Specialized olfactory receptor neurons mediating intra- and interspecific chemical communication in leafminer moths Eriocrania spp. (Lepidoptera: Eriocraniidae)
1
Department of Ecology, Lund University, SE-223 62 Lund, Sweden
2
Department of Crop Science, Chemical Ecology, Swedish University of
Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden
3
Department of Zoology, Lund University, SE-223 62 Lund, Sweden
4
Section of Ecology, Biological Faculty, University of Turku, FIN-20014
Turku, Finland
5
Institute of Organic Chemistry, University of Hamburg, Martin
Luther-King-Platz 6, D-20146, Hamburg, Germany
*
Present address: Department of Crop Science, Chemical Ecology, Swedish
University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden
Present address: Department of Crop Science, Chemical Ecology, Swedish
University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden
(e-mail:mattias.larsson{at}vv.slu.se )
Accepted 21 January 2002
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Summary |
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Field-trapping showed that type 3 receptor neurons mediate strongly antagonistic effects of (R)-heptan-2-ol and (R,Z)-4-hepten-2-ol on E. semipurpurella, while nonan-2-one should possibly be included as a synergist in the sex pheromone blend of this species. The attraction of E. cicatricella and E. sparrmannella to compounds mixed with the pheromone blend of E. semipurpurella shows that the pheromone components of E. semipurpurella have little or no antagonistic effects on these species.
The morphology and physiology of eriocraniid pheromone sensilla are very similar to those found in the order Trichoptera (caddisflies), suggesting a homology between pheromone detection systems in the two sister orders Lepidoptera and Trichoptera.
Key words: pheromone, single sensillum, receptor neurone, antagonist, enantiomer, chirality, behaviour, leafminer moth, Eriocrania spp
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Introduction |
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In ditrysian moths, comprising the majority of moth species, the male
pheromone detection apparatus has been thoroughly studied. These moths use
specialized olfactory receptor neurons, housed in long sensilla trichodea, to
detect pheromone components released by females. Each component of the female
pheromone blend is typically detected by a corresponding type of receptor
neuron on the male antenna (Boeckh,
1984). Except for electroantennographic recordings, no
electrophysiological investigations of pheromone receptor neurons have been
performed in the Eriocraniidae or other primitive moth families.
Some single-cell data on pheromone reception are available from the sister
order Trichoptera. Males and females of the caddisfly Rhyacophila
nubila have receptor neurons responding to heptan-2-one, heptan-2-ol,
nonan-2-one and nonan-2-ol (Larsson and
Hansson, 1998), which have been identified from the female sternal
glands (Löfstedt et al.,
1994
). The behavioural significance of these compounds has not
been established in R. nubila however. In the related species
Rhyacophila fasciata, in which pheromonal activity has been confirmed
(Löfstedt et al., 1994
),
both sexes also have receptor neurons with response properties similar to
those found in R. nubila (M. C. Larsson and B. S. Hansson,
unpublished results). In both species, the receptor neurons have a high
ability for chiral discrimination, although the behavioural effects of the
chirality of the compounds are unknown.
We have performed an electrophysiological and morphological investigation of pheromone sensilla in the eriocraniid moth Eriocrania semipurpurella. The purpose of our investigation was to study pheromone detection in a primitive moth and to make a comparison with what is known about the detection of structurally similar compounds in caddisflies. As olfactory stimuli, we used a set of ketones and secondary alcohols that function as semiochemicals in E. semipurpurella and the sympatric species E. cicatricella, E. sparrmannella and E. sangii. The results from the single-sensillum study prompted us to perform field-trapping experiments to elucidate the behavioural role that the electrophysiologically active compounds play in the chemical communication of Eriocrania spp.
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Materials and methods |
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Collection of experimental animals
For electrophysiological studies, we caught live E. semipurpurella
males in hollow containers baited with a blend of 50µg of
(R,Z)-6-nonen-2-ol and 50µg of (S,Z)-6-nonen-2-ol. The
animals were caught in 1995, 1996 and 1997 at two field sites with birch
stands outside Lund, Sweden, and outside Turku, Finland. For morphological
studies, we caught E. semipurpurella males in Lund by netting.
Chemicals
The nine compounds used in the electrophysiological and behavioural
experiments are listed in Tables
1 and
2. (R)-heptan-2-ol and
(S)-heptan-2-ol were purchased from Aldrich Chemical Co. The
synthesis of all other compounds followed the procedures described previously,
and chemical and enantiomeric purity were checked by chiral gas chromatography
(Kozlov et al., 1996). The
chemical purity of all compounds was at least 99%. The enantiomeric excess for
all the chiral compounds was 98% or greater, i.e. no more than 1% of the
antipode was present. The compounds were dissolved in hexane and then diluted
in decadic steps.
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Electron microscopy
For scanning electron microscopy, antennae from male E.
semipurpurella were fixed in 70% ethanol, dehydrated and air-dried. The
antennae were mounted on holders with white glue and sputter-coated with
gold/palladium. The specimens were studied in a JEOL T330 scanning electron
microscope operated at 10kV. For transmission electron microscopy, the
antennae were excised, cut into smaller pieces and immersed in 4%
glutaraldehyde in 0.15 moll-1 cacodylate buffer for 8h.
Postfixation was carried out in 1% osmium tetroxide for 2h. After dehydration,
the specimens were embedded in Epon resin and polymerized. Sections cut on a
diamond knife were stained with uranyl acetate and lead citrate in an LKB
ultrastainer. The sections were examined in a JEOL 1200 EX transmission
electron microscope. Olfactory sensilla were classified according to
morphological criteria, i.e. the structure of pores
(Altner, 1977).
Electrophysiology
Odour stimuli for electrophysiological experiments were prepared by
pipetting 10µl samples of hexane with dissolved compound onto small pieces
of filter paper (approximately 10cmx15 mm) placed in Pasteur pipettes
and letting the solvent evaporate. The amount of compound deposited in each
pipette ranged from 10pg to 100ng in decadic steps for the dose/response
trials. A blank cartridge containing only filter paper plus solvent was also
prepared. For screening, we used 1µg in each pipette. The test stimuli were
kept at -20 °C when they were not in use to minimize evaporation of the
test compounds. Each test cartridge was replaced within 2 days.
For the single-sensillum recordings, moths were restrained in holders cut
from small, plastic micropipette tips (Tamro MedLab, Mölndal, Sweden),
and the head and antennae were fixed with dental wax. A thin silver wire,
serving as a ground electrode, was inserted into the abdomen. Contact was
established with receptor neurons by means of tungsten microelectrodes,
sharpened electrolytically in KNO2-solution and inserted near the
base of olfactory sensilla (Boeckh,
1962). A binocular microscope with up to 300x magnification
and two Leitz micromanipulators were used to position the animals and the
recording electrode.
A charcoal-filtered and humidified air stream was blown over the antenna at a constant velocity of 0.5 m s-1 through a glass tube with the outlet approximately 15 mm from the antenna. Stimulation was performed by inserting the tip of the test pipette into a hole, 15 cm from the outlet of the glass tube, and blowing air (2.5 ml over 0.5 s) through the pipette. The stimulus air puffs were generated by a Syntech SFC-1/b stimulus controller (Hilversum, the Netherlands).
Upon contact with a sensillum (or sensilla), distinguished by spontaneous or penetration-induced action potentials (`spikes') from receptor neurons, we stimulated the antenna with the blank plus all the test compounds at the screening dose. If a neuron responded to any of the test compounds with a change in spike frequency different from that to the blank, a dose/response trial was performed in which all active compounds were presented to the antenna at all doses. All stimuli were delivered by dose level, starting with the lowest dose. At each dose level, the stimuli were delivered at random with an interval of at least 20 s, except at the higher levels, where the stimuli showing the lowest response were delivered first. At these high levels, it was also necessary to allow longer intervals between stimuli to let the neurons recover their normal spontaneous activity. Some neurons were classified only according to their responses to the screening stimuli.
The signal was amplified using a low-pass/high-pass high-impedance amplifier constructed in our laboratory. During the experiments, the neural responses were visualised on an oscilloscope and stored on videotape for later processing. The filtering of the signal through the amplifier did not suffice to remove enough low-frequency noise from the recordings, resulting in low signal-to-noise ratios for action potentials with low amplitudes. The signal from the videotape was therefore filtered a second time through a Syntech UN-06 amplifier with better filtering capacity before being transferred to a Compaq ProLinea 4/66 computer for analysis with the program Syntech Auto Spike v.3.0. The identification of individual neurons was based on differences in the amplitudes of their action potentials. The action potentials were counted, and the net response to a stimulus was calculated as the number of spikes over 1 s after stimulation minus the number of spikes over 1 s before stimulation. The net response to the blank was subtracted to avoid any non-specific responses, for example to the air puff.
Field-trapping
We conducted the field-trapping experiments in 1998, at a field site
outside Lund, using Delta traps. Within each replicate, the traps were
randomly placed at least 5 m apart, suspended 1-2 m above the ground from the
branches of young birch trees. The traps were emptied each day, except at the
end of the second trial (see below), when they were left for a whole week to
catch the last stray moths at the end of the field season. After each sampling
time, the position of each trap was changed to minimize the effects of habitat
heterogeneities. Odour dispensers for field-trapping experiments were prepared
from red rubber septa (Arthur H. Thomas Co.; Catalogue no. 1780-J07) by
pipetting 100 µl samples of hexane containing blends of dissolved compounds
onto each rubber septum.
During the first trial, conducted on 23-28 April, the effects of adding electrophysiologically active compounds to the previously reported pheromone blend of E. semipurpurella were tested. In each replicate, a reference bait containing 50 µg each of (R,Z)-6-nonen-2-ol and (S,Z)-6-nonen-2-ol was compared with six other baits containing the same blend plus 5 µg of another compound. The other compounds tested were (R)-heptan-2-ol, (S)-heptan-2-ol, (R,Z)-4-hepten-2-ol, (S,Z)-4-hepten-2-ol, (Z)-6-nonen-2-one and nonan-2-one. Treatments were compared with the reference bait using a MannWhitney U-test for pairwise comparisons.
In the second trial, conducted from 29 April to 7 May, the effects of adding different amounts of compounds to the pheromone blend of E. semipurpurella were tested. The same type of reference bait as in the first trial was used, while seven other baits containing the pheromone blend plus (R)-heptan-2-ol (0.5 and 5 µg), (S,Z)-4-hepten-2-ol (0.5, 5 and 50 µg), (Z)-6-nonen-2-one (0.5 µg) and nonan-2-one (0.5 µg) were tested. All treatments were compared using a KruskalWallis analysis of variance followed by a MannWhitney U-test for pair-wise comparisons.
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Results |
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Auricillic sensilla were the most numerous, with their leaf-shaped cuticular hairs arranged along the whole antennal surface. Each auricillic sensillum was 7-10 µm long and 4-5 µm wide and had a short shaft connecting it to the antennal surface. Its surface was provided with longitudinal furrows in which the pores were found (Fig. 1A). The numerous pores were found on both sides of the flattened cuticular hair. The cuticular walls of the hair had a maximal thickness of approximately 100 nm, and the pores were marked by invaginated less-electron-dense areas of the hair cuticle. Each auricillic sensillum was innervated by three sensory cells (N=27), with branched dendritic outer segments within the hair structure. In cross sections of the hairs, there were approximately 100 branches with a diameter of approximately 50 nm (Fig. 1C).
The trichoid sensilla were found only on the ventral part of the antennae in groups of approximately 10 on the proximal part of each flagellomere. The slightly curved cuticular hairs were approximately 25 µm long, and their distal parts were bent towards the antennal surface (Fig. 1B). The cuticular walls (thickness approximately 120 nm) were provided with pores, but the density of pores was considerably lower than in the auricillic sensilla. Each trichoid sensillum was innervated by two sensory cells (N=10), which had branched dendritic outer segments. The branching of the dendritic outer segments was moderate compared with that of the auricillic sensilla: in cross sections, there were 4-5 branches in the middle part of the hair (Fig. 1C).
Electrophysiology
We obtained 83 recordings from 26 male moths that lasted long enough for a
characterization with all screening stimuli. Contacts were obtained mainly
from the ventral side of each antennae, in the medial parts of the
flagellomeres. The sensilla from which we recorded could not be identified
with certainty in the light microscope, but the location of the recording
electrode showed that the recordings stemmed from auricillic sensilla. In each
recording, we simultaneously registered spikes from 1-3 neurons with different
spike amplitudes. The smaller spikes could not be clearly distinguished during
the experiments, but after filtering through a second amplifier they were
clearly distinguishable from the baseline noise
(Fig. 2). All responses to test
stimuli were characterized by an increase in spike frequency relative to the
spontaneous level of activity. We recorded from 139 receptor neurons, of which
87 responded to one or several of our test stimuli with a higher spike
frequency than to the blank. Blank stimuli generally elicited no spikes or
very few spikes above the spontaneous level of activity. Responding neurons
could all be grouped into five separate types depending on their response
characteristics (Fig. 3;
Table 2). We found all five
types of receptor neuron in months from both Sweden and Finland.
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The two most common types of receptor neuron, designated type 1 and type 2, responded to the two pheromone components of E. semipurpurella. Type 1 neurons responded selectively to (R,Z)-6-nonen-2-ol, while type 2 neurons responded selectively to (S,Z)-6-nonen-2-ol. Both types of receptor neuron had a high ability for chiral discrimination, with the sensitivity to the key compound being at least 100 times higher than to the respective enantiomer (Fig. 3; Table 2).
Another set of receptor neurons, designated type 3, responded identically to two different compounds, (R)-heptan-2-ol and (R,Z)-4-hepten-2-ol, which have not been identified in extracts of E. semipurpurella. The type 3 neurons had an ability for chiral discrimination similar to that of the type 1 and type 2 neurons, i.e. a 100-fold difference in sensitivity between the two key compounds and their respective enantiomers (Fig. 3; Table 2).
Type 4 neurons responded to both nine-carbon ketones, with a preference for (Z)-6-nonen-2-one over nonan-2-one, while type 5 neurons responded slightly to nonan-2-one alone, but only at the highest doses (100 ng to 1 µg).
Specific combinations of 2-3 neurons were frequently encountered (Table 3). Presumably these neurons resided in the same sensillum, although some cases of recordings from more than one sensillum cannot be excluded. Neurons may also occasionally have been damaged by the penetrating electrode and therefore never recorded or not responded. When two or more neurons were found together, the relationship between their spike amplitudes was usually, but not always, similar between different recordings. Receptor neurons for the two pheromone components usually had the highest spike amplitudes, with type 1>type 2, while other physiological types had lower amplitudes. Non-responding neurons typically had the lowest spike amplitudes (Table 3).
Field-trapping
In the first series of field-trapping experiments, (R)-heptan-2-ol
and (R,Z)-4-hepten-2-ol dramatically suppressed the catch of E.
semipurpurella males when added to the E. semipurpurella
pheromone blend. Other compounds had no significant effects, although traps
containing one of the two corresponding (S)-enantiomers or
nonan-2-one caught high numbers of E. semipurpurella males compared
with the reference traps (Fig.
4).
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In the later series of field-trapping experiments, testing different doses of the potentially active compounds, (R)-heptan-2-ol turned out to be antagonistic to E. semipurpurella at the 5 µg dose (ratios 1:1:0.1) but not at the 0.5 µg dose (ratios 1:1:0.01). (S,Z)-4-hepten-2-ol had no significant effect at 0.5 µg or 5 µg, but significantly reduced the catch at the 50 µg dose. The ketone (Z)-6-nonen-2-one had no effect, while 0.5 µg of nonan-2-one significantly increased the trap catch when added to the blend (Fig. 5).
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In the first series of field-trapping tests, a large number of E. cicatricella Zett. males were caught in the traps with 5 µg of (R,Z)-4-hepten-2-ol (Fig. 4). In the second series, several males of this species were also caught in the traps with 50 µg of (S,Z)-4-hepten-2-ol (Fig. 5). During the second series of field trials, E. cicatricella were caught primarily at the beginning of this series. No E. cicatricella males were caught during May (data not shown).
The addition of (S,Z)-4-hepten-2-ol to the blend had a dramatic effect on the species E. sparrmannella Bosc., which had not been caught in traps containing this compound during the first series of trials (Figs 4, 5). Increasing the dose of (S,Z)-4-hepten-2-ol from 0.5 to 50 µg led to a steep increase in the catch of E. sparrmannella males. E. sparrmannella males were predominantly caught during the later part of the second series of field trials (data not shown).
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Discussion |
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The olfactory receptor neurons found here explain the detection mechanisms
behind electroantennographic responses to female extracts previously measured
from male antennae (Kozlov et al.,
1996). In E. semipurpurella, each of the two most common
types of receptor neuron (type 1 and type 2) responded to one of the two
identified pheromone components, (R,Z)-6-nonen-2-ol and
(S,Z)-6-nonen-2-ol, respectively. These two types of neuron perform
the chiral discrimination necessary to differentiate the pheromone blends of
several `pheromone races' or sibling species within E. semipurpurella
(sensu lato). Both types of pheromone receptor neuron had a high
ability for chiral discrimination, with the key stimulus being at least 100
times more potent than its respective enantiomer. The dose/response
characteristics of the pheromone receptor neurons in E.
semipurpurella closely match those of receptor neurons in the two
caddisfly species R. nubila and R. fasciata, in which the
same or structurally related compounds were tested
(Larsson and Hansson, 1998
; M.
C. Larsson and B. S. Hansson, unpublished results). The ability for chiral
discrimination is high and appears to be of approximately the same magnitude
in the Rhyacophila and Eriocrania species. However,
responses to more than one enantiomer could be caused by enantiomeric
impurities in the stimuli, thus reflecting the purity of the test compounds
rather than the true discriminatory abilities of the receptor neurons, which
in reality could be considerably higher. Studies of pheromone detection in
scarab beetles, using enantiomers of exceptionally high purity, have indeed
demonstrated chiral receptor neurons in which the corresponding enantiomers
are almost completely inactive (Wojtasek
et al., 1998
; Larsson et al.,
1999
).
The type 3 receptor neurons identified in our study detect secondary alcohols not present in the pheromone blend of E. semipurpurella, but which are part of the pheromone blend of the sympatric species E. cicatricella. These neurons respond identically to the two compounds (R)-heptan-2-ol and (R,Z)-4-hepten-2-ol. Nevertheless, they have the same ability for chiral discrimination as the type 1 and type 2 neurons, i.e. both key stimuli are 100 times more potent than their respective (S)-enantiomers (but see above). The field-trapping tests showed that both (R)-heptan-2-ol and (R,Z)-4-hepten-2-ol work as pheromone antagonists, strongly suppressing the attraction of E. semipurpurella to its pheromone blend when added at a dose of 5 µg (ratios 1:1:0.1) (Figs 4, 5).
Inhibition of pheromone attraction by compounds not present in the
conspecific pheromone blend is a common phenomenon among insects, e.g. in the
noctuid moths Trichoplusia ni and Pseudoplusia includens
(Linn et al., 1988;
Grant et al., 1988
). These
antagonist compounds have often been found in pheromone blends of sympatric
species sharing some pheromone components. Pheromone antagonists are detected
by specialized receptor neurons that apparently function as fail-safes to
avoid attraction between heterospecifics in cases where mistakes could easily
be made. Examples of specialized antagonist detectors can be found among
noctuid moths (Grant et al.,
1988
; Almaas and Mustaparta,
1991
; Cossé et al.,
1998
) and among beetles from several families (Mustaparta et al.,
1977
,
1980
;
Okada et al., 1992
,
Wojtasek et al., 1998
), in
which chirality often determines the difference between pheromone components
and antagonists. It is worth noting that, in some cases, heterospecific
pheromone components can be synergistic, as when bark beetles or longhorn
beetles are attracted to heterospecific bark beetle semiochemicals that may
indicate weakened tree hosts
(Tømmerås et al.,
1984
; Allison et al.,
2001
).
The pheromone blends of E. semipurpurella and E.
cicatricella are based on different compounds, and there seems to be no
need for additional heterospecific antagonists to avoid cross-attraction. The
specialized receptor neurons and the antagonistic effect on attraction may,
however, have evolved primarily for the avoidance of other Eriocrania
species whose pheromone blends are not yet known. Antagonistic effects of
heterospecific pheromone components are not always reciprocal, as is apparent
in the study of Grant et al.
(1988) and the present study.
Both E. cicatricella and E. sparrmannella presumably lack
receptor neurons for E. semipurpurella pheromone components because
they are highly attracted to synthetic blends in which their own specific
attractants make up only a fraction of the total blend. Kozlov et al.
(1996
) showed that
non-reciprocal inhibitory effects may exist between E. cicatricella
and E. sparrmannella, however.
The antagonist neurons found in E. semipurpurella share some
features with antagonist neurons in other insect species. These neurons often
have broader response spectra than pheromone neurons, which could represent an
economic way of detecting several compounds mediating the same stop signal
(Wojtasek et al., 1998;
Baker et al., 1998
;
Cossé et al., 1998
).
Antagonist neurons are often co-localized with pheromone neurons in the same
sensilla. This may have an adaptive significance for the precise timing
necessary to separate odour filaments of different origin in the air
(Baker et al., 1998
;
Fadamiro et al., 1999
).
Conceivably, the type 3 neurons in our investigation may actually be two
neurons with identical spike amplitudes but different key stimuli. At the time
of the dose/response trials, we did not perform reciprocal adaptation
experiments since the nature of the type 3 neurons became firmly established
only through additional filtering during data analysis. However, the absence
of double spikes and other interference in the spike pattern of the type 3
neurons (Fig. 2) and the fact
that both physiological recordings and morphological studies of sensilla
auricillica revealed a maximum of three neurons strongly suggest that these
recordings stem from single neurons.
Eriocrania moths sometimes appear to make mistakes in chiral discrimination, in spite of their selective receptor neurons, although the concentrations applied here may have exceeded those that the moths would normally encounter in nature. E. cicatricella was somewhat attracted to 50 µg doses of (S,Z)-4-hepten-2-ol, the antipode of its pheromone component (Fig. 5). The same compound acted as an antagonist to E. semipurpurella when added to the pheromone blend at a dose of 50µg (Fig. 5). This matches the physiological response properties of the type 3 neurons, in that high doses of (S,Z)-4-hepten-2-ol have electrophysiological as well as behavioural effects. An alternative explanation for the electrophysiological and/or behavioural effects of (S,Z)-4-hepten-2-ol in these two moth species could be the presence of the enantiomer (R,Z)-4-hepten-2-ol as an impurity (see above).
Two types of receptor neuron (types 4 and 5) responded to ketones found in
the pheromone glands of female E. semipurpurella. Type 4 receptor
neurons responded to both (Z)-6-nonen-2-one and nonen-2-one (with
lower sensitivity). Type 5 neurons responded to nonen-2-one, but only at high
doses, which adds some doubt as to whether this compound is really the key
stimulus for these neurons. The role of the two ketones in the pheromone
communication of E. semipurpurella is unclear. The ketones are the
most abundant compounds in the pheromone gland extracts of E.
semipurpurella and E. sangii. When added to the blend according
to the ratios found in the females, the ketones act as inhibitors to E.
sangii and apparently to E. semipurpurella as well
(Kozlov et al., 1996). Our
field-trapping data indicate that nonan-2-one, but not
(Z)-6-nonen-2-one, could actually be a synergist to E.
semipurpurella at low doses, which is difficult to explain in the context
of our electrophysiological results unless we postulate the existence of
other, as yet unidentified, types of receptor neuron. A definite answer to
whether any of the ketones is a true pheromone component requires a
re-examination of the pheromone blend, including measurements of the amounts
actually released from females.
Our study has revealed a complex interplay between various semiochemicals taking place within and among different Eriocrania species, and it has shown how this interplay may be mediated at the level of the antennal receptor neurons. The results of our field-trapping studies further suggest a temporal separation between different Eriocrania species, with E. sparrmannella appearing later in the season than E. semipurpurella and E. cicatricella. Different `pheromone races' of E. semipurpurella have also demonstrated slight temporal shifts during other experiments in Turku (P. Metcalfe, M. V. Kozlov, W. Francke and C. Löfstedt, unpublished data). The evidence obtained here suggests a close homology between Trichoptera and primitive Lepidoptera not only in their systems of pheromone release but also in the antennal systems responsible for pheromone detection. As new gland structures and pheromone components arose later in more advanced Lepidoptera, so the task of pheromone detection may have shifted to new types of sensilla housing different physiological types of receptor neuron. The possibility that these two shifts occurred in parallel is intriguing but not yet substantiated.
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Acknowledgments |
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