticle below
these sensilla (Fig. 2C). As the dendrites enter the
external sensillum, they branch into many small den-
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established.
Groove mp sensilla are innevated by three unbranch-
ed dendrites (Fig. 4C) in a small dendritic chamber. In
cross section, the grooves appear as clefts between
rounded cuticular flutes. The clefts are rounded at their
base and extend the length of the groove. Pores are
slitlike (Fig. 4C), extending from the base of the cleft to
the dendritic chamber without pore tubules. There is an
outer ring of channels within the cuticular flutes giving
the sensilla double-w alled appearance (Figs. 4C, 4D).
Distally, dendrites are enclosed in a thick dendritic
sheath part way up into the external cuticular structure
(Fig. 4E). The intermediate sheath cell (trichogen)
surrounds the dendritic sheath below the cuticle. The
outer sheath cell with its lamellae lines the receptor

dritic extensions (Fig. 2D). The pattern in cross section
was variable (Fig. 2D). Often one dendrite remained
unbranched or else rolled upon itself in concentric
circles. Dendritic processes were close to but did not
appear to enter the flared pore bases (Fig. 2B). Sheath
cells included an intermediate or trichogen cell, which
wrapped around the distal dendrites until they began to
lymph cavity part way through the cuticle but not to the
base of the external sensillum. The receptor lymph
cavity is continuous with the cuticle-lined channels of
the external sensillum. Structures below the cuticle
could not be delineated because of difficutly in obtaining
serial sections.
The fourth type of sensillum, the thicker-walled

FIG.2. (A) SEM of a female S . opinator antennal bulb showing surface pores of a multiporous thin-walled sensillum type I .
(B) Cross section of a thin-walled sensilla (mpp) with a large dendrite rolled upon itself, and several other dendritic branches
(db). The pores (p) widen internally. Pore tubules are not present but there is a matrix of electron dense material in the sensillar
lumen. (C) Longitudinal section of a thin-walled multiporous sensillum arising from the cuticle surface without a cuticular collar
or depression. Distal dendrites ( 4 are not surrounded by a sheath. The intermediate sheath, or trichogen cell (s2) and the lamellae
of the outer sheath cell (s3) line the somewhat limited receptor lymph cavity (r). (D) TEM of cross sections of several thin-walled
multiporous sensilla (mpp type 1 or 2 or both). Note the variable number of dendritic branches (db) and dendrite pattern
differences. The sensilla emerging from the cuticle is mpp and its dendritic branching starts from the point of emergence from the
cuticle.
FIG.3. (A) TEM of a female E. volucris antennal bulb, longitudinal section of a thick-walled multiporous sensillum (mppt).
Note the thick walls (tc) with straight pores (p) without pore kettles and dendrites ( 4 in the sensillar lumen. (B) SEM of a female
M. venablesi antennal bulb with a grooved peg sensillum and a thick-walled multiporous chemosensillum (mppt) both arising
from cuticular depressions. (C) TEM cross section of a thick-walled multiporous sensillum with two dendrites ( 4 and several
pores @). (D) SEM of the antennal bulb of a male B. perplexa some distance from the sensory pit, showing a multiporous
sensillum (mpp-I), a groved peg sensillum (mpg), and several noninnervated setae (nis). (E) SEM of the antennal bulb of a
female Pipiza sp. with a multiporous perforated, round-tipped sensillum (mpp-1).
FIG.4. (A) SEM of a male S. pyrastri antennal bulb, groved peg sensillum (thin-walled, multiporous grooved type mpg). (B)
SEM of the antennal bulb of a male X. quadrimaculata multiporous grooved peg sensillum (mpg). Note the depression in the
cuticle. (C) A cross section of a grooved peg sensillum. Note the three unbranched dendrites, cuticle-lined spaces (cc) and the
pore between the grooves (p). (D) A longitudinal section through the tip of a grooved peg sensillum. Dendrites ( 4 extend almost
to the tip of the peg without branching, and the grooves (g) extend to the tip also. Note the cuticle-lined channels (cc). (E)
Longitudinal oblique section through the distal dendrites ( 4 of a grooved peg sensillum in a female M. venablesi antennal bulb.
There is an electron dense dendritic sheath (ds) surrounding the dendrites. In the receptor lymph cavity, lamellae of the outer
sheath or tormogen cell (s3) are visible.
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CAN. J. ZOOL. VOL. 60, 1982
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HOOD HENDERSON AND WELLINGTON
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 3 180 CAN. J. ZOOL. VOL. 60. 1982

mppt, were rare and consequently only infrequently

sectioned. Wall thickness was 0.18 k 0.02 pm, n = 10.
There were most commonly two dendrites (Fig. 3C) in
cross section but occasinally five were seen. From the
similar diameters of dendrites, it seems likely that there
were two similar sensilla, with different numbers of
dendrites rather than dendritic branching.
The pores of these sensilla lacked "pore kettles"
*
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(Figs. 3A, 3C) and had a narrowest diameter of 2.2

0.5 nm, n = 10. The pore channel flared slightly to the
exterior and to the interior. Pore tubules could not be
seen. In longitudinal and cross sections, there was no
dendritic sheath in the large central chamber (Figs. 3A,
3C). Neither was there a dendritic sheath surrounding
distal dendritic extensions in and below the cuticle in
most of these sections. There were a few sensilla in this
area, however, that did have a dendritic sheath although
there were always more than two dendrites inside it.
Though evidence is incomplete, this variation supports
the suggestion that the five-dendrite sensillum was not a
branched two-dendrite sensillum but a separate type.
Electroantennogramme recordings
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Two female M. venablesi were tested with the

following chemicals: volatile green plant substances
trans-2-hexen- l-ol, cis-2-hexen- l-ol, trans-3-hexen-
l-ol, cis-3-hexen- l-ol, cis-3-hexenyl-acetate (Roth
Chemicals), and hexanol-1 (Sigma Chemicals); crushed
carnation petals; crushed pea aphids; two other volatile
substances of plant origin, methylsalicylate and amylac-
etate; honeydew and some of its components, namely
tryptophan, indolealdehyde, and indoleacetaldehyde
(American Scientific Chemicals).
A positive response or antennal nerve depolarization
showed on the oscilloscope as a dip in the base line
followed by a recovery to the original level. Syrphid
antennae proved to be excellent preparations for EAGs.
Base-line noise was low and the signal was stable,
drifting only rarely. Preparations lasted up to 8 h,
allowing replicate testing of many substances.
Controls of dry (dry filter paper disc in the syringe)

FIG.5. Electroantennogrammeresponses to 2-mL quantities

of air saturated with each of the following substances: (A)
moist air control, (B) dry air control, (C) trans-2-hexen- 1-01,
(D) cis-2-hexen- l-ol, (E) trans-3-hexen- 1-01, (F) cis-
3-hexen- 1-01, ( G ) hexanol- 1 , (H) cis-3-hexenyl acetate, (I)
crushed carnation petals, (J) crushed aphids, (K) methyl-
salicylate, (L) arnylacetate , (M) honeydew (in water), (N)
indolealdehyde, and ( 0 ) indoleacetaldehyde. The deflection
distance down indicates the quantitative response of the
antennal nerve. The form of the dip indicates the smoothness
of the application. One second is indicated by two dashes of the
line under each response recording. The arrow indicates the
point in time of application.
 HOOD HENDERSON AND WELLINGTON
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dose in mL

I - . . . . ,
0.5 1 1.5 2 2 5 3
dose in m L
For personal use only.

0.5 1 1.5 2 25 3
dose i n mL

FIG.6. Dose-response curves for green plant volatiles in millivolt deflection units against dose of saturated air administered by
syringe to a constant air flow over female M. venablesi or E. volucris antennae prepared for electroantennogramme responses.
(A) Trans-2-hexen- l-ol. (B) Trans-3-hexen- l-ol. (C) Hexanol- 1. (D) Cis-2-hexen- l-ol. (E) Cis-3-hexen- l-ol. (F)
Cis-3-hexenyl acetate. (G) EAG responses in millivolt deflections for 2-mL quantities of air saturated with the following
substances: (1) amylacetate, (2) crushed carnation petals, (3) crushed aphids, (4) methylsalicylate, and (5) honeydew.

and moist air (wet disc in the syringe) elicited no
response, or only a slight response when an injection
was too quick or uneven (Figs. 5A, 5B). Dry and moist
controls were tested after every 8 or 9 stimulations. All
experimental filter paper discs were saturated with the
test solution. Variable quantities of test molecules could
be administered by varying the volume of saturated air
iqjected. Preliminary trials showed that a recovery time
no greater than 1 min was required to obtain maximal
response during subsequent stimulations.
Preparations varied slightly in their magnitude of
response, but there was rarely any question whether
there had been a response. Ten replicates of each of the
green plant volatiles elicited positive responses in both
antennal preparations. Responses to trans-2-hexen- l-ol
and trans-3-hexen-1-01 are shown in Figs. 5C, 5E.
Dose-response curves for these plant volatiles were
constructed for one antennal preparation (Figs. 6A, 6B).
The cis isomers of these two compounds showed no
differences in response (Figs. 5D, 5F). The dose-re-
sponse curves for these isomers are shown in Figs. 6D,
6E. Positive responses were also obtained for hexanol-1
(Fig. 5G) and cis-3-hexenylacetate (Fig. 5H).
Twenty to 30 pea aphids ground with 2 pL of
distilled water produced enough liquid to soak a filter
paper disc. Antennae were subjected to 2 mL of satu-
rated air from this syringe. This treatment was repeated
twice and each time a slight reaction was recorded (Fig.
5J). The mean response is plotted in Fig. 6G.
The liquid from crushed white carnation petals was
used to soak a filter paper disc. One antenna was given
graded tests with this stimulus in amounts of 0.4, 2.0
(Fig. 51), and 3 mL. It responded with respective
deflections of 0.23,0.46, and 1.24 mV. The response to
2 mL is shown in Fig. 6G.
Two other volatile substances of plant origin, methyl-
 3182 CAN. 1. ZOOL. VOL. 60, 1982
salicylate and amylacetate, had strong odours easily
detectible by humans. These substances were each
tested once. There were responses to 2-mL quantities of
both chemicals (Figs. 5K, 5L). The magnitudes of the
responses are shown in Fig. 6G for comparison with
other substances tested.
Honeydew was collected by placing a plastic petri
dish lid under a heavily infested broad bean leaf
Can. J. Zool. Downloaded from www.nrcresearchpress.com by Université de Sherbrooke on 11/21/12
overnight. The resulting solids were dissolved in 0.1 mL
distilled water and used to saturate a filter paper disc.
When 2 mL of saturated air from this syringe were
passed over one antenna, there was only a very slight
deflection of the baseline (Fig. 5M). Honeydew compo-
nents, indolealdehyde (both saturated in distilled water)
and indoleacetaldehyde (0.01% in distilled water) were
applied to antennae five and two times, respectively,
with no response (Figs. 5N, 50). Similarily, there was
no response to tryptophan. Thus, while plant substances
and crushed aphids elicited definitive EAG responses
from female M. venablesi antennae, honeydew, some of
its components, and oxidation products did not.
Discussion
For personal use only.
Antennal sensilla
Antennal sensilla of the syrphids studied here con-
tained no apparent mec hano- or contact chemosensilla.
All sensilla were confined to the antennal bulb and
appeared to be olfactory in nature. The absence of
chemosensory sensilla on the dipteran arista has been
noted by others (Bay and Pitts 1976; Dethier et al. 1963;
Lewis 1971;White and Bay 1980), and no structure of a
chemosensitive nature has ever been reported on the
scape or pedicel (Greenberg and Ash 1972). This
specialization has been reported for other higher Diptera
(Slifer and Sekhon 1964; White and Bay 1980).
The long noninnervated setae covering the antennal
bulb may possibly serve a protective function or play a
role in modifying (i.e., slowing and dispersing) airflow
over the sensilla. Except in the sensory "pit" area of
some syrphids, these setae cover the antennal bulb
entirely and the shorter sensilla are found dispersed
among them.
Pit-su@aced, multiporous sensilla
Thin-walled, pitted multiporous sensilla of types I
and I1 (mpp or sensilla basiconica) found in this study
bear a resemblance to those commonly found in other
Diptera (Bay and Pitts 1976; Dethier et al. 1963; Lewis
1971; Slifer and Sekhon 1964; White and Bay 1980) in
size, wall thickness, number of neurons, and dendritic
branching. Their pore structure, however, is unusual.
Whereas other flies studied all had pore kettles and pore
tubules associated with each cuticular perforation, pores
of the present sensilla widen into a bell-shaped cavity
continuous with the lumen of the sensillum. Possibly
pore tubules are not needed to complete the connection
through cuticle. This arrangement of pores was reported
for sensilla trichodea of the sand fly Culicoides furens
(Chu-Wang et al. 1975). The absence of a dendritic
sheath has been observed in the previously mentioned
sensilla of C. furens (Chu-Wang et al. 1975) and also in
the face fly Musca autumnalis (Bay and Pitts 1976).
The variation in pattern of dendritic branching within
the sensillum was also observed by Lewis (1971) in
Stomoxys calcitrans. According to Lewis, a finely
branching dendrite in an olfactory sensillum is likely to
be more sensitive than a larger unbranched one. This
difference therefore may indicate variable sensitivity in
neurons. The functional significance of concentrically
layered dendrites has not been elucidated, but it has been
suggested that the increased surface area similarly
increases the receptive surface (McIver 1972). Various
"rolled" arrangements of dendrites have been reported in
thin-walled pegs (sensilla basiconica) on the palps of
female culicine mosquitoes (McIver 1972), in pegs in
pits (sensilla coeloconica) on the antennae of culicine
mosquitoes (McIver 1973), in the bulb-shaped sensilla
of the palps of C. furens (Chu-Wang et al. 1975) as well
as in the apparently olfactory clavate sensilla (with
pitted surface) on the antenna of S. calcitrans (Lewis
1971). In the sandfly and culicine mosquitoes, the
sensilla with similar "rolled" dendrites are suggested to
function as carbon dioxide receptors (Chu-Wang et al.
1975; McIver 1973).
Groove-su@aced, multiporous sensillum
The grooved pegs in this study were surface struc-
tures, never found in pits, as they have been for C.
furens (Chu-Wang et al. 1975) and Anopheles stephensi
(Boo and McIver 1976). This surface arrangement is
also common among other flies studied (Bay and Pitts
1976; Dethier et al. 1963; Lewis 1971; Slifer and
Sekhon 1964; White and Bay 1980). The number of
grooves found here, 10- 12, is in the low range of the
number reported for other Diptera, 10-16. Pores are a
common features in these sensilla, and only in one
species, Aedes aegypti, (McIver 1974) do terminal
pores replace pores along the grooves. Groove pores
have no pore tubules (Zacharuk 1980) but sensilla
containing them are considered olfactory because of
neurophysiological evidence (Kellogg 1970 for those
with terminal pores, and Altner et al. 1973, in Zacharuk
1980, for multiporous types). The three unbranched
dendrites found in the present study is within the range
of one to five found in other dipterans studied. In only
one dipteran have dendrites been found to branch in
these sensilla (in A. stephensi, Boo and McIver 1976).
The mpg sensilla found here were also shorter than most
by about half, giving them a stout appearance. As in
comparable sensilla previously studied, the dendritic
 HOOD HENDERSON AND WELLINGTON
sheath in this mpg sensillum extended all or part of the
way up into the peg lu,men.
Groove-surfaced mp sensilla are a common feature on
dipteran antennae, whether these antennae are bulbous
as in the syrphid, or flagellar as in mosquitoes and
blackflies (Boo and McIver 1976; McIver 1974; Mercer
and McIver 1973). The functions of grooved pegs have
been studied neurophysiologically in mosquitoes. Kel-
logg (1970) found that grooved pegs of A. aegypti
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responded to ammonia, anisole, and to water vapour.
This latter observation, however, could not be con-
firmed for either males or females by Davis (1977) or
Davis and Sokolove (1976). In females, the mpg
sensillum has responded to lactic acid (Davis and
Sokolove 1976), fatty acids and essential oils (of
floral scents) (Lacher 1967), and commercial repellents
(Davis and Rebert 1972). In males, this same sensillum
did not respond to the repellents (Davis 1977). Blunt-
tipped type I1 sensilla trichodea in A. aegypti females
were most responsive to chemicals associated with the
oviposition site (Davis 1976) while in males, they were
most sensitive to several chemical stimuli associated
with the host plant (Davis 1977). Morphologically
similar types of sensilla, therefore, do not necessarily
For personal use only.
function similarly.
Thick-walled, multiporous sensilla
The thickness of the cuticular walls of these sensilla is
not much greater than those of the other multiporous
sensilla on the antennae (0.18 pm as opposed to 0.15
pm). The difference arises from the form of the pores.
Because of the area taken up by the bell-shaped inner
pore (see fig. 4D) in the mpp types I and I1 sensilla,
many parts of the cuticle are much thinner than the
reported mean thickness. In contrast, the pores were
fewer and much narrower throughout their length in the
"thick-walled" sensilla, so that the thickness of most
parts of the intervening cuticle is close to the mean value
(see Fig. 3C). In fact, our "thick-walled" mppt sensilla
fall just short of the range given by Zacharuk (1980) for
wall thickness of this type of sensillum (0.2-1.0 km).
Although this mppt sensillum was not tapered to a
point, it appears from the literature that, in other ways, it
is most similar to the sensilla trichodea of other authors.
These sensilla trichodea tend to be "hairs," sometimes
pointed, sometimes blunt, and often curved. Uniporous
sensilla are sometimes included in this category but only
those mppt sensilla reported for dipterans are considered
in this discussion. Lengths of these sensilla vary, from
11 pm (A. aegypti, McIver 1978) to 83 pm (Phormia
regina, Dethier et al. 1963) and often one species has
two or more lengths (Lewis 1971;McIver 1978; McIver
and Siemicki 1979).
Dendrites in this sensillum were unbranched. They
have been reported branched (Bay and Pitts 1976;
3 183
McIver 1978; McIver and Siemicki 1979) and unbranch-
ed (Dethier et al. 1963; Lewis 1971; White and Bay
1980) in comparable sensilla. In the present study the
pore channel was the same diameter throughout (ca.
22.2nm) but this is usually not the case in other mppt
sensilla. White and Bay (1980) reported a V-shaped
channel widening to the interior in Haematobium
irritans irritans, as did Bay and Pitts (1976) for M .
autumnalis. The absence of pore tubules noted in
syrphids was also recorded in A. aegypti (McIver 1978;
McIver and Siemicki 1979) but tubules were present in
H. I. irritans (White and Bay 1980) and M. autumnalis
(Bay and Pitts 1976). Even density of pores varies
considerably in the species in which it has been reported
(2-20/pm2, Zacharuk 1980). Clearly, this type of
sensillum, for which we have least information, is also
the most variable in the literature. Without further
speculation, the porous nature of the cuticle of these
sensilla classes them as olfactory (Zacharuk 1980).
Electroantennogrammes
Oviposition sites are characterized by a range of
chemical stimuli of which honeydew has been accorded
most credit as the source of olfactory stimulation for
ovipositing syrphids (Bombosc h and Volk 1966; Dixon
1959; Schneider 1969). The recent work of Hagen et al.
(1976) and van Emden and Hagen (1976) on green
lacewings suggests that the actual attractants are two
components of honeydew, tryptophan and indoleacetal-
dehyde. The absence of a definitive EAG response to
honeydew in these experiments with M. venablesi and
E. volucris therefore was somewhat surprising, though
it was confirmed by the insensitivity of the antenna to the
components of honeydew tested, tryptophan, indoleal-
dehyde, and indoleacetaldehyde. The EAG findings -
were contrary to the observed responses, however
slight, of mated females in the olfactometer (Hood
Henderson 1981) to a mixture of tryptophan and
indoleacetaldehyde. Although no EAG has been per-
formed on green lacewings, the work af van Emden and
Hagen ( 1976) strongly suggests the presence of antenna1
olfactory sensilla sensitive to honeydew components.
At least two possibilities exist for the lack of
response. Firstly, syrphids may detect honeydew using
sensilla other than those in the antenna, or secondly, that
honeydew is detected by the antenna but the EAG
method is not adequate to demonstrate this. The site of
reception of information from tryptophan and indole-
acetaldehyde could then be olfactory sensilla elsewhere
on the body or possibly gustatory sensilla sensitive
enough to respond to air-borne molecules prior to
contact with the source. This additional capacity is
known to occur in some contact chemoreceptors (Za-
charuk 1980). Although gustatory ovipositor hairs have
responded to these compounds (i.e., honeydew, tryp-
 3184 C A N . J. ZOOL. VOL. 60, 1982
tophan, indoleacetaldehyde; Hood Henderson 1982),
the method used could not detect nervous activity prior
to contact of the hair tip with the test solution. Possible
olfactory sensitivity of these hairs remains to be investi-
gated. The second possibility is that the EAG response
to honeydew, however doubtful, was in fact real. The
relationship between magnitude of an EAG response
and behaviour may not be proportional. Similarily,
Can. J. Zool. Downloaded from www.nrcresearchpress.com by Université de Sherbrooke on 11/21/12
perception of a stimulus by an insect is not necessarily
the same as reception of the stimulus at the antennal site.
The absence of an EAG response to tryptophan and
indoleacetaldehyde despite a slight behavioural re-
sponse in the olfactometer (Hood Henderson 1981) may
be an example of this. It is possible that if single
sensillum recordings could be made of the various
antennal sensilla, a specific response to honeydew and
its components may be found.
Honeydew is not the only component of the oviposi-
tion complex, however. In olfactometer trials, the
stimulus was not complete without the plant (Hood
Henderson 1981). The sensory impact of host-plant
odours is one of the first and most important triggers
setting off the feeding process of a phytophagous insect
For personal use only.
(Schoonhoven 1968). All of the common green plant
volatile substances tested here induced a response by the
antenna of the aphidophagous M. venablesi, just as they
have for many kinds of phytophagous insects (Visser
1979). Most of the volatile substances tested with
syrphid antennae were straight chain, 6-carbon saturated
and unsaturated alcohols formed by oxidative degrada-
tion of plant lipids. They have been reported as volatile
components of numerous plant species in various
families (Visser and Ave 1978). With evidence that
common green plant emanations are exploited by other
insects; with behavioural evidence that some syrphids
use plant cues almost exclusively for locating oviposi-
tion sites (Chandler 1968a), and with the positive EAG
results herein described, it is reasonable to expect that
aphidophagous syrphids have the capacity to detect and
in fact utilize volatile green plant substances. That they
did not respond to crushed broad bean in olfactometer
trials (Hood Henderson 1981) suggests that some plant
odours by themselves may not be a sufficient stimulus to
elicit a complete behavioural response in these species.
Although the respective EAG responses to crushed
carnation petals and crushed aphids may have been
partly due to flower and aphid odours, they were more
probably due to the small concentrations of the same
green plant substances which elicited the earlier anten-
nal responses. Both stimuli would be expected to
contain these compounds.
The EAG response to methylsalicylate is probably
important because this compound is found in plants,
though it is not so common as the volatile green plant
substances. Unlike these compounds, its chemical core
structure is cyclic, rather than straight chained. The only
structural element it has in common with them is an
exposed hydroxyl group, which may be an important
requirement at receptor sites. For example, Visser
(1979) changed the position of the terminal hydroxyl
group during tests of several short-chain alcohols and
aldehydes on the Colorado potato beetle, and found that
the EAG response, while still present, was much
reduced after the change. If the exposed hydroxyl group
is not involved, then the strong odour of methylsalicyl-
ate might be readily detected by a more general chemical
sense. The form of the response, which was different
from that of other chemicals tested (Fig. 5K), provides
some evidence for this alternative possibility. When
exposed to methylsalicylate, the stimulated nerve took
much longer to recover, indicating that this particular
molecule continued to stimulate the receptor site longer
than the other molecules. Weak responses to methyl-
salicylate have been demonstrated in antennae of the
Colorado potato beetle (Visser 1979) and in the blunt-
tipped sensilla trichodea, type 11, of female A . aegypti
(Davis 1976).
The antenna of aphidophagous syrphids is indeed a
very important and perhaps exclusively olfactory organ.
By the number and diversity of sensilla, it must have a
large range of sensitivities. However, the results of this
study suggest that while volatile plant odours are within
that range, honeydew may not be. Chandler ( 1 9 6 8 ~ )
suggested that, in the syrphids' evolution, the
phytophagous habit was the oldest, whereas the
entomophagous habit was more recent. He suggested
that the response to host plants is normally masked in
truly aphidophagous species. This masking may have
been demonstrated by the lack of response by syrphids to
whole or crushed plants in the olfactometer (Hood
Henderson 1981). Its continued presence in aphido-
phagous forms is evidenced by the breaking down of this
masking under certain conditions such as ageing or
oviposition site deprivation. The EAG results in this
study support his observation that host plant recognition
without aphids does occur in entomophagous species
and that host plant factors are important even for species
that normally will not oviposit without aphids.
There may, of course, be other emanations related to
aphids to which these syrphids respond, but this study
did not test them. The EAG response to crushed aphids,
for instance, merits further study to determine whether
there was actually a response to the aphids or to ingested
plant material. To investigate further the possibility of a
response to honeydew, single sensillum recordings of
antennal sensilla would be necessary.
Host-plant odours (and perhaps aphid odours) along
with plant form and colour are perhaps the sensory cues
that operate at a distance to bring a female into close
proximity of her preferred oviposition sites. Once a
 HOOD HENDERSON AND WELLINGTON 3 185

habitat has been recognised, closer observation is called 1968d. Height

for, in a hover search. Here also, olfactory and visual
cues are probably important. Honeydew may not
become important until the female lands to investigate
with her tarsi, labellum, and ovipositor. The ovipositor
is sensitive to honeydew and some of its components,
CHU-WANG,
namely tryptophan, indoleacetaldehyde , alanine , suc-
rose, and water (Hood Henderson 1982) supporting our
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- -preferences for oviposition of
aphidophagous Syrphidae (Diptera). ~ n t o m o ~ h a ~13:
a,
187-195.
1969. Locomotory behaviour of first instar larvae of
aphidophagous Syrphidae (Diptera) after contact with
aphids. Anim. Behav. 17: 673-678.
I., R. C. AXTELL,and D. L. K L ~ N E1975. .
Antennal and palpal sensilla of the sandfly Culicoides furens
(Poey) (Diptera: Ceratopogonidae). Int . J. Insect Morphol.

suggestion that the importance of honeydew is in Embryol. 4: 131-149.

close-range searching rather than in the initial scanning DAVIS,E. E. 1976. A receptor sensitive to oviposition site
search for an oviposition site. attractantson the antennae of the mosquito Aedes aegypti. J.
Insect Physiol. 22: 137 1- 1376.
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University of Alberta, for facilities to complete the sensitive receptors on the antennae of the mosquito, Aedes
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Toronto, for critically reading the manuscript, and to DETHIER, V. G., J. R. LARSEN, and J. R. ADAMS.1963. The
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